AMFReview

Environmental Pollution 268 (2021) 115549
Contents lists available at ScienceDirect
Environmental Pollution
journal homepage: www.elsevier.com/locate/envpol
Review
Sustainable improvement of soil health utilizing biochar and

arbuscular mycorrhizal fungi: A review
Nihal Gujre a, 1, Ankit Soni a, Latha Rangan b, Daniel C.W. Tsang c, Sudip Mitra a, 1, *
a
Agro-ecotechnology Laboratory, Centre for Rural Technology, Indian Institute of Technology Guwahati (IITG), Guwahati, Assam 781039, India
b
Department of Biosciences and Bioengineering, Indian Institute of Technology Guwahati (IITG), Guwahati, Assam 781039, India
c
Department of Civil and Environmental Engineering, The Hong Kong Polytechnic University, Hung Hom, Kowloon, Hong Kong, China
a r t i c l e i n f o a b s t r a c t
Article history: Conservation of soil health and crop productivity is the central theme for sustainable agriculture prac-
Received 8 April 2020 tices. It is unrealistic to expect that the burgeoning crop production demands will be met by a soil
Received in revised form ecosystem that is increasingly unhealthy and constrained. Therefore, the present review is focused on
18 July 2020
soil amendment techniques, using biochar in combination with arbuscular mycorrhizal fungi (AMF),
Accepted 8 August 2020
Available online 28 August 2020
which is an indispensable biotic component that maintains plant-soil continuum. Globally significant
progress has been made in elucidating the physical and chemical properties of biochar; along with its
This paper has been recommended for role in carbon sequestration. Similarly, research advances on AMF include its evolutionary background,
€ rg Rinklebe.
acceptance by Jo functions, and vital roles in the soil ecosystem. The present review deliberates on the premise that
biochar and AMF have the potential to become cardinal to management of agro-ecosystems. The wider
Keywords: perspectives of various agronomical and environmental backgrounds are discussed. The present state of
Arbuscular mycorrhizal fungi knowledge, different aspects and limitations of combined biochar and AMF applications (BC þ AMF),
Biochar mechanisms of interaction between biochar and AMF, effects on plant growth, challenges and future
Soil amendment
opportunities of BC þ AMF applications are critically reviewed. Given the severely constrained nature of
Soil quality
soil health, the roles of BC þ AMF in agriculture, bioremediation and ecology have also been examined. In
Sustainable agriculture
spite of the potential benefits, the functionality and dynamics of BC þ AMF in soil are far from being fully
elucidated.
© 2020 Elsevier Ltd. All rights reserved.
1. Introduction example, humungous pressure is brought to bear on 2.4% of land

area occupied by 18% and 15% of global human and livestock pop-
The life-sustaining role of soil in agriculture and food security is ulation, respectively (Pal et al., 2019). A decrease in crop production
undermined by the rapid worldwide degradation of surface soil efficiency is also confronted in China due to heavy metals (HMs)
through increased erosion, salinity, acidification, and compaction contamination of more than 2 107 ha of farmland; 16.1% of this
(Scholes et al., 2018). Degradation is primarily driven by soil area exceeds designated limits for soil pollution (Palansooriya et al.,
pollution, improper management practices, extreme climate 2020). These examples of challenging circumstances, from the
events, lack of technological innovations and resilience systems world’s most densely populated countries, endorse the deployment
(Shao et al., 2019; Van Leeuwen et al., 2019). The consequent eco- of environmentally friendly, economically viable, and sustainable
nomic and social ramifications result in slower economic growth, technologies. Biochar along with AMF is a potentially achievable,
heightened food insecurity, increased poverty, and livelihood appropriate, and advantageous amendment for soil quality reme-
vulnerability; thus disrupting sustained agricultural production in diation and improvement (Fang et al., 2018; O’Connor et al., 2018).
the developing regions, especially in the tropical regimes (Lomba Across the globe, BC þ AMF have gained much attention for their
et al., 2019; Shao et al., 2019; Smetanova et al., 2019). In India, for wide range of applications particularly in improving nutrients
cycling (Castan~ eda et al., 2020; Moland et al., 2018), drought-
resistant (Hashem et al., 2019) and restoration of soil quality
(Gonza lez-Cha
vez et al., 2017; Ohsowski et al., 2018). Numerous
* Corresponding author.
E-mail addresses: sudipmitra@yahoo.com, sudipmitra@iitg.ac.in (S. Mitra).
experiments have been carried out to assess the BC þ AMF effects
1
Equal contribution. on crops which can be influenced by various biochar properties, i.e.,
https://doi.org/10.1016/j.envpol.2020.115549
0269-7491/© 2020 Elsevier Ltd. All rights reserved.
N. Gujre, A. Soni, L. Rangan et al. Environmental Pollution 268 (2021) 115549
pH, residence time, temperature, and surface area (Palansooriya a study indicated an increase of 0.59e1.05 in soil pH after the
et al., 2019; Rafique et al., 2020; Vejvodova et al., 2020; Yang application of biochar from different feedstock (Yuan and Xu, 2010).
et al., 2020). However, BC þ AMF effects on the crop and plants Temperatures of 300e700 C with long residence time are
can be attributed to many other factors, which include crop types, characteristics of slow pyrolysis, whereas fast pyrolysis proceeds at
soil types and microbiological communities present in the soil high heating rate (>700 C) with short residence time of less than
(Azeem et al., 2020; Paymaneh et al., 2018). 10 s. Pore size, a prime component of biochar surface morphology,
Biochar is a carbon-based by-product of biomass pyrolysis in an is also dependent on residence time. Biochar obtained from slow
oxygen-depleted environment, which is commonly used to pyrolysis has increased porosity, higher pH (7), and a greater
improve soil health and mitigate greenhouse gas (GHG) emissions. surface area of 100e800 m2 g1 (Weber and Quicker, 2018). When
Biochar cum fertilizer application can enhance soil quality, plant residence time is increased to 120 min at 500e900 C, the pore size
growth, and nutrition (Li et al., 2019; Palansooriya et al., 2020). increases; but beyond 120 min, it displays a clear reduction in size.
Biochar, with its innate heterogeneity of pores and surface struc- Micrograph assessment revealed pores with honeycomb-like
ture, increases available surface area inside the soil; facilitating structures in certain biochar; possibly induced by entwined bio-
water and gaseous exchange, nutrient recycling, and carbon storage polymers connected by biomolecule structural bonds in feedstock
(Mitra et al., 2016; Ruan et al., 2019; Zheng et al., 2018). The cells (Wu et al., 2016).
structure of biochar also augments the habitats for micro biota Biomass degradation occurs in three stages; the first at less than
within the soil matrix, thus actively aiding soil rejuvenation (Mia 150 C allows evaporation of moisture, light volatile compounds
et al., 2014; Yu et al., 2019). In addition, biochar and its mineral and hemicellulose breakdown. The second ranges from 150 to
composites can effectively remediate the organic and inorganic 400 C causing cellulose break down; and in the third stage,
contaminants present in the soil (Mian et al., 2019; Zhang and Wu, decomposition of lignin and combustion of the residual char are
2017). triggered by temperatures >400 C (Narzari et al., 2017).
AMF, among diverse soil microbiota (bacteria, fungi, algae, Application of biochar is predominantly dictated by its surface
archaea, arthropods, nematodes, protozoa, and other in- morphology (Ho et al., 2017; Mitra et al., 2016; Premarathna et al.,
vertebrates), are remarkably significant regulators of soil produc- 2019). Biochar with wider surface area and pores offer potential
tivity (Lilleskov et al., 2019; Lenoir et al., 2016). Highly evolved and sites for soil microbiota, creating diverse microbial community
mutualistic relationships between soil fungi and plant roots are structures inside the soil (Lehmann et al., 2011; Jaafar et al., 2014).
formed by AMF. In the pedosphere, the host plant, fungus The porous structure offers rich source of carbon, nutrient, and
phenology, soil conditions, and environmental factors governing water for microbial growth and reproduction (Yu et al., 2019). The
this mutualistic relationship. The extended surface area provided enlarged pore surface is thus helpful for soil nutrition retention,
by the dense network of AMF mycelia improve nutrient acquisition enhanced nutrient transfer to plants, and concomitant prevention
uptake by plant roots and facilitate soil aggregation (Lenoir et al., of nutrient loss from agricultural soil (Pradhan et al., 2018).
2016). Recent researches have been carried out for the identifica- For soil applications biochar with low ash content and high
tion, isolation, and culture of mycorrhiza; observational studies surface area is preferred; although the relationship between bio-
(Delavaux et al., 2019; Kokkoris et al., 2019), field trials (Adeyemi char properties and its applicability as a soil amendment is not
et al., 2020; Gu et al., 2020; Thirkell et al., 2019), greenhouse ex- conclusive (Ahmad et al., 2014). Biochar alone or in combination
periments (Bourles et al., 2020; Shamshiri et al., 2020), and other with some other manure is projected to have a wide range of ap-
related experiments (Tamayo et al., 2018; Teutscherova et al., 2019). plications; particularly in adsorption of HMs (Tsang et al., 2014),
A holistic review of BC þ AMF for sustainable soil health will water and wastewater treatment (Sun et al., 2019; Wang et al.,
provide a pivotal document for the scientific community and in- 2019a; Zhang et al., 2018), and reclamation of mines (Gwenzi
dustrial/government stakeholders. Therefore, the present review et al., 2015; Ippolito et al., 2019; Tsang et al., 2014).
will discuss and critically analyze the individual and complemen-
tary roles of biochar and AMF in improving soil health, enhancing 2.2. Biochar and its chemical properties
crop yield, remediation of soil contaminants, and enhancing live-
lihood opportunities. Infographics are provided to augment Chemical properties of biochar are pH-dependent, which ulti-
concept and mechanism assimilation. The contents (i) summarize mately increases CEC (Cation exchange capacity) (Ahmad et al.,
the recent data regarding the different forms of biochar along with 2014). Fig. 1 illustrates chemical changes post biochar addition to
their physical and chemical properties, (ii) address the functional- soil. The elemental analysis of biochar reveals that it mainly con-
ities and dynamics of biochar and AMF, and (iii) emphasize the sists of carbon (C), hydrogen (H), oxygen (O), ash, and trace
challenges and future scope for biochar along with AMF (BC þ AMF) amounts of nitrogen (N) and sulphur (S) (Table 1). In most of the
applications for soil quality improvements. biochar H, N and O contents decreased with an increase in tem-
perature; ascribed to loss of volatile components, and dehydration
of organic compounds (Weber and Quicker, 2018). Similarly, H:C
2. Biochar as a potential soil amendment technique and O:C ratios also decreased with the increase in temperature,
suggesting that the biochar surfaces of the biochar were more ar-
2.1. Biochar and its physical properties omatic and less hydrophobic (Weber and Quicker, 2018). O:C ratio
is an indicative tool used for assessment of the stability of biochar. If
A wide range of biomass yield biochar after pyrolysis in an O:C is less than 0.2, it indicates a stable biochar with a half-life of
oxygen-depleted environment; for example, wood chips, crop more than 1000 years. However, if the ratio is 0.2e0.6, it indicates
residues, nutshells, seed mill screenings, and algal biomass con- an intermediate half-life period (100e1000 years) (Spokas, 2013). It
stitutes the conventional feedstock. Physical and chemical charac- is noteworthy, that higher pyrolysis temperature leads to increase
teristics of biochar are dictated by feedstock and pyrolysis in the levels of recalcitrant carbon in biochar; indicating retention
parameters (Tomczyk et al., 2020; Wan et al., 2020). Wood-based of significantly higher stable carbon fractions, than the biochar
biochar has comparatively higher pH than biochar from crop res- produced at low temperature (Shen et al., 2019). Higher surface
idue and manure (Brewer and Brown, 2012; Shaheen et al., 2019). area and alkaline biochar supports higher metal absorption ca-
Biochar with high pH induces liming effect in the soil. Results from pacities and faster uptake kinetics (Shen et al., 2019).
2
Fig. 1. Impact of biochar amendment on soil dynamics.
For instance, biochar derived from dairy manure is also helpful Fig. 2. K2CO3 and KOH are by far the most effective chemical acti-
in the remediation of lead and atrazine with a higher removal ef- vators, generating larger activated carbon yield, with a higher pore
ficiency of 100% and 77%. Biochar is helpful in the remediation of fraction, with lower ash and sulphur content (Foo et al., 2012; Wang
other toxic elements such as dioxins (Chai et al., 2012), polycyclic et al., 2020a). The maximum specific surface area of 1352.86 m2 g1
aromatic hydrocarbons (PAHs) (Kong et al., 2018; Xiong et al., 2017), is achieved using K2CO3 at 800 C (Cha et al., 2016). Although
and pesticides (Mandal et al., 2017; Niazi et al., 2018; Tabassum physical and chemical activation processes help in improving the
et al., 2019). However, its adsorption capacity is mainly depen- efficiency of biochar; the effects of in situ oxidization, acidification,
dent on the feedstock used, as the quantity of minerals in biochar is fragmentation, or partial degradation could compromise its effi-
a product of the raw materials used. ciency post field application in the long term (Spokas, 2013; Qian
For more promising and wider applications of biochar, different et al., 2015).
types of activation methods were adopted; predominantly the
physical and chemical ones (Fig. 2). Physical activation was carried 2.3. Biochar and its effect on soil biology
out using CO2, Ozone, and steam, at temperatures below 700 C
(Cha et al., 2016; Hu et al., 2019; Sizmur et al., 2017). It enhanced the Biochar addition to the soil is virtually irreversible as it interacts
decomposition of the unstructured part, followed by depletion of with different biotic and abiotic components. Plant growth may be
fine pore crystalloids resulting in much larger pores and surface negatively or positively impacted by the biotic interactions with
area. The use of CO2 could either increase or decrease specific mutualistic or antagonistic species and abiotic interactions
surface area and pore size depending on the pyrolysis temperature involving mineral nutrients, sunlight, and moisture. In general,
and residence time (Zhang et al., 2014; Wan et al., 2019). Activation biochar addition to the soil results in an overall increase in crop
rate is much higher with the use of steam, and activated biochar productivity, crop yield, soil microbial biomass, and rhizobia
could be produced if biochar is physically treated with 40% of nodulation (He et al., 2016; Kim et al., 2016; Lehmann and Joseph,
steam. 2015; Sun et al., 2019; Yu et al., 2019). The productivity prevails
Chemical activation was achieved using different chemical with biochar induced the increase in various macro and micro-
agents, e.g., KOH (Cha et al., 2016; Foo et al., 2012), NaOH (Park nutrients contents in soil.
et al., 2013), NH3 and K2CO3 (Foo et al., 2012), respectively. Use of The high concentrations of C, N, phosphorus (P), calcium (Ca),
hydrochloric acid, phosphoric acid, and sulphuric acid for chemical and potassium (K) in biochar may directly or indirectly enhance the
activation of biochar were also reported (Biswas et al., 2020; soil nutrients and promote the soil pore fractions (Weber and
Lonappan et al., 2020). Chemicals agents help in forming the micro- Quicker, 2018; Yu et al., 2019). The biochar orifices are beneficial
pores through subsequent dehydration and oxidation processes. to microbial habitats with amplified air supply, moisture, nutrient
Quinone groups, which act as electron shuttling and redox-active content and residence time; thus augmenting the physical and
moieties, could improve the efficiency of contaminant removal chemical conditions for plant and biota growth (O’Neill et al., 2009;
(Klupfel et al., 2014). The activation process using sodium hydrox- Yu et al., 2019; Jaafar et al., 2014). Consequently, the addition of
ide and potassium hydroxide in biochar is graphically presented in biochar expands incidence and diversity of bacterial populations in
3
Table 1
Biochar and its characteristics as derived from different feedstocks.
Characteristic of Biochar PT HR BY MC FC AC VC C H N O pH ABS BET PV References
Biochar from cereal feedstocks

Rice husk 400 e e e e 47.9 38.2 37.2 1.2 1.3 12.4 6.7 e e e Kameyama et al. (2016)
Wheat grain 650 20 55.5 e e e e 57.1 4.9 2.9 35.0 9.9 e 178.4 e Caban et al. (2019)
Wheat straw 650 e e e e e e 57.1 4.8 2.2 35.9 8.9 e 249.5 e Caban et al. (2019)
Maize straw 350 20 e e e 49.6 e 39.3 e e 1.1 e 0.5 0.02 Glab et al. (2020)
Barley straw 800 10 21.8 2.9 11.8 6.4 78.8 45.4 e e e e e e e Ahmed et al. (2018)
Corn Stover 600 e e e e 16.7 23.5 70.6 e e e 9.4 e 252.1 e Lehmann et al. (2011)
Oat grain 650 20 79.5 e e e e 57.5 4.6 2.6 35.3 10.2 e 309.5 e Caban et al. (2019)
Oat straw 650 20 e e e e e 51.1 4.7 1.1 43.1 10.6 e 294.3 e Caban et al. (2019)
Sweet sorghum bagasse's 500 e e 4.2 15.9 3.5 76.3 45.7 5.8 0.3 48.2 e e e e Yin et al. (2013)
Millet biomass 600 3.0 35.5 e e e e 69.1 2.5 0.9 9.9 e e e e Camelo et al. (2018)
Biochar from oil yielding plant feedstocks
Jatropa deoiled cake 350 e 39.9 e 46.9 25.8 20.9 44.1 2.9 8.6 44.4 9.4 e e e Narzari et al. (2017)
Jatropa deoiled cake 550 e 29.5 e 57.7 26.8 15.6 50.1 2.3 9.1 38.8 10.6 e e e Narzari et al. (2017)
Jatropa deoiled cake 650 e 25.2 e 59.4 29.9 9.2 52.8 1.2 8.6 35.3 10.8 e e e Narrzari et al. (2017)
Jatropa seed cover 350 e 30.2 e 48.4 19.3 26.1 66.7 2.2 1.4 29.6 8.2 e e e Narrzari et al. (2017)
Jatropa seed cover 550 e 28.7 e 53.2 23.4 15.9 67.5 2.0 2.1 28.4 9.8 e e e Narrzari et al. (2017)
Jatropa seed cover 650 e 23.0 e 58.0 26.4 13.5 71.1 1.5 1.6 25.7 10.5 e e e Narzari et al. (2017)
Rape straw 400 34.5 e e e e 63.7 1.9 0.9 13.5 9.2 e e e Zhang et al. (2020)
Peanut shell 950 e 21.9 32.7 75.1 14.6 6.2 74.9 0.8 0.9 7.4 e e 210.3 e Lee et al. (2016)
Peanut shell 481 5.4 e e 65.54 7.6 23.1 71.5 2.9 2.1 16.6 9.3 e 2.5 e Lee et al. (2016)
Canola meal 750 e e 4.8 57.4 25.5 12.3 63.2 2.2 0.8 33.0 e e 356.0 0.2 Devi et al. (2020)
Moringa seed 450 10.0 e e e e e 84.9 e 7.0 8.0 e e e e Bagheri et al. (2020)
Biochar from forest derived feedstocks
Wood stem e e 50.3 e e 12.8 e 84.8 e e e 9.6 e e e Jindo et al. (2014)
Wood bark 400 e 28.3 e e e 32.4 70.2 4.1 0.8 20.5 7.0 44.9 11.9 e Jindo et al. (2014)
Apple chips 600 e 16.6 e e e 11.1 81.5 1.9 0.5 13.6 10.0 122.0 208.7 e Jindo et al. (2014)
Apple plant chips 800 e 15.5 e e e 6.8 84.8 0.6 0.3 5.8 10.0 298.5 545.4 e Jindo et al. (2014)
Apple plant chips 400 e 35.8 e e e 32.1 70.5 3.7 0.7 21.5 6.4 38.7 5.6 e Jindo et al. (2014)
Oak 600 e 22.0 e e e 12.3 81.2 1.9 0.5 15.9 8.8 131.3 288.6 e Jindo et al. (2014)
Oak 800 e 19.1 e e e 7.9 82.8 0.7 0.3 17.3 9.7 250.3 398.1 e Jindo et al. (2014)
Oak bark 450 e e 22.8 64.5 11.1 e 71.2 2.6 0.5 12.99 e e 1.9 1.1 Mohan et al. (2014)
Pine cone 200 7 e 62.3 35.6 0.8 e 69.7 2.1 1.0 27.1 4.1 e 0.5 2.4 Igalavithana et al. (2017)
Pine cone 500 7 e 10.0 79.6 8.9 e 74.7 e e e e e 192.9 10.2 Igalavithana et al. (2017)
Hickory wood 600 e e e e e e 84.7 1.8 0.3 11.3 e e 256.0 e Shaheen et al. (2019)
Mulberry wood 450 e 32.7 e e e e 70.8 3.3 1.9 23.8 11.1 31.4 Shaheen et al. (2019)
Long leaf pine 500 30 29.5 e e e e 86.8 3.3 3.7 5.9 e e e Oginni et al. (2020)
Red oak 500 30 29.3 e e e e 72.2 2.7 7.3 17.6 e e e e Oginni et al. (2020)
Hard mapple 500 30 30.1 e e e e 85.5 2.5 1.6 10.12 e e e e Oginni et al. (2020)
Mesquite wood 300 e 40.5 2.1 67.6 18.2 4.22 66.5 3.7 1.9 19.7 e e e 3.1 Abdin et al. (2020)
Biochar from commercial crop feedstocks
Bagasse 500 10 43.7 e e 8.6 e 85.6 e e e 9.3 e e e Cha et al. (2016)
Sugarcane e e 62.9 e e 15.9 e 84.4 e e e 10.3 e e e Cha et al. (2016)
Coco peat e e 53.5 e e 6.9 e 87.85 e e e 6.9 e e e Cha et al. (2016)
Coffee residue 400 5 35.8 1.23 75.39 4.18 3.48 15.09 2.3 0.005641 Zhang et al. (2020)
600 5 26.8 3.22 79.4 2.1 3.3 11.9 0.6 0.003108.0 Zhang et al. (2020)
Almond shell 450 e e 7.21 51.5 48.4 e e e e e 8.2 e e Ali et al. (2020)
Cottonseed hull 350 e 36.8 34.9 52.6 5.7 e 77 4.5 15.7 1.9 e e 4.7 e Uchimiya et al. (2011)
Cottonseed hull 650 e 25.4 13.3 70.3 8.3 e 91 1.26 5.9 1.6 e e 34 0.007 Uchimiya et al. (2011)
Cottonseed hull 800 e 24.2 11.4 69.5 9.2 e 90 0.6 7.0 1.9 e e 322.0 274.0 Uchimiya et al. (2011)
Biochar from other feedstocks
Seagrass 600 e e e e e e e e e e e e 496.0 0.1 Ncibi et al. (2009)
Congress grass 300 30 e e e e e 55.1 4.9 4.2 35 9.8 e e e Kumar et al. (2013)
Algae 450 10 14.0 41.0 45.0 41.0 11.0 6.0 40.5 e e e e Amin et al. (2019)
Sewage sludge 350 20 12.4 e 24.0 e 3.3 e e 0.7 0.01 Glab et al. (2020)
Fish bone 400 58.9 1.1 12.7 80.7 5.5 13.2 1.0 1.8 3.2 e e 81.8 e Abdin et al. (2020)
Fish bone 600 51.2 1.0 7.7 86.1 5.4 9.3 0.6 0.9 3.1 e e 90.0 e Abdin et al. (2020)
‘-’ ¼ No information available; PT¼ Pyrolysis temperature in degree celsius; HR¼Heating rate (Degree celsius minute1); BY¼Biochar yield in percentage; MC ¼ Moisture
content in percentage; FC¼Fixed carbon in percentage; AC ¼ Ash content in percentage; VC¼Volatile content in percentage; C¼Carbon in percentage H¼ Hydrogen in
percentage; N¼Nitrogen in percentage; O¼Oxygen in percentage; pH ¼ pH (H2O); ABS ¼ Absorbance (mg g1 D/W); BET¼Brunauer Emmett Teller surface area (m2 g1);
PV¼Pore Volume cm3 g1.
anthrosol soil up to a depth of 1 m (O’Neill et al., 2009). Some initiate significant increase in surface adsorption, flocculation,
theories also suggest that biochar ultimately alters microbial bacterial cell bridging, and entrapment of bacterial cells to the
community structure and soil enzyme activities, as microbes living biochar pores. Therefore, in the biochar-amended soil system,
within its pores are shielded from microarthropods (Fig. 3) (Thies abundance in mesofauna and microfauna is a function of
and Rillig, 2009; Awasthi et al., 2020; Chintala et al., 2014; soilebiochar interaction (Lehmann et al., 2011).
Nguyen et al., 2018). In addition, soil biota-biochar interactions Among the mesofauna, soil earthworms conspicuously
4
Fig. 2. Physical and chemical activations of biochar and their effects on its surface.
Fig. 3. Biochar as potential habitat for soil fauna.
5
assimilate fresh organic matter over the old and recalcitrant debris application of biochar; a massive 53% is translocated by wind and
(Khan et al., 2019b; Singh et al., 2017). Their ingestion alters biochar water, perilously exposing non-target terrestrial and aquatic sys-
microbial activities and properties; besides carrying biochar deeper tems through erosion (Major et al., 2009).
into the soil and accumulating HMs in their tissues (Lehmann et al., A recent research reveals that significant portion of biochar gets
2011; Beesley and Dickinson, 2011; Khan et al., 2019a). Despite mineralized inside soil while only a trace portion remains stable
many studies on biochar and earthworms, a clear knowledge gap (El-Naggar et al., 2018). In comparison with other sequestration
does exist for other mesofauna such as nematodes and micro- strategies such as afforestation and reforestation, biochar carbon
arthropods (Lubbers et al., 2013; Khan et al., 2020a). Biochar has its sequestration increases with the residence time (Sohi et al., 2010;
own dynamics inside the soil. Sometimes microbes, which colonize El-Naggar et al., 2019). It is suggested that biochar could help in
the pores of the biochar inhibit diffusion process (Quilliam et al., isolating 50% of carbon from the soil. This percentage is much
2013). However, quantitative data does not exist for physical pro- beyond the 3% from combustion or the 10e20% over a period of
tection of soil microbes in biochar pores and their access to avail- 5e10 years from biological decomposition (Lehmann et al., 2011).
able carbon substrates. Chen and Yuan (2011) reported that certain As a consequence of climate change and other anthropogenic
toxic compounds such as catechols might get adsorbed on the practices, CO2 concentration in the ambient air has reached
biochar surface, subsequently inhibiting microbial growth and approximately to 413 ppm (GCC Global Climate Change, 2020). Net
shrinking the microbial population. While in some cases, biochar CO2 emission could be reduced to 0.9 Gigaton (Gt) if 50% of crop
with low molecular weight and dissolved organic carbon (DOC) is residues and 67% of forest residues are used as a feedstock for
preferred by microorganisms as a potential carbon substrate biochar (Laird et al., 2009). Thus, effective implementation of bio-
(Stewart et al., 2013). In soil, biochar addition creates an artificial char is imperative to mitigate the adverse effects of climate change.
niche for the microorganisms. Thus, soil bacteria such as Pseudo- In developing countries such as India, biochar production from crop
monas sp., Azotobacter sp., Rhizobium sp. and Azospirilium sp. residue could lower GHG emission by about 4.8% to even as much as
accumulate in biochar pore sizes of 0.3e3 mm (Awasthi et al., 2020). 10.7%. These figures take into account biochar effectiveness cir-
Protozoa play a crucial role in mineralizing nutrients, making them cumscribed by feedstock type, specific temperature, and activation
available for plants and other microbiota, and they inhabit in pore or modification process (Rajagopal et al., 2017). Therefore, biochar
sizes of 7e30 mm . The majority of protozoa consume bacteria, but production from crop residue has dual benefits of waste utilization
the vampyrellids group of amoebae, eat fungi. Another essential as well as offsetting GHG emission. A recent study reported that,
group of microorganism in the soil are the fungi, which inhabit in about 12% of current anthropogenic CO2 emissions could be curbed
pore sizes of 2e80 mm and are protected against fungivores ro- using biochar (El-Naggar et al., 2019). It also suggests that the
dents. In soil biota, three different types of fungi are dominants i.e. maximum sustainable potential for carbon abatement from biochar
decomposers, mutualists and pathogens or parasites fungi. Water is 1e1.8 Gt C per year by 2050. However, the particular effects of
molecules in the soil have a deep relation with the decomposition biochar application on soil GHG emissions remain debatable and
of biochar, and it plays a significant role in processes such as are portrayed in different studies (Cayuela et al., 2014).
dissolution, hydrolysis, carbonation and de-carbonation, hydration, Biochar application in soil directly or indirectly affects N cycle.
and redox reactions. Thus, water and dissolved substances would Biochar application induces reduction in N2O emission and pro-
fill in the pore size between 1 nm and 50 nm or <100 nm and motes growth of denitrifying rhizobials such as Bradyrhizobiaceae
provide balanced water resources to microbes. and Hyphomicrobiaceae (Anderson et al., 2011). Biochar with its
large surface area offers reactive surface for N and P attachment in
2.4. Biochar and its role in C, N and P cycles soil microbial biomass, which modulates N and P bioavailability in
soil. Concurrently, functional groups attached to the surface of
Over millennia, biochar in ancient terra preta soil has improved biochar, participate in the adsorption process of NO3 (Huang et al.,
soil health (Gaunt and Lehmann, 2008; Lehmann and Rondon, 2020). Biochar is known to assist the regulation of mineralization,
2006; Ogawa et al., 2006; Woolf et al., 2010). The origin of this N2 fixation, nitrification, ammonia volatilization, increasing NHþ 4
biochar can be traced back to volcanic eruptions and forest fires, storage by enhancing cation exchange capacity and denitrification
which burnt the biomass that later accumulated over centuries in (Gul and Whalen, 2016). In contrast, a study suggested that the
the soil. Biochar not only enhances the quality of soil but also effect of biochar is negligible on the available N in soil and plant’s
mitigates the greenhouse gaseous (carbon dioxide and methane) tissue (Biederman and Harpole, 2013). The role of biochar in soil P
directly by sequestering carbon. Carbon sequestration in the simple cycle is regulated by biochar-mediated microbial enrichment,
term refers to the storage of carbon for a longer duration. On a consequently impacting P use efficiency (PUE) of plants grown
global scale carbon cycle operates in four important biomes, the (Anderson et al., 2011). Biochar used as a liming agent in acidic soils
terrestrial, atmospheric, oceanic, and geological. Carbon seques- renders the bound P bioavailable (Cui et al., 2011). Furthermore,
tration through biochar allows transferring of carbon from active biochar and P availability would be more beneficial in acidic soils of
carbon biome to the passive carbon biome. In the passive carbon low latitudes, where agriculture is limited by P availability (Steiner
biome, it is stored as stable or inert carbon inside soil. During its et al., 2008). Leaf biochar had significant effect on the P dynamics in
storage period, it is resistant or less reactive to the chemical process the high altitude forests of Cunninghamia lanceolata (Chinese fir);
such as oxidation of CO2 or reduction to CH4 (Lehmann et al., 2011). mediated by P-solubilizing bacteria, such as Burkholderia-Para-
Thus, with highly compressed aromatic structures, biochar serves burkholderia, Planctomyces, Sphingomonas and Singulisphaera,
as an excellent viable tool for sequestering carbon over decades and which can indirectly improve P availability in soil (Zhou et al.,
even centuries (Lehmann et al., 2011; Yu et al., 2019). The afore- 2020).
mentioned properties of biochar have initiated research endeav-
ours across the globe, seizing the opportunity to achieve a more 3. AMF as an indispensable part of soil ecosystem
sustainable carbon cycle, by employing biochar for carbon
sequestration (Munera-Echeverri et al., 2020). Coupled to the Soil is one of the most complex ecosystems in the world. In the
benefits of biochar, there is farmer participation in the global car- previous section, the review focused on abiotic amendment tech-
bon stock market by direct application of biochar in agricultural niques i.e. biochar. Within the soil, fungus is an indispensable biotic
fields (Robb et al., 2020). However, the real danger lurks in the component that also maintains plant-soil continuum (Godoy et al.,
6
2017; Zhang et al., 2016). Palaeontological and evolutionary evi- favourable soil structure with a binding effect (Baruah and Sahu,
dences suggest that fungi work together with vascular plants to 2019; Rillig et al., 2010). Fungal network inside the soil is useful
enhance soil quality (Lopez-Obando et al., 2015). Paleobotanists for mitigating the HMs and water stress (Al-Arjani et al., 2020;
have shown that these symbiotic relationships existed long before Krishnamoorthy et al., 2019; Rask et al., 2019). In the pedosphere,
the evolution of land plants (Kamel et al., 2017; Selosse et al., 2015). AMF aids soil aggregation with a viscous glycoprotein known as
They developed with the arbuscules in Devonian period (400 Mya), glomalin. It is of red-brown in colour, with a robust reinforcing
hyphae and spores during the Ordovician period (460 Mya) and effect, thus rejuvenating the overall soil quality (Magurno et al.,
glomeromycota during Ediacaran period (600 Mya) (Maherali et al., 2019; Wang et al., 2020b). Moreover, glomalin is the primary
2016; Koyama et al., 2019). component of AMF that binds with ions present in rhizosphere,
In the soil ecosystem, some common associations that occur are which enhances the metal binding capacity of glomalin (Janeeshma
Vesicular-Arbuscular Mycorrhizae (VAM), Ectomycorrhizae (ECM), and Puthur, 2020). AMF releases glomalin during hyphal turnover,
Orchid mycorrhizae, Ericoid mycorrhizae, Ectendomycorrhizae and after their death in the soil, which later forms a glycoprotein,
(Arbutoid), Centianoid mycorrhizae, and Monotropoid mycor- i.e., glomalin-related soil protein (GRSP). GRSP enhances soil
rhizae. Among the seven different types of mycorrhizae, the quality along with HMs sequestration in sediments (Wang et al.,
endomycorrhizal association is most common and found in all 2019b) and soil (Jia et al., 2016). A recent study suggested that
types of soil. VAM produces arbuscules and vesicle, and are GRSP reduces the Cd contamination during interflow and leaching
therefore called arbuscular mycorrhizal fungi or AMF. AMF helps to (He et al., 2020), besides increasing the C pool in some of threat-
balance nutrient levels and improve the functioning of the soil ened ecosystems of world e.g. Mangrove ecosystem (Wang et al.,
system (Wei et al., 2016). It reproduces using spores which are 2018).
small multinucleate, asexual, and their number are increased
significantly by the mycelium. Biodiversity, ecosystem variability 4. Functionality and dynamics of biochar and AMF
and productivity can be maintained with the help of AMF diversity.
Globally around 85% of the plant families are colonized by mycor- Biochar as a soil amendment is one of the best possible solutions
rhiza in all types of ecosystems (Wang et al., 2010). to speed up the restoration and rejuvenation process of degraded
Several studies have endorsed the interwoven relationship be- land. Biochar application for managing soil biota and conserving
tween biotic and abiotic factors in soil. Inside the pedosphere, AMF soil quality is a theme of burgeoning interest; though the exact soil
hyphae bond with the plants roots. A dense network of AMF hyphae alteration processes by biochar are not well understood. Additive
is helpful in the formation of soil aggregates, which regulates water benefits of biochar include direct or indirect effect on plant growth.
inflow, increases pore space and prevents erosion (Al-Arjani et al., Plant and AMF mutualism under the additive effect of biochar
2020; Mathur et al., 2019; Zhang et al., 2019a), and forms a sig- works better, as suggested by many researchers (Table 2). Despite a
nalling mechanism for plant defence (Cabral et al., 2019; Tao et al., bulk of research, interactions between biochar and AMF are chal-
2016). A study conducted by Wilkinson et al. (2019) indicated that lenging to predict inside the soil. Relationship between biochar and
the mycelia network stimulated the uninfected plant to initiate AMF depends on both biochar properties and type of fungi, along
defence mechanisms against aphid attacks. with edaphic conditions, i.e. structure and texture, soil organic
In the soil environment, AMF presents different modes of in- matter (SOM), soil minerals (nitrogen and phosphorus) and soil
teractions with biotic communities. For example, the cytoplasm of biological communities (Solaiman et al., 2019). Biochar effects on
AMF, may harbour soil bacteria like Actinomycetes and Spiroplasma. soil aggregation were the main focus of several studies. However,
While in some AMF species, parasitic or necrotrophic relationships some recent studies on relatively short-term effects of biochar, had
exist with other fungi. Such relationships would inhibit spore for- focused on soil carbon storage, type of biochar and its additive ef-
mation, germination and dispersion mediated by Rhizoctonia sp., fects (Wang, 2012; Yu et al., 2018). A comprehensive investigation
Chytrids (Protoctistan fungi), Rhizidiomcopsis sp., Spizellomyces sp. using FAME analysis and EEM-PARAFAC modelling suggested that
and Humicola sp. (Secilia and Bagyaraj, 1988). Species of collembola biochar could alter soil dissolved organic matter, thereby affecting
(Springtails), lumbricus and nematodes feed on fungal hyphae. the soil microbiota (Yang et al., 2019).
Squirrels and rodents, which share the niche with AMF ingest
hypogeous sporophores, thus transporting AMF spores to distant 4.1. Mechanisms of interaction between biochar and AMF
localities through their faecal matter. While some organisms such
as aphids and barn swallows directly help in spreading of AMF BC þ AMF interaction has been considered to improve soil
spores (Fig. 4). quality and enhance plant growth through nutrition uptake and
AMF generally occur in the topsoil zone of 0e20 cm, but are not supporting beneficial microorganism (Elzobair et al., 2016). Many
confined to it, and may extend to 70 cm or even more. The popu- researchers suggested three types of mechanisms for combined
lation of AMF is highest in the spring season and the average applications of BC þ AMF, i.e., enhancement of the soil quality,
concentration of propagules found in the soil is about providing shelter from fungal grazer, and improving signalling
2 104e1 106 (Bhardwaj et al., 2020). AMF are detritivores and mechanism between plant and AMF (Hammer et al., 2015; Vanek
have a close association with organic carbon; their population is and Lehmann, 2015; Zwetsloot et al., 2016). Moreover, the above
regulated by the different crop systems and allied practices (Wei mechanisms would help in facilitating AMF growth via spore
et al., 2019; Lehman et al., 2019; Singh and Singh, 2019). Howev- germination and hyphal branching (Hammer et al., 2014, 2015).
er, significant increase in AMF population is observed with crops Inside the soil matrix biochar acts as a nutrient adsorber, and fine
like sorghum, chickpea and maize, whereas there is restricted sections of root with AMF are helpful for nutrition uptake (Hammer
growth in oats, barley and wheat. Practices including tillage, crop et al., 2014). However, BC þ AMF not only enhances the soil quality
rotation, residual crop burning, poor drainage, fungicide applica- but also remediates the HMs present in the soil. Different pot and
tions and waterlogging have a disastrous effect on AMF; by field trials indicated the phytoremediation potential of biochar and
breaking the soil aggregates and disrupting the mycelia network AMF. A recent study indicated that co-application of BC þ AMF
(Baruah and Sahu, 2019). AMF can also sequester considerable increased the soil pH, thereby improving Cd immobilization and
amount of carbon, via its turnover rates and exudations. An decreasing its bioavailability (Liu et al., 2018). A similar study on
extensive fungal network located around the roots provides a remediating the Pb-contaminated soils with BC þ AMF revealed
7
Fig. 4. Relationship of AMF with various biotic components of soil ecosystem.
that the combined application resulted in higher root colonization, (2019) also conducted a field experiment in an acidic soil cultivated
increased microbial biomass carbon, and enhanced GRSP (Khan with cacao (Theobroma cacao L.) over a period of 15 months. They
et al., 2020a). Above combination (BC þ AMF) reportedly reduces applied three doses of biochar derived from bamboo residues
Arsenic (As) contamination as well (Al-Shamma et al., 2017). (ranging from 0, 7.5, 15% (W/W) and found significant increase in
Moreover, combined application also favoured N and P uptake stem diameter and plant height with 15% of the biochar and AMF
during drought (Hashem et al., 2019), increased shoot biomass applications, as compared to the control soil. Recently, Khan et al.
(Xiao et al., 2020) and enhanced resin-extractable P up to 67% (2020b) showed a significant increase in grain biochemistry and
(Zwetsloot et al., 2016), thereby improving overall soil quality. nutrient content in barley grain in a Pb-contaminated soil in
Additionally, their combined application under conditions of Pakistan. The treatment comprised lignin-derived biochar and AMF
drought may substantially enhance the crop production (Hashem consortium of Funneliformis mosseae, Rhizophagus aggregatus,
et al., 2019; Luo et al., 2017). The increase in plant response from Claroideoglomus etunicatum and Rhizophagus intraradices at
BC þ AMF application is most commonly observed in degraded soils 220,462 propagules kg1. Likewise, shrimp waste biochar and
such as sandpit mines (Ohsowski et al., 2018), and calcareous soil Funneliformis mosseae, were also used as soil treatment, which
(Mau and Utami, 2014); however its effectiveness is not always significantly increased the P uptake and growth of corn (Kazemi
significant in soils contaminated with HMs (Qiao et al., 2015; Zhang et al., 2019). Positive effect was also observed in Spain when dry
et al., 2019b). An attempt towards mine restoration was made using olive derived biochar and AMF applied on wheat crop (Vejvodova
J. curcas along with BC þ AMF application. The results showed et al., 2020). BC þ AMF responds to different conditions. Liu et al.
contrasting effects on soil and plant growth (Gonza lez-Cha
vez (2017) in a pot experiment studied the phytotoxic effect of woody
et al., 2017). Use of BC þ AMF also showed an affect on the biochar and AMF on potato (Solanum tuberosum) growth in sandy
growth of fowl manna grass (Glyceria striata L.) in Canada (Moland loam soil in China. They found that the biochar had limited
et al., 2018). Under drought and extreme conditions, biochar can act adsorption for mineral N and P uptake.
as a buffer by providing safe habitat for AMF, which results in Nzanza et al. (2012) also assessed the impacts of BC þ AMF on
increased in number of spores, mycelium, vesicles and arbuscules. tomato (Solanum lycopersicum L.) growth in soil with two biochar
Moreover, the combined application of BC þ AMF has many addi- treatments (5 t ha1 or unamended) and G. mosseae. They observed
tional benefits for plant growth and nutrient cycling, such as that BC þ AMF combined application resulted in 26% reduction in
increasing photosynthetic attributes, relative water content (RWC), leaf P content than in plants without any inoculation. Concurrently,
and membrane stability (Hashem et al., 2019). it revealed that the impact of BC þ AMF applications on plant was
Biochar derived from locally available materials along with AMF highly dependent on the local conditions, biochar used and
had enhanced the plant growth. For example, the addition of cow experimental set-up. For example, a meta-analysis, which
dung-derived biochar at the rate of 4.5 and 7.5 g kg1 and 10e15 comprised of 371 studies, revealed that the biochar amendment
AMF spores kg1 increased maize yield (Zea mays L.) in calcareous displayed no role in enhancement of percentage colonization of the
soil of Indonesia (Mau and Utami, 2014). Similarly, Aggangan et al. roots. The insignificant effect observed in the AMF might be
8
Table 2
Chronological developments in the assessment of biochar’s effects on AMF and soil.
Year Feedstock/Biochar Test plant/substrate Effect on AMF and rhizosphere of plant References
1984 Wood Soil Lowers AMF population due to high salinity in the soil Killham and
Firestone (1984)
1985 Wood Soil Lowers AMF population due to higher concentration of salt Killham (1985)
1990 Wood Soil Positive effect on mechanical impedance and increases root proliferation Bengough and
Mullins (1990)
1990 Charcoal Glycine max L. Infected with the growth of AMF under grown humus rich andosol Saito (1990)
1994 Rice husk Citrus limon L. Increase the percentage of AMF infection in the roots Ishii and Kadoya
(1994)
2000 Crowberry Betula utilis Higher growth of micro biota observed Pietika€inen et al.
(2000)
2000 Charcoal Zea mays L. Decreases in AMF abundance. Gaur and
Adholeya (2000)
2000 Crowberry Soil Organic carbon influences the functionality of AMF. Pietika€inen et al.
(2000)
2001 Charcoal Leguminous crops Biological nitrogen fixation reduces and plantemicrobe interactions increases Giller (2001)
2002 Wood Soil Provide a habitat for AMF and ensuring greater infection rate through inoculum Saito and
Marumoto (2002)
2002 Charcoal Asparagus officialis Increased infection rate of AMF colonization Matsubara et al.
(2002)
2003 Wood Vigna radiata and Oryza sativa Biochar release and provide elevated amounts of available nutrients to plants Lehmann et al.
(2003)
2003 Biochar Quercus sp. and Acer sp. Higher amount of phosphorus content in soil leads to decrease in the AMF Corbin et al.
population. (2003)
2005 Biochar Glycine max L. Higher amount of phosphorus content in soil leads to decrease in the AMF Grant et al. (2005)
population.
2005 Mineral fertilization Zea mays L. Mineral fertilization reduced the growth of AM Fungi in long term field experiments Gryndler et al.
(2006)
2006 Charcoal/Peat bark Prunus persica Negative interaction with the AMF Kipkoriony and
Fusao (2006)
2006 Biochar Triticum aestivum Decrease in the AMF population Covacevich et al.
(2006)
2006 Biochar Zea mays L. Increases or decreases the AMF external hyphae Gryndler et al.
(2006)
2007 Woody biochar Phaseolus vulgaris Increases in nitrogen uptake from 50 to 72% providing suitable niche for AMF growth. Rondon et al.
(2007)
2007 Biochar Herbaceous plant Enhances the AMF population, facilitate the production of extraradical hyphae for Warnock et al.
nutrient uptake (2007)
2009 Biochar Crops Increases total phosphorus content in the soil Nursyamsi and
Setyorini (2009)
2009 Biochar Soil and crop Increases AMF population Birk et al. (2009)
2010 Deepnabanded oil mallee Triticum aestivum Increased AMF colonization during dry seasons in low Phosphorus soil; increases C Blackwell et al.
biochar storage in soil and minimizing leaching of nutrients (2010)
2010 Eucalyptus wood biochar Triticum aestivum Increases 20e40% of AMF colonization Solaiman et al.
(2010)
2010 Hydrochar Daucus carota Stimulate spore germination of AMF Rillig et al. (2010)
2010 Biochar Mangifera indicaL. trunks and Neutral to decreased AMF abundance with biochar additions Warnock et al.
branches (2010)
2010 Biochar Spinacia oleracea L. High alkaline biochar impart negative effect on AMF Zuccarini (2010)
2011 Biochar Plant and crops Improve plant growth which enhances soil quality and soil health Lehmann et al.
(2011)
2011 Biochar Asparagus officinalis Increased AMF colonization via the sorption of allelochemicals Elmer and
Pignatello (2011)
2012 Biochar þ AM Fungi Plant and soil Provides habitat for activities of soil microorganisms Fischer and Glaser
(2012)
2013 Grass Daucus carota L. Addition of Biochar increases the concentration of dissolve organic carbon, nitrogen Mukherjee and
and phosphorus Zimmermann
(2013)
2013 Biochar Sorghum bicolor Decreased above ground plant biomass by 42% relative to the mycorrhizae and high LeCroy et al.
nitrogen treatment, while simultaneously promoting mycorrhizal root colonization. (2013)
2014 Charcoal/Wood Daucus carota roots Provides access to AMF hyphae in microsites within biochar for enhance uptake Hammer et al.
(2014)
2016 Eucalyptus biochar Citrus aurantium Biochar treatment alone would not enhances the soil quality Ibrahim (2016)
2017 Wheat straw Zea mays L., Arachis hypogaea L., Observed higher root colonization in intercropped maize Liu et al. (2017)
Glycine max L.
2017 Maize straw Zea mays L. Biochar application at 50 t ha1 significantly increased the PLFAs (Phospholipid fatty Luo et al. (2017)
acids) of AMF
2018 Wheat straw Glycine Max. Both fungi and bacteria were involved in nitrogen retention, especially gram Yu et al. (2018)
negative bacteria
2019 Rice husk Oryza sativa Alkaline conditions resulting from biochar amendment favour fungal growth over Oladele et al.
bacterial growth. (2019)
2019 Pruned branches of Triticum aestivum, Zea mays L. AMF can be increased in an alkaline calcareous soil with low fertility Malik et al. (2019)
Acacia and Cicer arientinum, Vigna
radiata
(continued on next page)
9
Table 2 (continued )
Year Feedstock/Biochar Test plant/substrate Effect on AMF and rhizosphere of plant References
2020 Amur silvergrass rice Soil Biochar reduced the Pb bioavailability, while rice straw biochar increased the As; El-Naggar et al.
straw and umbrella tree Biochar addition enhances the dissolved organic matter (DOM) and AMF growth (2020)
wood inside sandy soil
attributed to the alteration in the plant nutrient environment and decrease in phosphorus mineralization rates in soil (Xiao et al.,
disruption of signalling mechanism (Biederman and Harpole, 2020). On the contrary, some studies suggested that biochar with
2013). However, due to the diverse impacts of BC þ AMF on plant a higher phosphorus content and produced during higher tem-
growth and soil, there is an urgent need to decode the mechanisms perature regime does not provide a favourable environment for
and functions of BC þ AMF for effective implementation of a con- AMF to grow (Liu et al., 2019, 2020). Thus, biochar applications are
sortium for field applications. A far more in-depth analysis is required to be tailored according to the different soil conditions to
required to cater for the need of the researchers, farmers, policy- benefit the growth of AMF (Aggangan et al., 2019; Hashem et al.,
makers, and other stakeholders concerning the usability of suitable 2019).
and locally available feedstock, their feasible production conditions,
and tailored mixing and application ratio for different soil types.
4.2. Effects of biochar along with AMF (BC þ AMF) on plant growth
Biochar, with its rich sources of carbon, can support AMF
growth, leading to their combined utility in improvement of crop
BC þ AMF would help in increasing the root growth of the plant
performance. This combination would only enhance the extant
while some of the researchers also suggested the use of soilless
broad range biochar applicability in soil system, and positively
culture with only biochar as substrate. In such cultures, plants
impact the science of soil management (Aggangan et al., 2019;
extract nutrients from the pores of biochar assisted by AMF hyphae.
Ohsowski et al., 2018; Yusif et al., 2018). Biochar applications and
This type of culture technique could ultimately improve the root
their outcomes are dynamic and depend upon various governing
biomass by 47% and root tip number by 64%. The best results were
factors. In most of the cases, AMF functionality improved post
obtained using coconut biochar, which significantly improved the
addition of biochar, but scientific validation and long-term field
storage roots of Asparagus niger species (Matsubara et al., 2002).
trials are required to corroborate this evidence (Hashem et al.,
Similar results were shown in rice (Noguera et al., 2010), wetland
2019; Liang et al., 2019). Fig. 5 illustrates the mechanism underly-
grasses (Ohsowski et al., 2018; Liang et al., 2019), and tomato (Yusif
ing the biochar and AMF interactions inside the soil system. Biochar
et al., 2018). Combined applications of biochar and AMF showed
applications can alter soil phosphorus availability via modulation of
positive results, endorsed by increased nitrogen fixation in
soil pH (Shen et al., 2016; Solaiman et al., 2019). For example, on
chickpea, under the condition of drought tolerance (Hashem et al.,
adding biochar of higher pH to the alkaline soil, it would lead to a
2019). In the same way, woody biochar is helpful in increasing the
Fig. 5. Biochar enhances the soil amelioration capacity of AMF.
10
existing mycorrhizal colonization, and extra radical hyphal length aggregation, thus sequestering and maintaining carbon stock inside
which results in alleviating water-stressed conditions in pasture the soil, and creating a temporary carbon pool for plant species to
soil (Mickan et al., 2016). Yang et al. (2020) reported that BC þ AMF flourish (Rafique et al., 2020). AMF symbionts inhabit inside bio-
addition in soil promoted the growth of potato (Solanum tuber- char pores and increase metal adsorption capacity and water stress
osum), mainly by improving its nutrient uptake capacity. tolerance for the plant. Flavonoids, sesquiterpenes, and strigo-
The potential role of AMF and biochar is to increase the transfer lactones released by the plant roots increase the functioning of the
of photosynthate in plant (Xiao et al., 2020). It is also helpful in soil mycorrhizal network inside the soil. A recent study showed positive
Table 3
Recent studies reported on applications of BC þ AMF.
Investigated parameters Biochar feedstock AMF Strain Targetted plant Major outcome References
species
Plant phosphorus Mixed maple and Rhizophagus clarum Phaseolus vulgaris No alter in P uptake, but shifted uptake Vanek and
hickory sawmill towards AMF for FeeP and roots for NaeP Lehmann
waste (2015)
AMF colonization Acacia saligna wood, Rhizophagus intraradices Sorghum bicolor Better P use efficiency was associated with Blackwell
Jarrah wood, higher mycorrhizal colonization et al. (2015)
Wundowie jarrah
Plant growth under Coniferous wood Funneliformis coronatum (Giovann.) L. sativa var. Increased uptake of P and Mn Hammer
salinity condition chips capitata et al. (2015)
Effect on plant-available Bone Rhizophagus clarum Zea mays L. P inputs and AMF root interactions improved Zwetsloot
phosphorus plant nutritional status et al. (2016)
Effect of phosphorus Chicken manure and Rhizophagus sp. Triticum aestivum Increase in soil pH and mycorrhizal Madiba
wheat chaff L. colonization et al. (2016)
Plant growth and Switchgrass, mixed Rhizophagus intraradices Allium porrum L. Reduction in AMF colonization Han et al.
phosphorus (P) uptake hardwood and (2016)
mixed softwood
Phosphorus and Wood Rhizophagus irregularis Solanum Negative effect on P/N uptake. Liu et al.
Nitrogen tuberosum (2017)
Pb(Lead) and Cd) Corn Acaulospora sp. Jatropha curcas L.High desorption of Cd and Pb Gonz alez-
(Cadmium) Chavez
et al. (2017)
Organic carbon, Available Orchard pruning - Vitis vinifera L. Increases organic carbon by 20.7%, available Amendola
ammonium, available ammonium by 84.4% and available water et al. (2017)
water content content of the soil by 11.8%.
Soil nutrients Chips of spruce, pine Rhizophagus intraradices Glyceria striata Increase liming effect and an increase in Moland
and fir trees nutrient availability et al. (2018)
Phosphorus uptake Sewage sludge Rhizophagus irregularis Triticum aestivum No effect on phosphorus uptake Efthymiou
L. et al. (2018)
Phosphorus uptake Activated biochar Claroideoglomus and Funneliformis sp. Andropogon Partial remediation Paymaneh
gerardii et al. (2018)
Cadmium (Cd) Wheat-straw Rhizophagus intraradices Zea mays L. Cd concentration decreases in plant tissue Liu and Fan
(2018)
Soil nutrients Chips of spruce, pine Rhizophagus intraradices Glyceria striata Increase liming effect and an increase in Moland
and fir trees nutrient availability et al. (2018)
Plant growth Bamboo Rhizophagus, Gigaspora, Entrophospora, Theobroma cacao Increases the yield and growth of plant Aggangan
and Acaulospora sp. L. et al. (2019)
Physico-chemical 32 different biochar Rhizophagus sp. Trifolium Increased AMF colonization and plant Solaiman
parameters subterraneum and growth. et al. (2019)
Triticum aestivum
L.
Effect of phosphorus Sewage sludge Rhizophagus sp. Zea mays L Increased Microbial biomass carbon de
Figueiredo
et al. (2019)
Arsenic (As) Cow dung, sawdust, Rhizophagus sp. Vigna radiate L. AMF was relatively effective against As stress Alam et al.
and rice husk were (2019)
Cadmium (Cd) Rice straw Rhizophagus aggregatum, R.. intraradices, Medicago sativa Cd addition significantly decreased Zhang et al.
R. elunicatum and R. versiforme mycorrhizal colonization (2019b)
Soil N and N2O emission. Common reed grass Rhizophagus sp. Phragmites AMF increased CO2 emission and significantly Liang et al.
australis decreased soil inorganic N, especially when (2019)
biochar addition.
Drought stress Button mangrove Claroideoglomus etunicatum, Rhizophagus Cicer arietinum L. Improves growth of plant. Increases the Hashem
irregularis, and Funneliformis mosseae nitrogen fixation attributes. et al. (2019)
Soil fertility and crop Bamboo Rhizophagus, Gigaspora, Entrophospora, Theobroma cacao Biochar and AMF can improve the overall Aggangan
growth and Acaulospora. L. growth and increase the yield of cacao plants et al. (2019)
Total petroleum Oak leaves Rhizophagus etunicatum, Rhizophagus Trifolium arvense TPH reduced by 9.5% Abbaspour
hydrocarbons (TPH) intraradices and Rhizophagus mosseae and Malva et al. (2020)
sylvestris L.
Plant growth and Cd/Pb Charring plant or Funneliformis mosseae, Rhizophagus Zea mays L. Improves maize growth and decreasing Cd/Pb Zhuo et al.
accumulation animal biomass versiforme and Rhizophagus intraradices accumulation in maize. (2020)
Soil polluted from Pb Lignin biochar Funneliformis mosseae, Rhizophagus Hordeum vulgare Lead reduces below the critical limit in grain Khan et al.
(Lead) acid aggregatus, Claroideoglomus etunicatum of barley (2020b)
batteries and barley and Rhizophagus intraradices
grain
11
impact on bioactive compounds, thereby increasing the fruit yield revealing that relation between the biochar and AMF need to be
in tomatoes (Solanum lycopersicum) (Castan ~ eda et al., 2020). The taken into account while ameliorating the soil in different agro
majority of data on biochar applications focus on seedling re- climatic conditions. Otherwise, the amelioration could diminish the
sponses, physical and chemical improvement of soil, and microbial yield of the crops especially when only biochar is considered for
changes. However, long-term field experiments with AMF would amelioration. To overcome such issues, some advanced research
provide new insights into about water use, mycelia network and its focused on engineered biochar composites, sludge derived biochar,
functionality, soil aggregations, and mechanism of HMs absorption. and phosphogypsum (Cho et al., 2019; Yoo et al., 2018), which
A field study carried out by Warnock et al. (2007) revealed the apparently had wider applicability. Therefore, although many the-
positive effect on sorghum yield amendment with AMF and euca- ories and assumptions have been made regarding the mechanisms
lyptus biochar. Similar work was carried out using Glomus mosseae of biochar and AMF interactions inside the soil, conclusive and
as AMF incoula and Theobroma cacao L. as test species when comprehensive evidence is still unavailable.
bamboo biochar was applied to soil (Aggangan et al., 2019). Inside Among the many benefits, biochar and AMF applications have
the soil, plants acquire nutrients from the biochar using its AMF’s certain limitations; biochar applications are site-specific, compat-
extended root network, i.e. mycorrhizal hyphae. An experiment ibility of the AMF species depends upon feedstock used and feed-
conducted by Ibrahim (2016) suggested that with biochar appli- stock availability, and significantly varies among different
cations of 10 mg ha1 and 20 mg ha1, along with AMF shoot dry geographical areas. The functionality of biochar is not clearly un-
weight substantially increases from 0.99 to 1.92 g and 1.88e3.28 g derstood, and responses of soil to biochar and AMF impulses are
respectively. Another study on biochar applications with AMF still in the growing phase. Varied raw material options, emerging
species (Glomus sp., Gigaspora, Scutellospora, and Acaulospora) conversion technologies, and intermittent distribution channels
indicated an improvement in overall crop yield. Positive effects of with complicated landscape hinder these technological benefits.
BC þ AMF are not only limited to the rhizospheric zones of plants Hence, future suitability of biochar and AMF must be ensured
but also on the morphological parameters like greater floral clus- and supported by scientific evidence, which could help in avoiding
ters, more abundant leaves, more intensely coloured flowers and many adverse consequences. Biochar and AMF consortium must be
higher chlorophyll content (Conversa et al., 2015). Table 3 provides focused on meeting the needs of the end-user and emphasize the
a brief account of recent researches, which took place with the interconnectedness of stakeholders involved in various stages of
combined applications of BC þ AMF. production, logistic, conversion and end-use of biochar. A strategic
and systematic approach is necessary to assess the future potential
4.3. Challenges and future development of BC þ AMF applications of biochar with AMF. Varied and diverse biochar systems in terms of
production and application would help in providing site-specific
Globally, agriculture plays an essential role in the economies of solutions, which have the potential to tackle several issues at the
nations, yet soil pollution is a prevalent and persistent problem. The same time for achieving United Nation’s sustainable development
soil quality has a direct relationship to the yield of crops and its goals. Biochar obtained from locally available biomass has been
productivity. Thus, an attempt has been made to collate and discuss proposed as an innovative alternative for waste utilization and soil
scientific information regarding both biochar and AMF applications amelioration over the long term. Developing simple, cost-effective
for soil quality improvement. and practical method for utilizing biochar and AMF independently
Along with the wider perspectives of biochar properties on the or as consortium (BC þ AMF) is the challenge of this hour.
various agronomical and environmental backgrounds, one of the
prime objectives of the review was to explore different aspects of 5. Conclusions
biochar and AMF applications, their limitations, and present
knowledge, in soil quality improvement. However, optimum bio- Worldwide deterioration in soil quality has accelerated the food
char ratio depends upon the type and properties of both soil and scarcity and environmental challenges. However, green restoration
biochar. Numerous scientific attempts have showed that both fac- process using biochar coupled with AMF (BC þ AMF) might be a
tors could be vital for increasing the quality and quantity of crop suitable and sustainable option. Our review attempted to identify
yields (Table 4). and address the knowledge gaps in the potential role of BC þ AMF
The role of BC þ AMF has the potential to become a key strategy for soil quality rejuvenation. Biochar can provide a suitable habitat
for agro-ecosystems management and to make informed decisions for AMF, and their coupled application would lead to an increase in
with possible applicable and replicable outcomes for rural com- the overall biomass productivity, crop performance, and soil qual-
munities. Validated BC þ AMF applications would allow for more ity. It would also increase the root zone system of the plant by
confident adoption of techniques across the world. It is worth increasing the overall surface area for the retention of water and
Table 4
AMF’s dependency on different summer and winter crops.
Mycorrhiza’s dependency on different crops
Winter crops (Scientific name) Summer crops (Scientific name)
Linseed Linum usitatissimum þþþþþ Cotton Gossypium hirsutum þþþþþ

Faba Bean Vicia faba þþþþþ Sunflower Helianthus annuus þþþþ
Field pea Pisum sativum þþþ soybean Glycine max þþþþ
Oats Avena sativa þþþ Navy beans Phaseolus vulgaris þþþþ
Wheat Triticum aestivum þþþ Mung Bean Vigna radiata þþþþ
Triticale Triticosecale þþþ Maize Zea mays þþþþþ
Barley Hordeum vulgare L. þ Pigeon Pea Cajanus cajan þþþþþ
Canola Brassica napus L. - Lablab Lablab purpureus þþþþþ
Chickpea Cicer arietinum - Sorghum Sorghum bicolor þþþþ
Dependency legends: High ¼ þþþþþ; Moderate ¼ þþþþ; Low ¼ þþþ; Independent ¼

Note: Dependency scores is based on cited references in the review paper.
12
nutrients, which work particularly well for drought-affected areas. marine Chlorella sp. residue for bio-oil production as the biomass feedstock and
microwave absorber. Energy Convers. Manag. 195, 819e829.
It also reduces the dependence on chemical fertilizers by aug-
Anderson, C.R., Condron, L.M., Clough, T.J., Fiers, M., Stewart, A., Hill, R.A.,
menting nutrient uptake capacity of the plants. The overall effects Sherlock, R.R., 2011. Biochar induced soil microbial community change: impli-
of BC þ AMF are still unclear, further work is needed to elucidate cations for biogeochemical cycling of carbon, nitrogen and phosphorus. Pedo-
the long-term benefits. Most of the lab and field-based experiments biologia 54 (5e6), 309e320.
Awasthi, M.K., Duan, Y., Liu, T., Awasthi, S.K., Zhang, Z., 2020. Relevance of biochar to
across the globe pay more attention to the short-term individual influence the bacterial succession during pig manure composting. Bioresour.
effects of biochar and AMF, while the post-application life cycle Technol. 122962.
assessment of BC þ AMF is still at a nascent stage. The functional Azeem, M., Sun, D., Crowley, D., Hayat, R., Hussain, Q., Ali, A., Tahir, M.I.,
Jeyasundar, P.G.S.A., Rinklebe, J., Zhang, Z., 2020. Crop types have stronger ef-
relationships among biochar application and AMF colonization, and fects on soil microbial communities and functionalities than biochar or fertilizer
their collective roles in improving soil fertility require further in- during two cycles of legume-cereal rotations of dry land. Sci. Total Environ. 715,
vestigations in the future. 136958.
Bagheri, A., Abu-Danso, E., Iqbal, J., Bhatnagar, A., 2020. Modified biochar from
Moringa seed powder for the removal of diclofenac from aqueous solution.
Author statement Environ. Sci. Pollut. Res. 27 (7), 7318e7327.
Baruah, G., Sahu, J., 2019. A systematic review on the role of mycorrhiza in soil
genesis using scientometrics analysis. In: Mycorrhizosphere and Pedogenesis.
Nihal Gujre, contributed in carrying out investigation, data Springer, Singapore, pp. 95e109.
curuation, formal analysis and writing - original draft. Ankit Soni, Beesley, L., Dickinson, N., 2011. Carbon and trace element fluxes in the pore water of
assisted in literature review and draft preparation. Latha Rangan an urban soil following green waste compost woody and biochar amendments,
inoculated with the earthworm Lumbricus terrestris. Soil Biol. Biochem. 43,
and Daniel C.W. Tsang, took part in manuscript writing, reviewing 188e196.
and editing. Sudip Mitra, contributed in conceptulization, meth- Bengough, A.G., Mullins, C.E., 1990. Mechanical impedance to root growth: a review
odology, supervision, fund acquisition and writing - original draft of experimental techniques and root growth responses. J. Soil Sci. 41, 341e358.
Bhardwaj, Y., Sharma, M.P., Pandey, J., Dubey, S.K., 2020. Variations in microbial
and revising it. community in a tropical dry deciduous forest across the season and topo-
graphical gradient assessed through signature fatty acid biomarkers. Ecol. Res.
35 (1), 139e153.
Declaration of competing interest
Biederman, L.A., Harpole, W.S., 2013. Biochar and its effects on plant productivity
and nutrient cycling: a meta-analysis. GCB bioenergy 5 (2), 202e214.
The authors declare that they have no known competing Birk, J.J., Steiner, C., Teixeira, W.C., Zech, W., Glaser, B., 2009. Microbial response to
financial interests or personal relationships that could have charcoal amendments and fertilization of a highly weathered tropical soil. In:
Woods, W.I., Teixeira, W.G., Lehmann, J., Steiner, C., WinklerPrins, A.M.G.A.,
appeared to influence the work reported in this paper. Rebellato, L. (Eds.), Amazonian Dark Earths: Wim Sombroek’s Vision. Springer,
Berlin, pp. 309e324.
Biswas, S., Siddiqi, H., Meikap, B.C., Sen, T.K., Khiadani, M., 2020. Preparation and
Acknowledgement
characterization of raw and inorganic acid-activated pine cone biochar and its
application in the removal of aqueous-phase Pb 2þ metal ions by adsorption.
Sudip Mitra acknowledges the generous grant provided by the Water, Air, Soil Pollut. 231 (1), 3.
Blackwell, P., Krull, E., Butler, G., Herbert, A., Solaiman, Z., 2010. Effect of banded
Department of Biotechnology, Government of India, Twinning
biochar on dryland wheat production and fertilizer use in south-western
(DBT-NER/AGRI/29/2015). Nihal Gujre thanks IIT Guwahati for Australia: an agronomic and economic perspective. Aust. J. Soil Res. 48,
providing him the Senior Research Fellowship. 531e545.
Bourles, A., Guentas, L., Charvis, C., Gensous, S., Majorel, C., Crossay, T., Cavaloc, Y.,
Burtet-Sarramegna, V., Jourand, P., Amir, H., 2020. Co-inoculation with a bac-
References terium and arbuscular mycorrhizal fungi improves root colonization. plant
mineral nutrition, and plant growth of a Cyperaceae plant in an ultramafic soil
Abbaspour, A., Zohrabi, F., Dorostkar, V., Faz, A., Acosta, J.A., 2020. Remediation of an 1e11. Mycorrhiza.
oil-contaminated soil by two native plants treated with biochar and mycor- Brewer, C.E., Brown, R.C., 2012. Biochar. In: Sayigh, A. (Ed.), Comprehensive
rhizae. J. Environ. Manag. 254, 109755. Renewable Energy. Elsevier, Oxford, pp. 357e384.
Abdin, Y., Usman, A., Ok, Y.S., Tsang, Y.F., Al-Wabel, M., 2020. Competitive sorption Caban, M., Folentarska, A., Lis, H., Kobylis, P., Kumirska, J., Stepnowski, P.,
and availability of coexisting heavy metals in mining-contaminated soil: con- Ciesielski, W., 2019. Valuable polar moieties on cereal-derived biochars. Col-
trasting effects of mesquite and fishbone biochars. Environ. Res. 181, 108846. loids Surf. A Physicochem. Eng. Asp. 561, 275e282.
Adeyemi, N.O., Atayese, M.O., Olubode, A.A., Akan, M.E., 2020. Effect of commercial Cabral, C., Wollenweber, B., Anto nio, C., Ravnskov, S., 2019. Activity in the arbuscular
arbuscular mycorrhizal fungi inoculant on growth and yield of soybean under mycorrhizal hyphosphere warning neighbouring plants. Front. Plant Sci. 10, 511.
controlled and natural field conditions. J. Plant Nutr. 43 (4), 487e499. Camelo, A., Genuino, D.A., Maglinao Jr, A.L., Capareda, S.C., Paes, J.L.,
Aggangan, N.S., Cortes, A.D., Rean ~ o, C.E., 2019. Growth response of cacao (Theo- Owkusumsirisakul, J., 2018. Pyrolysis of pearl millet and napier grass hybrid
broma cacao L.) plant as affected by bamboo biochar and arbuscular mycorrhizal (PMN10TX15): feasibility, byproducts, and comprehensive characterization. Int.
fungi in sterilized and unsterilized soil. Biocat. Agri. Biotechnol. 22, 101347. J. Renew. Energy Resour. 8 (2), 682e691.
Ahmad, M., Rajapaksha, A.U., Lim, J.E., Zhang, M., Bolan, N., Mohan, D., 2014. Biochar Castan~ eda, W., Toro, M., Solorzano, A., Zún ~ iga-Da
vila, D., 2020. Production and
as a sorbent for contaminant management in soil and water: a review. Che- nutritional quality of Tomatoes (Solanum lycopersicum var. Cerasiforme) are
mosphere 99, 19e33. improved in the presence of Biochar and inoculation with arbuscular mycor-
Ahmed, M.J., Hameed, B.H., 2018. Adsorption behavior of salicylic acid on biochar as rhizae. Am. J. Plant Sci. 11 (3), 426e436.
derived from the thermal pyrolysis of barley straws. J. Clean. Prod. 195, Cayuela, M.L., Van Zwieten, L., Singh, B.P., Jeffery, S., Roig, A., Sanchez-
1162e1169. Monedero, M.A., 2014. Biochar’s role in mitigating soil nitrous oxide emissions:
Al-Arjani, A.B.F., Hashem, A., Abd_Allah, E.F., 2020. Arbuscular mycorrhizal fungi a review and meta-analysis. Agric. Ecosyst. Environ. 191, 5e16.
modulates dynamics tolerance expression to mitigate drought stress in Ephedra Cha, J.S., Park, S.H., Jung, S.C., Ryu, C., Jeon, J.K., Shin, M.C., Park, Y.K., 2016. Pro-
foliata Boiss. Saudi J. Biol. Sci. 27 (1), 380e394. duction and utilization of biochar: a review. J. Ind. Eng. Chem. 40, 1e15.
Al-Shamma, S., Backhouse, D., Cowie, A., Wilson, S.C., 2017. Mycorrhiza and Biochar Chai, Y.Z., Currie, R.J., Davis, J.W., Wilken, M., Martin, G.D., Fishman, V.N., Ghosh, U.,
for Remediation and Plant Production in Soils Polluted with Arsenic accessed. 2012. Effectiveness of activated carbon and biochar in reducing the availability
https://hdl.handle.net/1959.11/22588. (Accessed 14 July 2020). of polychlorinated dibenzo-p-dioxins/dibenzofurans in soils. Environ. Sci.
Alam, M.Z., McGee, R., Hoque, M.A., Ahammed, G.J., Carpenter-Boggs, L., 2019. Effect Technol. 46, 1035e1043.
of arbuscular mycorrhizal fungi, selenium and biochar on photosynthetic pig- Chen, B.L., Yuan, M.X., 2011. Enhanced sorption of polycyclic aromatic hydrocarbons
ments and antioxidant enzyme activity under arsenic stress in mung bean by soil amended with biochar. J. Soils Sediments 11, 62e71.
(Vigna radiata). Front. Physiol. 10, 193. Chintala, R., Owen, R., Kumar, S., Schumacher, T.E., Malo, D., 2014. Biochar impacts
Ali, S., Rizwan, M., Shakoor, M.B., Jilani, A., Anjum, R., 2020. High sorption efficiency on denitrification under different soil water contents. World Cong. Soil Sci. 6,
for as (III) and as (V) from aqueous solutions using novel almond shell biochar. 157.
Chemosphere 243, 125e330. Cho, D.W., Yoon, K., Ahn, Y., Sun, Y., Tsang, D.C., Hou, D., Ok, Y.S., Song, H., 2019.
Amendola, C., Montagnoli, A., Terzaghi, M., Trupiano, D., Oliva, F., Baronti, S., Fabrication and environmental applications of multifunctional mixed metal-
Miglietta, F., Chiatante, D., Scippa, G.S., 2017. Short-term effects of biochar on biochar composites (MMBC) from red mud and lignin wastes. J. Hazard
grapevine fine root dynamics and arbuscular mycorrhizae production. Agric. Mater. 374, 412e419.
Ecosyst. Environ. 239, 236e245. Conversa, G., Bonasia, A., Lazzizera, C., Elia, A., 2015. Influence of biochar, mycor-
Amin, M., Chetpattananondh, P., Ratanawilai, S., 2019. Application of extracted rhizal inoculation, and fertilizer rate on growth and flowering of Pelargonium
13
(Pelargonium zonale L.) plants. Front. Plant Sci. 6, 429. Biochar production and applications in sub- Saharan Africa: opportunities,
Corbin, J.D., Avis, P.G., Wilbur, R.B., 2003. The role of phosphorus availability in the constraints, risks and uncertainties. J. Environ. Manag. 150, 250e261.
response of soil nitrogen cycling, understory vegetation and arbuscular Hammer, E.C., Balogh-Brunstad, Z., Jakobsen, I., Olsson, P.A., Stipp, S.L.S., Rillig, M.C.,
mycorrhizal inoculum potential to elevated nitrogen inputs. Water, Air, Soil 2014. A mycorrhizal fungus grows on biochar and captures phosphorus from its
Pollut. 147, 141e161. surfaces. Soil Biol. Biochem. 77, 252e260.
Covacevich, F., Marino, M.A., Echeverrica, H.E., 2006. The phosphorus source de- Hammer, E.C., Forstreuter, M., Rillig, M.C., Kohler, J., 2015. Biochar increases
termines the arbuscular mycorrhizal potential and the native mycorrhizal arbuscular mycorrhizal plant growth enhancement and ameliorates salinity
colonization of tall fescue and wheat grass. Eur. J. Soil Biol. 42, 127e138. stress. Appl. Soil Ecol. 96, 114e121.
Cui, H.J., Wang, M.K., Fu, M.L., Ci, E., 2011. Enhancing phosphorus availability in Han, Y., Douds Jr., D.D., Boateng, A.A., 2016. Effect of biochar soil-amendments on
phosphorus-fertilized zones by reducing phosphate adsorbed on ferrihydrite Allium porrum growth and arbuscular mycorrhizal fungus colonization. J. Plant
using rice straw-derived biochar. J. Soils Sediments 11 (7), 1135. Nutr. 39 (11), 1654e1662.
de Figueiredo, C.C., Chagas, J.K.M., da Silva, J., Paz-Ferreiro, J., 2019. Short-term ef- Hashem, A., Kumar, A., Al-Dbass, A.M., Alqarawi, A.A., Al-Arjani, A.B.F., Singh, G.,
fects of a sewage sludge biochar amendment on total and available heavy metal Farooq, M., Abd_Allah, E.F., 2019. Arbuscular mycorrhizal fungi and biochar
content of a tropical soil. Geoderma 344, 31e39. improves drought tolerance in chickpea. Saudi J. Biol. Sci. 26 (3), 614e624.
Delavaux, C.S., Weigelt, P., Dawson, W., Duchicela, J., Essl, F., van Kleunen, M., He, L., Liu, Y., Zhao, J., Bi, Y., Zhao, X., Wang, S., Xing, G., 2016. Comparison of
Ko€ nig, C., Pergl, J., Pysek, P., Stein, A., Winter, M., 2019. Mycorrhizal fungi in- strawbiochar- mediated changes in nitrification and ammonia oxidizers in
fluence global plant biogeography. Nat. Ecol. Evol. 3 (3), 424e429. agricultural oxisols and cambosols. Biol. Fertil. Soils 52 (2), 137e149.
Devi, P., Kothari, P., Dalai, A.K., 2020. Stabilization and solidification of arsenic and He, Y.M., Yang, R., Lei, G., Li, B., Jiang, M., Yan, K., Zu, Y.Q., Zhan, F.D., Li, Y., 2020.
iron contaminated canola meal biochar using chemically modified phosphate Arbuscular mycorrhizal fungi reduce cadmium leaching from polluted soils
binders. J. Hazard Mater. 385, 121559. under simulated heavy rainfall. Environ. Pollut. 263, 114406.
Efthymiou, A., Jensen, B., Jakobsen, I., 2018. The roles of mycorrhiza and Penicillium Ho, S.H., Chen, Y.D., Yang, Z.K., Nagarajan, D., Chang, J.S., Ren, N.Q., 2017. High-ef-
inoculants in phosphorus uptake by biochar-amended wheat. Soil Biol. Bio- ficiency removal of lead from wastewater by biochar derived from anaerobic
chem. 127, 168e177. digestion sludge. Bioresour. Technol. 246, 142e149.
El-Naggar, A., Lee, S.S., Awad, Y.M., Yang, X., Ryu, C., Rizwan, M., Rinklebe, J., Hu, Q., Yang, H., Wu, Z., Lim, C.J., Bi, X.T., Chen, H., 2019. Experimental and modeling
Tsang, D.C., Ok, Y.S., 2018. Influence of soil properties and feedstocks on biochar study of potassium catalyzed gasification of woody char pellet with CO2. Energy
potential for carbon mineralization and improvement of infertile soils. Geo- 171, 678e688.
derma 332, 100e108. Huang, L.Q., Fu, C., Li, T.Z., Yan, B., Wu, Y., Zhang, L., Ping, W., Yang, B.R., Chen, L.,
El-Naggar, A., El-Naggar, A.H., Shaheen, S.M., Sarkar, B., Chang, S.X., Tsang, D.C., 2020. January. Advances in research on effects of biochar on soil nitrogen and
Rinklebe, J., Ok, Y.S., 2019. Biochar composition-dependent impacts on soil phosphorus. In: IOP Conference Series: Earth and Environmental Science, vol.
nutrient release, carbon mineralization, and potential environmental risk: a 424. IOP Publishing, 012015.
review. J. Environ. Manag. 241, 458e467. Ibrahim, Ortas, 2016. The role of mycorrhizae and biochar in plant growth and soil
El-Naggar, A., Lee, M.H., Hur, J., Lee, Y.H., Igalavithana, A.D., Shaheen, S.M., Ryu, C., quality. In: Bruckman, V.J., Vraol, E.A., Uzun, B.B., Liu, J. (Eds.), Biochar: A
Rinklebe, J., Tsang, D.C., Ok, Y.S., 2020. Biochar-induced metal immobilization Regional Supply Chain Approach in View of Climate Change Mitigation. Cam-
and soil biogeochemical process: an integrated mechanistic approach. Sci. Total bridge University Press, Newyork, pp. 336e350.
Environ. 698, 134112. Igalavithana, A.D., Lee, S.E., Lee, Y.H., Tsang, D.C., Rinklebe, J., Kwon, E.E., Ok, Y.S.,
Elmer, W.H., Pignatello, J.J., 2011. Effect of biochar amendments on mycorrhizal 2017. Heavy metal immobilization and microbial community abundance by
associations and Fusarium crown and root rot of asparagus in replant soils. vegetable waste and pine cone biochar of agricultural soils. Chemosphere 174,
Plant Dis. 95, 960e966. 593e603.
Elzobair, K.A., Stromberger, M.E., Ippolito, J.A., Lentz, R.D., 2016. Contrasting effects Ippolito, J.A., Cui, L., Novak, J.M., Johnson, M.G., 2019. Biochar for Mine-Land
of biochar versus manure on soil microbial communities and enzyme activities Reclamation in: Biochar from Biomass and Waste. Elsevier, pp. 75e90.
in an Aridisol. Chemosphere 142, 145e152. Ishii, T., Kadoya, K., 1994. Effects of charcoal as a soil conditioner on citrus growth
Fang, J., Zhan, L., Ok, Y.S., Gao, B., 2018. Mini review of potential applications of and vesicular-arbuscular mycorrhizal development. J. Jpn. Soc. Hortic. Sci. 63,
hydrochar derived from hydrothermal carbonization of biomass. J. Ind. Eng. 529e535.
Chem. 57, 15e21. Jaafar, N.M., Clode, P.L., Abbott, L.K., 2014. Microscopy observations of habitable
Fischer, D., Glaser, B., 2012. Synergisms between compost and biochar for sus- space in biochar for colonisation by fungal hyphae from soil. J. Integr. Agr. 13,
tainable soil amelioration. In: Kumar, S., Bharti, A. (Eds.), Management of 483e490.
Organic Waste. In Tech, Rijeka, Croatia Functions in Soil, vol. 105. Advances in Janeeshma, E., Puthur, J.T., 2020. Direct and indirect influence of arbuscular
Agronomy, pp. 47e82. mycorrhizae on enhancing metal tolerance of plants. Arch. Microbiol. 202 (1),
Foo, K.Y., Hameed, B.H., 2012. Porous structure and adsorptive properties of pine- 1e16.
apple peel based activated carbons prepared via microwave assisted KOH and Jia, X., Zhao, Y., Liu, T., Huang, S., Chang, Y., 2016. Elevated CO2 increases glomalin-
K2CO3 activation. Microporous Mesoporous Mater. 148 (1), 191e195. related soil protein (GRSP) in the rhizosphere of Robinia pseudoacacia L. seed-
Gaunt, J.L., Lehmann, J., 2008. Energy balance and Emissions associated with bio- lings in Pb-and Cd-contaminated soils. Environ. Pollut. 218, 349e357.
char sequestration and pyrolysis bioenergy production. Environ. Sci. Technol. Jindo, K., Mizumoto, H., Sawada, Y., Sanchez-Monedero, M.A., Sonoki, T., 2014.
42, 4152e4158. Physical and chemical characterization of biochars derived from different
Gaur, A., Adholeya, A., 2000. Effects of the particle size of soil-less substrates upon agricultural residues. Biogeosciences 11 (23), 6613e6621.
AM fungus inoculum production. Mycorrhiza 10, 43e48. Kamel, L., Keller-Pearson, M., Roux, C., Ane , J.M., 2017. Biology and evolution of
GCC (Global Climate Change), 2020. Global climate change vital signs of the planet. arbuscular mycorrhizal symbiosis in the light of genomics. New Phytol. 213 (2),
NASA. Accessed on. https://climate.nasa.gov/vital-signs/carbon-dioxide/. 531e536.
(Accessed 23 May 2020) Kameyama, K., Miyamoto, T., Iwata, Y., Shiono, T., 2016. Influences of feedstock and
Giller, K.E., 2001. Nitrogen Fixation in Tropical Cropping Systems, second ed. CAB pyrolysis temperature on the nitrate adsorption of biochar. J. Soil Sci. Plant Nutr.
International, Wallingford. 62 (2), 80e184.
_
Glab, T., Zabi n ski, A., Sadowska, U., Gondek, K., Kope c, M., Mierzwa-Hersztek, M., Kazemi, R., Ronaghi, A., Yasrebi, J., Ghasemi-Fasaei, R., Zarei, M., 2019. Effect of
Tabor, S., Stanek-Tarkowska, J., 2020. Fertilization effects of compost produced shrimp wasteederived biochar and arbuscular mycorrhizal fungus on yield,
from maize, sewage sludge and biochar on soil water retention and chemical antioxidant enzymes, and chemical composition of corn under salinity stress.
properties. Soil Till. Res. 197, 104493. J. Soil Sci. Plant Nutr. 19 (4), 758e770.
Godoy, R., Silva-Flores, P., Aguilera, P., Marín, C., 2017. Microbial Interactions in the Khan, M.B., Cui, X., Jilani, G., Lazzat, U., Zehra, A., Hamid, Y., Hussain, B., Tang, L.,
plant-soil continuum. J. Soil Sci. Plant Nutr. 17 (4), 1e3. Yang, X., He, Z., 2019a. Eisenia fetida and biochar synergistically alleviate the
Gonz alez-Cha vez, M.D.C.A., Carrillo-Gonza lez, R., Hernandez Godinez, M.I., Evan- heavy metals content during valorization of biosolids via enhancing vermi-
gelista Lozano, S., 2017. Jatropha curcas and assisted phytoremediation of a compost quality. Sci. Total Environ. 684, 597e609.
mine tailing with biochar and a mycorrhizal fungus. Int. J. Phytoremediation 19 Khan, M.B., Cui, X., Jilani, G., Ting, Y., Zehra, A., Hamid, Y., Hussain, B., Tang, L.,
(2), 174e182. Yang, X., He, Z., 2019b. Preincubation and vermicomposting of divergent bio-
Grant, C., Bittman, S., Montreal, M., Plenchette, C., More, C., 2005. Soil and fertilizer solids exhibit vice versa multielements stoichiometry and earthworm physi-
phosphorus: effect on plant P supply and mycorrhizal development. Can. J. ology. J. Environ. Manag. 243, 144e156.
Plant Sci. 85, 3e14. Khan, M.B., Cui, X., Jilani, G., Tang, L., Lu, M., Cao, X., Sahito, Z.A., Hamid, Y.,
Gryndler, M., Larsen, J., Hrselovac, H., Rezaccovac, V., Gryndlerovac, H., Kubact, J., Hussain, B., Yang, X., He, Z., 2020a. New insight into the impact of biochar
2006. Organic and mineral fertilization, respectively, increase and decrease the during vermi-stabilization of divergent biowastes: literature synthesis and
development of external mycelium of arbuscular mycorrhizal fungi in a long- research pursuits. Chemosphere 238, 124679.
term field experiment. Mycorrhiza 16, 159e166. Khan, M.A., Ramzani, P.M.A., Zubair, M., Rasool, B., Khan, M.K., Ahmed, A., Khan, S.A.,
Gu, S., Wu, S., Guan, Y., Zhai, C., Zhang, Z., Bello, A., Guo, X., Yang, W., 2020. Turan, V., Iqbal, M., 2020b. Associative effects of lignin-derived biochar and
Arbuscular mycorrhizal fungal community was affected by tillage practices arbuscular mycorrhizal fungi applied to soil polluted from Pb-acid batteries
rather than residue management in black soil of northeast China. Soil Till. Res. effluents on barley grain safety. Sci. Total Environ. 710, 136294.
198, 104552. Killham, K., 1985. A physiological determination of the impact of environmental
Gul, S., Whalen, J.K., 2016. Biochemical cycling of nitrogen and phosphorus in stress on the activity of microbial biomass. Environ. Poll. Ser. A. 38 (3),
biochar-amended soils. Soil Biol. Biochem. 103, 1e15. 283e294.
Gwenzi, W., Chaukura, N., Mukome, F.N.D., Machado, S., Nyamasoka, B., 2015. Killham, K., Firestone, M.K., 1984. Salt stress control of intracellular solutes in
14
Streptomycetes indigenous to saline soils. Appl. Environ. Microbiol. 47, Lonappan, L., Liu, Y., Rouissi, T., Brar, S.K., Surampalli, R.Y., 2020. Development of
301e306. biochar-based green functional materials using organic acids for environmental
Kim, H.-S., Kim, K.-R., Yang, J.E., Ok, Y.S., Owens, G., Nehls, T., Wessolek, G., Kim, K.- applications. J. Clean. Prod. 244, 118841.
H., 2016. Effect of biochar on reclaimed tidal land soil properties and maize (Zea Lopez-Obando, M., Ligerot, Y., Bonhomme, S., Boyer, F.D., Rameau, C., 2015. Strigo-
mays L.) response. Chemosphere 142, 153e159. lactone biosynthesis and signaling in plant development. Development 142,
Kipkoriony, L.R., Fusao, M., 2006. Effect of mycorrhizal inoculation and activated 3615e3619.
charcoal on growth and nutrition in peach (Prunus persica) seedlings treated Lubbers, I.M., Van Groenigen, K.J., Fonte, S.J., Six, J., Brussaard, L., Van
with peach root-bark extracts. J. Jpn. Soc. Hortic. Sci. 75 (6), 463. Groenigen, J.W., 2013. Greenhouse-gas emissions from soils increased by
Klupfel, L., Keiluweit, M., Kleber, M., Sander, M., 2014. Redox properties of plant earthworms. Nat. Clim. Change 3, 187e194.
biomass-derived black carbon (biochar). Environ. Sci. Technol. 48, 5601e5611. Luo, S., Wang, S., Tian, L., Li, S., Li, X., Shen, Y., Tian, C., 2017. Long-term biochar
Kokkoris, V., Pogiatzis, A., Hart, M.M., 2019. Contrasting common measures of application influences soil microbial community and its potential roles in
arbuscular mycorrhizal fungal root colonization. J. Microbiol. Methods 167, semiarid farmland. Appl. Soil Ecol. 117, 10e15.
05727. Madiba, O.F., Solaiman, Z.M., Carson, J.K., Murphy, D.V., 2016. Biochar increases
Kong, L., Gao, Y., Zhou, Q., Zhao, X., Sun, Z., 2018. Biochar accelerates PAHs availability and uptake of phosphorus to wheat under leaching conditions. Biol.
biodegradation in petroleum-polluted soil by biostimulation strategy. J. Hazard Fertil. Soils 52 (4), 439e446.
Mater. 343, 276e284. Magurno, F., Malicka, M., Posta, K., Wozniak, G., Lumini, E., Piotrowska-Seget, Z.,
Koyama, A., Maherali, H., Antunes, P.M., 2019. Plant geographic origin and phy- 2019. Glomalin gene as molecular marker for functional diversity of arbuscular
logeny as potential drivers of community structure in root-inhabiting fungi. mycorrhizal fungi in soil. Biol. Fertil. Soils 55 (4), 411e417.
J. Ecol. 107 (4), 1720e1736. Maherali, H., Oberle, B., Stevens, P.F., Cornwell, W.K., McGlinn, D.J., 2016. Mutualism
Krishnamoorthy, R., Venkatramanan, V., Senthilkumar, M., Anandham, R., persistence and abandonment during the evolution of the mycorrhizal symbi-
Kumutha, K., Sa, T., 2019. Management of heavy metal polluted soils: osis. Am. Nat. 188 (5), 13e125.
perspective of arbuscular mycorrhizal fungi. In: Sustainable Green Technologies Major, J., Steiner, C., Downie, A., Lehmann, J., 2009. Biochar effects on nutrient
for Environmental Management. Springer, Singapore, pp. 67e85. leaching. In: Lehmann, J., Joseph, S. (Eds.), Biochar for Environmental Man-
Kumar, S., Masto, R.E., Ram, L.C., Sarkar, P., George, J., Selvi, V.A., 2013. Biochar agement Science and Technology. Earthscan, London, pp. 271e287.
preparation from Parthenium hysterophorus and its potential use in soil appli- Malik, Z., Shah, Z., Tariq, M., 2019. Biochar improves viability of arbuscular
cation. Ecol. Eng. 55, 67e72. mycorrhizal fungi (AMF) in soil and roots of wheat (Triticum aestivum) and
Laird, D.A., Brown, R.C., Amonette, J.E., Lehmann, J., 2009. Review of the pyrolysis maize (Zea mays L.) under various cropping systems. Sarhad J. Agric. 35 (3),
platform for co-producing bio-oil and biochar. Biofuel Bioprod. Bior. 3, 834e846.
547e562. Mandal, A., Singh, N., Purakayastha, T.J., 2017. Characterization of pesticide sorption
LeCroy, C., Masiello, C.A., Rudgers, J.A., Hockaday, W.C., Silberg, J.J., 2013. Nitrogen, behaviour of slow pyrolysis biochars as low cost adsorbent for atrazine and
biochar, and mycorrhizae: alteration of the symbiosis and oxidation of the char imidacloprid removal. Sci. Total Environ. 577, 376e385.
surface. Soil Biol. Biochem. 58, 248e253l. Mathur, S., Tomar, R.S., Jajoo, A., 2019. Arbuscular mycorrhizal fungi (AMF) protects
Lee, J.W., Hawkins, B., Kidder, M.K., Evans, B.R., Buchanan, A.C., Day, D., 2016. photosynthetic apparatus of wheat under drought stress. Photosynth. Res. 139
Characterization of biochars produced from peanut hulls and pine wood with (1e3), 227e238.
different pyrolysis conditions. Bioresour. Bioprocess. 3 (1), 15. Matsubara, Y., Hasegawa, N., Fukui, H., 2002. Incidence of Fusarium root rot in
Lehman, R.M., Osborne, S.L., Taheri, W.I., Buyer, J.S., Chim, B.K., 2019. Comparative asparagus seedlings infected with arbuscular mycorrhizal fungus as affected by
measurements of arbuscular mycorrhizal fungal responses to agricultural several soil amendments. J. Jpn. Soc. Hortic. Sci. 71, 370e374.
management practices. Mycorrhiza 29 (3), 227e235. Mau, A.E., Utami, S.R., 2014. Effects of biochar amendment and arbuscular mycor-
Lehmann, J., Joseph, S., 2015. Biochar for Environmental Management: Science, rhizal fungi inoculation on availability of soil phosphorus and growth of maize.
Technology and Implementation. Routledge. J. Degrade. Min. Land Manage. 1 (2), 69.
Lehmann, J., Rondon, M., 2006. Bio-char soil management on highly weathered soils Mia, S., Van Groenigen, J., Van de Voorde, T., Oram, N., Bezemer, T., Mommer, L.,
in the humid tropics. In: Uphoff, N., Ball, A.S., Fernandes, E., Herren, H., Jeffery, S., 2014. Biochar application rate affects biological nitrogen fixation in
Husson, O., Laing, M., Palm, C., Pretty, J., Sanchez, P., Sanginga, N., Thies, J. (Eds.), red clover conditional on potassium availability. Agric. Ecosyst. Environ. 191,
Biological Approaches to Sustainable Soil Systems. Taylor and Francis Group, 83e91.
Boca Raton, pp. 517e530. Mian, M.M., Liu, G., Yousaf, B., Fu, B., Ahmed, R., Abbas, Q., Munir, M.A.M., Ruijia, L.,
Lehmann, J., da Silva Jr., J.P., Steiner, C., Nehls, T., Zech, W., Glaser, B., 2003. Nutrient 2019. One-step synthesis of N-doped metal/biochar composite using NH3-
availability and leaching in an archaeological Anthrosol and a Ferralsol of the ambiance pyrolysis for efficient degradation and mineralization of Methylene
Central Amazon basin: fertilizer, manure and charcoal amendments. Plant Soil Blue. J. Environ. Sci. 78, 29e41.
249, 343e357. Mickan, B.S., Abbott, L.K., Stefanova, K., Solaiman, Z.M., 2016. Interactions between
Lehmann, J., Rillig, M.C., Thies, J., Masiello, C.A., Hockaday, W.C., Crowley, D., 2011. biochar and mycorrhizal fungi in a water-stressed agricultural soil. Mycorrhiza
Biochar effects on soil biota e a review. Soil Biol. Biochem. 43, 1812e1836. 26 (6), 565e574.
Lenoir, I., Lounes-Hadj Sahraoui, A., Fontaine, J., 2016. Arbuscular mycorrhizal Mitra, S., Singh, P., Manzoor, S., Bhattacharyya, P., Bera, T., Kumar Patra, A.,
fungal-assisted phytoremediation of soil contaminated with persistent organic Rangan, L., Borah, P., 2016. Can rice and wheat biochar amendment protect the
pollutants: a review. Eur. J. Soil Sci. 67 (5), 624e640. carbon loss from tropical soils-An experimental study. Environ. Prog. Sustain.
Li, Q., Zhang, H., Guo, S., Fu, K., Liao, L., Xu, Y., Cheng, S., 2019. Groundwater pollution Energy 35 (1), 183e188.
source apportionment using principal component analysis in a multiple land- Mohan, D., Kumar, H., Sarswat, A., Alexandre-Franco, M., Pittman Jr, C.U., 2014.
use area in southwestern China. Environ. Sci. Pollut. Res. 27, 9000e9011. Cadmium and lead remediation using magnetic oak wood and oak bark fast
Liang, J.F., An, J., Gao, J.Q., Zhang, X.Y., Song, M.H., Yu, F.H., 2019. Interactive effects of pyrolysis bio-chars. Chem. Eng. J. 236, 513e528.
biochar and AMF on plant growth and greenhouse gas emissions from wetland Moland, S., Robicheau, B.M., Browne, R., Newell, R., Walker, A.K., 2018. Determining
microcosms. Geoderma 346, 11e17. the effects of biochar and an arbuscular mycorrhizal inoculant on the growth of
Lilleskov, E.A., Kuyper, T.W., Bidartondo, M.I., Hobbie, E.A., 2019. Atmospheric ni- fowl mannagrass (Glyceria striata) (Poaceae). FACETS 3 (1), 441e454.
trogen deposition impacts on the structure and function of forest mycorrhizal Mukherjee, A., Zimmerman, A.R., 2013. Organic carbon and nutrient release from a
communities: a review. Environ. Pollut. 246, 148e162. range of laboratory-produced biochars and biocharesoil mixtures. Geoderma,
Liu, L., Fan, S., 2018. Removal of cadmium in aqueous solution using wheat straw 193, pp. 122e130.
biochar: effect of minerals and mechanism. Environ. Sci. Pollut. Res. 25 (9), Munera-Echeverri, J.L., Martinsen, V., Strand, L.T., Cornelissen, G., Mulder, J., 2020.
8688e8700. Effect of conservation farming and biochar addition on soil organic carbon
Liu, C., Liu, F., Ravnskov, S., Rubæk, G.H., Sun, Z., Andersen, M.N., 2017. Impact of quality, nitrogen mineralization, and crop productivity in a light textured
wood biochar and its interactions with mycorrhizal fungi, phosphorus fertil- Acrisol in the sub-humid tropics. PloS One 15 (2), e0228717.
ization and irrigation strategies on potato growth. J. Agron. Crop Sci. 203 (2), Narzari, R., Bordoloi, N., Sarma, B., Gogoi, L., Gogoi, N., Borkotoki, B., Kataki, R., 2017.
131e145. Fabrication of biochars obtained from valorization of biowaste and evaluation of
Liu, L., Li, J., Yue, F., Yan, X., Wang, F., Bloszies, S., Wang, Y., 2018. Effects of arbuscular its physicochemical properties. Bioresour. Technol. 242, 324e328.
mycorrhizal inoculation and biochar amendment on maize growth, cadmium Ncibi, M.C., Jeanne Rose, V., Mahjoub, B., 2009. Preparation and characterization of
uptake and soil cadmium speciation in Cd-contaminated soil. Chemosphere raw char and physically activated carbons derived from marine Posidonia oce-
194, 495e503. anica(L.) fibres. J. Hazard Mater. 165, 240e249.
Liu, M., Che, Y., Wang, L., Zhao, Z., Zhang, Y., Wei, L., Xiao, Y., 2019. Rice straw biochar Nguyen, T.T.N., Wallace, H.M., Xu, C.Y., Zwieten, L.V., Weng, Z.H., Xu, Z., Che, R.,
and phosphorus inputs have more positive effects on the yield and nutrient Tahmasbian, I., Hu, H.W., Bai, S.H., 2018. The effects of short term, long term and
uptake of Lolium multiflorum than arbuscular mycorrhizal fungi in acidic Cd- reapplication of biochar on soil bacteria. Sci. Total Environ. 636, 142e151.
contaminated soils. Chemosphere 235, 32e39. Niazi, N.K., Bibi, I., Shahid, M., Ok, Y.S., Burton, E.D., Wang, H., Shaheen, S.M.,
Liu, M., Zhao, Z., Chen, L., Wang, L., Ji, L., Xiao, Y., 2020. Influences of arbuscular Rinklebe, J., Lüttge, A., 2018. Arsenic removal by perilla leaf biochar in aqueous
mycorrhizae, phosphorus fertiliser and biochar on alfalfa growth, nutrient solutions and groundwater: an integrated spectroscopic and microscopic ex-
status and cadmium uptake. Ecotoxicol. Environ. Saf. 196, 110537. amination. Environ. Pollut. 232, 31e41.
Lomba, A., Buchadas, A., Honrado, J.P., Moreira, F., 2019. Are we missing the big Noguera, D., Rondon, M., Laossi, K.-R., Hoyos, V., Lavelle, P., de Carvalho, M.H.C.,
picture? Unlocking the social-ecological resilience of high nature value farm- Barot, S., 2010. Contrasted effect of biochar and earthworms on rice growth and
lands to future climate change. In: Climate Change-Resilient Agriculture and resource allocation in different soils. Soil Biol. Biochem. 42, 1017e1027.
Agroforestry. Springer, Cham, pp. 53e72. Nursyamsi, D., Setyorini, D., 2009. Availability of P in neutral and alkaline soils.
15
J. Soil Clim. 30, 1e12 (in Indonesian). Mycorrhizas. Springer, Dordrecht, pp. 273e279.
Nzanza, B., Marais, D., Soundy, P., 2012. In: Effect of Arbuscular Mycorrhizal Fungal IPBES, Scholes, R., Montanarella, L., Brainich, A., Barger, N., ten Brink, B., Cantele, M.,
Inoculation and Biochar Amendment on Growth and Yield of Tomato. https:// Erasmus, B., Fisher, J., Gardner, T., Holland, T.G., Kohler, F., Kotiaho, J.S., Von
repository.up.ac.za/handle/2263/20948. Maltitz, G., Nangendo, G., Pandit, R., Parrotta, J., Potts, M.D., Prince, S.,
O’Connor, D., Peng, T., Zhang, J., Tsang, D.C., Alessi, D.S., Shen, Z., Bolan, N.S., Hou, D., Sankaran, M., 2018. In: Willemen, L. (Ed.), Summary for Policymakers of the
2018. Biochar application for the remediation of heavy metal polluted land: a Assessment Re-port on Land Degradation and Restoration of the Intergovern-
review of in situ field trials. Sci. Total Environ. 619, 815e826. mental Science Policy Platform on Biodiversity and Ecosystem Services. IPBES
Ogawa, M., Okimori, Y., Takahashi, F., 2006. Carbon sequestration by carbonization Secretariat, Bonn, Germany. https://www.ipbes.net/system/tdf/spm_3bi_ldr_
of biomass and forestation: three case studies. Mitig. Adapt. Strategies Glob. digital.pdf?file¼1&type¼node&id¼28335.
Change 11, 429e444. Secilia, J., Bagyaraj, D.J., 1988. Fungi associated with pot cultures of vesicular-
Oginni, O., Yakaboylu, G.A., Singh, K., Sabolsky, E.M., Unal-Tosun, G., Jaisi, D., arbuscular mycorrhizas. Trans. Br. Mycol. Soc. 91 (117), 1e19.
Khanal, S., Shah, A., 2020. Phosphorus adsorption behaviors of MgO modified Selosse, M.A., Strullu-Derrien, C., Martin, F.M., Kamoun, S., Kenrick, P., 2015. Plants,
biochars derived from waste woody biomass resources. J. Environ. Chem. Eng. 8 fungi and oomycetes: a 400-million year affair that shapes the biosphere. New
(2), 103723. Phytol. 206, 501e506.
Ohsowski, B.M., Dunfield, K., Klironomos, J.N., Hart, M.M., 2018. Plant response to Shaheen, S.M., Niazi, N.K., Hassan, N.E., Bibi, I., Wang, H., Tsang, D.C., Ok, Y.S.,
biochar, compost, and mycorrhizal fungal amendments in post-mine sandpits. Bolan, N., Rinklebe, J., 2019. Wood-based biochar for the removal of potentially
Restor. Ecol. 26 (1), 63e72. toxic elements in water and wastewater: a critical review. Int. Mater. Rev. 64 (4),
Oladele, S.O., Adeyemo, A.J., Awodun, M.A., 2019. Influence of rice husk biochar and 216e247.
inorganic fertilizer on soil nutrients availability and rain-fed rice yield in two Shamshiri, M.H., Bagheri, V., Alaei, H., Salehi, H., 2020. Investigating the role of three
contrasting soils. Geoderma 336, 1e11. species of arbuscular mycorrhizal fungi on growth, acid phosphatase enzyme
O’Neill, B., Grossman, J., Tsai, M.T., Gomes, J.E., Lehmann, J., Peterson, J., Neves, E., activity and phenolic compounds in zinnia plant under drought stress condi-
Thies, J.E., 2009. Bacterial community composition in Brazilian Anthrosols and tions. J. Crop Prod. 9 (4), 65e81.
adjacent soils characterized using culturing and molecular identification. Shao, H., Chu, L., Lu, H., Qi, W., Chen, X., Liu, J., Kuang, S., Tang, B., Wong, V., 2019.
Microb. Ecol. 58, 23e35. Towards sustainable agriculture for the salt-affected soil. Land Degrad. Dev. 30
Pal, D.K., 2019. Degradation in Indian tropical soils: a commentary. In: Ecosystem (5), 574e579.
Services and Tropical Soils of India. Springer, Cham, pp. 85e103. Shen, Q., Hedley, M., Camps Arbestain, M., Kirschbaum, M.U.F., 2016. Can biochar
Palansooriya, K.N., Wong, J.T.F., Hashimoto, Y., Huang, L., Rinklebe, J., Chang, S.X., increase the bioavailability of phosphorus? J. Soil Sci. Plant Nutr. 16 (2),
Bolan, N., Wang, H., Ok, Y.S., 2019. Response of microbial communities to 268e286.
biochar-amended soils: a critical review. Biochar 1 (1), 3e22. Shen, Z., Hou, D., Jin, F., Shi, J., Fan, X., Tsang, D.C., Alessi, D.S., 2019. Effect of pro-
Palansooriya, K.N., Shaheen, S.M., Chen, S.S., Tsang, D.C., Hashimoto, Y., Hou, D., duction temperature on lead removal mechanisms by rice straw biochars. Sci.
Bolan, N.S., Rinklebe, J., Ok, Y.S., 2020. Soil amendments for immobilization of Total Environ. 655, 751e758.
potentially toxic elements in contaminated soils: a critical review. Environ. Int. Singh, S.P., Singh, M.K., 2019. Mycorrhiza in sustainable crop production. In:
134, 105046. Agronomic Crops. Springer, Singapore, pp. 461e483.
Park, J., Hung, I., Gan, Z., Rojas, O.J., Lim, K.H., Park, S., 2013. Activated carbon from Singh, P., Mitra, S., Majumdar, D., Bhattacharyya, P., Prakash, A., Borah, P., Paul, A.,
biochar: influence of its physicochemical properties on the sorption charac- Rangan, L., 2017. Nutrient and enzyme mobilization in earthworm casts: a
teristics of phenanthrene. Bioresour. Technol. 149, 383e389. comparative study with addition of selective amendments in undisturbed and
Paymaneh, Z., Gryndler, M., Konvalinkov a, T., Benada, O., Borovi
cka, J., Bukovsk
a, P., agricultural soils of a mountain ecosystem. Int. Biodeterior. Biodegrad. 119,
Püschel, D., Rez acova, V., Sarcheshmehpour, M., Jansa, J., 2018. Soil matrix de- 437e447.
termines the outcome of interaction between mycorrhizal symbiosis and bio- Sizmur, T., Fresno, T., Akgül, G., Frost, H., Moreno-Jime nez, E., 2017. Biochar modi-
char for Andropogon gerardii growth and nutrition. Front. Microbiol. 9, 2862. fication to enhance sorption of inorganics from water. Bioresour. Technol. 246,
Pietika €inen, J., Kiikkil€
a, O., Fritze, H., 2000. Charcoal as a habitat for microbes and its 34e47.
effects on the microbial community of the underlying humus. Oikos 89 (2), Smetanova, A., Follain, S., David, M., Ciampalini, R., Raclot, D., Crabit, A., Le
231e242. Bissonnais, Y., 2019. Landscaping compromises for land degradation neutrality:
Pradhan, A., Chan, C., Roul, P.K., Halbrendt, J., Sipes, B., 2018. Potential of conser- the case of soil erosion in a Mediterranean agricultural landscape. J. Environ.
vation agriculture (CA) for climate change adaptation and food security under Manag. 235, 282e292.
rainfed uplands of India: a transdisciplinary approach. Agric. Syst. 163, 27e35. Sohi, S., Krull, E., Lopez-Capel, E., Bol, R., 2010. A review of biochar and its use and
Premarathna, K.S.D., Rajapaksha, A.U., Sarkar, B., Kwon, E.E., Bhatnagar, A., Ok, Y.S., function in soil. Adv. Agron. 105, 47e82.
Vithanage, M., 2019. Biochar-based engineered composites for sorptive Solaiman, Z.M., Blackwell, P., Abbott, L.K., Storer, P., 2010. Direct and residual effect
decontamination of water: a review. Chem. Eng. J. 372, 536e550. of biochar application on mycorrhizal root colonisation, growth and nutrition of
Qian, K., Kumar, A., Zhang, H., Bellmer, D., Huhnke, R., 2015. Recent advances in wheat. Soil Res. 48, 546e554.
utilization of biochar. Renew. Sustain. Energy Rev. 42, 1055e1064. Solaiman, Z.M., Abbott, L.K., Murphy, D.V., 2019. Biochar phosphorus concentration
Qiao, Y., Crowley, D., Wang, K., Zhang, H., Li, H., 2015. Effects of biochar and dictates mycorrhizal colonisation, plant growth and soil phosphorus cycling.
Arbuscular mycorrhizae on bioavailability of potentially toxic elements in an Sci. Rep. 9 (1), 1e11.
aged contaminated soil. Environ. Pollut. 206, 636e643. Spokas, K.A., 2013. Impact of biochar field aging on laboratory greenhouse gas
Quilliam, R.S., Glanville, H.C., Wade, S.C., Jones, D.L., 2013. Life in the ‘charosphere’ e production potentials. Glob. Change Biol. Bioenergy 5, 165e176.
does biochar in agricultural soil provide a significant habitat for microorgan- Steiner, C., Glaser, B., Geraldes Teixeira, W., Lehmann, J., Blum, W.E., Zech, W., 2008.
isms? Soil Biol. Biochem. 65, 28e29. Nitrogen retention and plant uptake on a highly weathered central Amazonian
Rafique, M., Ortas, I., Rizwan, M., Chaudhary, H.J., Gurmani, A.R., Munis, M.F.H., ferralsol amended with compost and charcoal. J. Soil Sci. Plant Nutr. 171,
2020. Residual effects of biochar and phosphorus on growth and nutrient 893e899.
accumulation by maize (Zea mays L.) amended with microbes in texturally Stewart, C.E., Zheng, J., Botte, J., Cotrufo, F., 2013. Co-generated fast pyrolysis biochar
different soils. Chemosphere 238, 124710. mitigates greenhouse gas emissions and increases carbon sequestration in
Rajagopal, V., Malarvizhi, P., Choudhary, R.L., Krishnani, K., Ramesh, K., temperate soils. Glob. Change. Biol. Bioenerg. 5, 153e164.
Gopalakrishnan, B., Singh, N., 2017. Prospects of biochar in climate change Sun, H., Dan, A., Feng, Y., Vithanage, M., Mandal, S., Shaheen, S.M., Rinklebe, J.,
mitigation in Indian agriculture-an analysis. https://krishi.icar.gov.in/jspui/ Shi, W., Wang, H., 2019. Floating duckweed mitigated ammonia volatilization
handle/123456789/27801. and increased grain yield and nitrogen use efficiency of rice in biochar amended
Rask, K.A., Johansen, J.L., Kjøller, R., Ekelund, F., 2019. Differences in arbuscular paddy soils. Chemosphere 237, 124532.
mycorrhizal colonisation influence cadmium uptake in plants. Environ. Exp. Tabassum, R.A., Shahid, M., Niazi, N.K., Dumat, C., Zhang, Y., Imran, M., Bakhat, H.F.,
Bot. 162, 223e229. Hussain, I., Khalid, S., 2019. Arsenic removal from aqueous solutions and
Rillig, M.C., Mardatin, N.F., Leifheit, E.F., Antunes, P.M., 2010. Mycelium of arbuscular groundwater using agricultural biowastes-derived biosorbents and biochar: a
mycorrhizal fungi increases soil water repellency and is sufficient to maintain column-scale investigation. Int. J. Phytoremediation 21 (6), 509e518.
water-stable soil aggregates. Soil Biol. Biochem. 42, 1189e1191. Tamayo, E., Knight, S.A., Valderas, A., Dancis, A., Ferrol, N., 2018. The arbuscular
Robb, S., Joseph, S., Aziz, A.A., Dargusch, P., Tisdell, C., 2020. Biochar’s cost con- mycorrhizal fungus Rhizophagus irregularis uses a reductive iron assimilation
straints are overcome in small-scale farming in tropical soils in lower-income pathway for high-affinity iron uptake. Environ. Microbiol. 20 (5), 1857e1872.
countries. Land Degrad. Dev. https://doi.org/10.1002/ldr.3541. Tao, L., Ahmad, A., de Roode, J.C., Hunter, M.D., 2016. Arbuscular mycorrhizal fungi
Rondon, M., Lehmann, J., Ramírez, J., Hurtado, M., 2007. Biological nitrogen fixation affect plant tolerance and chemical defences to herbivory through different
by common beans (Phaseolus vulgaris L) increases with biochar additions. Biol. mechanisms. J. Ecol. 104 (2), 561e571.
Fertil. Soils 43, 688e708. Teutscherova, N., Vazquez, E., Arango, J., Arevalo, A., Benito, M., Pulleman, M., 2019.
Ruan, X., Sun, Y., Du, W., Tang, Y., Liu, Q., Zhang, Z., Doherty, W., Frost, R.L., Qian, G., Native arbuscular mycorrhizal fungi increase the abundance of ammonia-
Tsang, D.C.W., 2019. Formation, characteristics, and applications of environ- oxidizing bacteria, but suppress nitrous oxide emissions shortly after urea
mentally persistent free radicals in biochars: a review. Bioresour. Technol. 281, application. Geoderma 338, 493e501.
457e468. Thies, J.E., Rillig, M.C., 2009. Characteristics of biochar: biological properties. In:
Saito, M., 1990. Charcoal as a microhabitat for VA mycorrhizal fungi, and its practical Lehmann, J., Joseph, S. (Eds.), Biochar for Environmental Management: Science
implication. Agric. Ecosyst. Environ. 29, 341e344. and Technology. Earthscan, London, pp. 85e105.
Saito, M., Marumoto, T., 2002. Inoculation with arbuscular mycorrhizal fungi: the Thirkell, T.J., Cameron, D.D., Hodge, A., 2019. Contrasting nitrogen fertilisation rates
status quo in Japan and the future prospects. In: Diversity and Integration in alter mycorrhizal contribution to barley nutrition in a field trial. Front. Plant Sci.
16
10, 1312. elemental uptake of Trifolium repens in response to biochar addition, arbuscular
Tomczyk, A., Sokołowska, Z., Boguta, P., 2020. Biochar physicochemical properties: mycorrhizal fungi and phosphorus fertilizer applications in low-Cd-polluted
pyrolysis temperature and feedstock kind effects. Rev. Environ. Sci. Biotechnol. soils. Environ. Pollut. 260, 113761.
19, 191e215. Xiong, B., Zhang, Y., Hou, Y., Arp, H.P.H., Reid, B.J., Cai, C., 2017. Enhanced biodeg-
Tsang, D.C.W., Yip, A.C.K., Olds, W.E., Weber, P.A., 2014. Arsenic and copper stabi- radation of PAHs in historically contaminated soil by M. gilvum inoculated
lisation in a contaminated soil by coal fly ash and green waste compost. Envi- biochar. Chemosphere 182, 316e324.
ron. Sci. Pollut. Res. 21, 194e10204. Yang, X., Tsibart, A., Nam, H., Hur, J., El-Naggar, A., Tack, F.M., Wang, C.H., Lee, Y.H.,
Uchimiya, M., Chang, S., Klasson, K.T., 2011. Screening biochars for heavy metal Tsang, D.C., Ok, Y.S., 2019. Effect of gasification biochar application on soil
retention in soil: role of oxygen functional groups. J. Hazard Mater. 190, quality: trace metal behavior, microbial community, and soil dissolved organic
432e441. matter. J. Hazard Mater. 365, 684e694.
Van Leeuwen, C.C., Cammeraat, E.L., de Vente, J., Boix-Fayos, C., 2019. The evolution Yang, Q., Ravnskov, S., Neumann Andersen, M., 2020. Nutrient uptake and growth of
of soil conservation policies targeting land abandonment and soil erosion in potato: arbuscular mycorrhiza symbiosis interacts with quality and quantity of
Spain: a review. Land use policy 83, pp. 174e186. amended biochars. J. Soil Sci. Plant Nutr. 183 (2), 220e232.
Vanek, S.J., Lehmann, J., 2015. Phosphorus availability to beans via interactions Yin, R., Liu, R., Mei, Y., Fei, W., Sun, X., 2013. Characterization of bio-oil and bio-char
between mycorrhizas and biochar. Plant Soil 395 (1e2), 105e123. obtained from sweet sorghum bagasse fast pyrolysis with fractional con-
Vejvodova , K., Sz
akov a, J., García-Sa nchez, M., Praus, L., Romera, I.G., Tlustos, P., densers. Fuel 112, 96e104.
2020. Effect of dry olive residueebased biochar and arbuscular mycorrhizal Yoo, J.C., Beiyuan, J., Wang, L., Tsang, D.C., Baek, K., Bolan, N.S., Ok, Y.S., Li, X.D., 2018.
fungi inoculation on the nutrient status and trace element contents in wheat A combination of ferric nitrate/EDDS-enhanced washing and sludge-derived
grown in the as, Cd, Pb, and Zn contaminated soils. J. Soil Sci. Plant Nutr. https:// biochar stabilization of metal-contaminated soils. Sci. Total Environ. 616,
doi.org/10.1007/s42729-020-00193-2. 572e582.
Wan, Z., Sun, Y., Tsang, D.C.W., Yu, I.K.M., Fan, J., Clark, J.H., Zhou, Y., Cao, X., Gao, B., Yu, L., Yu, M., Lu, X., Tang, C., Liu, X., Brookes, P.C., Xu, J., 2018. Combined application
Ok, Y.S., 2019. Sustainable biochar catalyst synergized with copper heteroatoms of biochar and nitrogen fertilizer benefits nitrogen retention in the rhizosphere
and CO2 for singlet oxygenation and electron transfer routes. Green Chem. 21, of soybean by increasing microbial biomass but not altering microbial com-
4800e4814. munity structure. Sci. Total Environ. 640, 1221e1230.
Wan, Z., Sun, Y., Tsang, D.C.W., Hou, D., Cao, X., Zhang, S., Gao, B., Ok, Y.S., 2020. Yu, H., Zou, W., Chen, J., Chen, H., Yu, Z., Huang, J., Tang, H., Wei, X., Gao, B., 2019.
Electroactive biochars for green and sustainable environmental remediation: Biochar amendment improves crop production in problem soils: a review.
mechanisms and outlook. Green Chem. 22, 2688e2711. J. Environ. Manag. 232, 8e21.
Wang, L., Wang, Y., Ma, F., Tankpa, V., Bai, S., Guo, X., Wang, X., 2019a. Mechanisms Yuan, J.H., Xu, R.K., 2010. The amelioration effects of low temperature biochar
and reutilization of modified biochar used for removal of heavy metals from generated from nine crop residues on an acidic Ultisol. Soil Use Manag. 27 (1),
wastewater: a review. Sci. Total Environ. 668, 1298e1309. 110e115.
Wang, Q., Wang, W., Zhong, Z., Wang, H., Fu, Y., 2020b. Variation in glomalin in soil Yusif, S.A., Dare, M.O., Babalola, O.A., Popoola, A.R., Sharif, M.R., Habib, M.Y., 2018.
profiles and its association with climatic conditions, shelterbelt characteristics, The roles of biochar and arbuscular mycorrhizal inoculation on selected soil
and soil properties in poplar shelterbelts of Northeast China. J. For. Res. 31 (1), biological properties and tomato performance. FUTY J. Environ. 12 (2), 1e8.
279e290. Zhang, X., Wu, Y., 2017. Application of coupled zero-valent iron/biochar system for
Wang, B., Yeun, L.H., Xue, J.Y., Liu, Y., Ane , J.-M., Qiu, Y.L., 2010. Presence of three degradation of chlorobenzene-contaminated groundwater. Water Sci. Technol.
mycorrhizal genes in the common ancestor of land plants suggests a key role of A J. Int. Assoc. Water Pollut. Res. 75, 571.
mycorrhizas in the colonization of land by plants. New Phytol. 186, 514e525. Zhang, X., Zhang, S., Yang, H., Feng, Y., Chen, Y., Wang, X., Chen, H., 2014. Nitrogen
Wang, Q., Mei, D., Chen, J., Lin, Y., Liu, J., Lu, H., Yan, C., 2019b. Sequestration of heavy enriched biochar modified by high temperature CO2eammonia treatment:
metal by glomalin-related soil protein: implication for water quality improve- characterization and adsorption of CO2. Chem. Eng. 257, 20e27.
ment in mangrove wetlands. Water Res. 148, 142e152. Zhang, B., Li, S., Chen, S., Ren, T., Yang, Z., Zhao, H., Liang, Y., Han, X., 2016. Arbuscular
Wang, J., Pan, X., Liu, Y., Zhang, X., Xiong, Z., 2012. Effects of biochar amendment in mycorrhizal fungi regulate soil respiration and its response to precipitation
two soils on greenhouse gas emissions and crop production. Plant Soil 360, change in a semiarid steppe. Sci. Rep. 6 (1), 1e10.
287e298. Zhang, H., Xue, G., Chen, H., Li, X., 2018. Magnetic biochar catalyst derived from
Wang, L., Bolan, N.S., Tsang, D.C.W., Hou, D., 2020a. Green immobilization of toxic biological sludge and ferric sludge using hydrothermal carbonization: prepa-
metals using alkaline enhanced rice husk biochar: effects of pyrolysis temper- ration, characterization and its circulation in Fenton process for dyeing
ature and KOH concentration. Sci. Total Environ. 720, 137584. wastewater treatment. Chemosphere 191, 64e71.
Wang, Q., Lu, H., Chen, J., Hong, H., Liu, J., Li, J., Yan, C., 2018. Spatial distribution of Zhang, Z., Zhang, J., Xu, G., Zhou, L., Li, Y., 2019a. Arbuscular mycorrhizal fungi
glomalin-related soil protein and its relationship with sediment carbon improve the growth and drought tolerance of Zenia insignis seedlings under
sequestration across a mangrove forest. Sci. Total Environ. 613, 548e556. drought stress. N. For. 50 (4), 593e604.
Warnock, D.D., Lehmann, J., Kuyper, T.W., Rillig, M.C., 2007. Mycorrhizal responses Zhang, F., Liu, M., Li, Y., Che, Y., Xiao, Y., 2019b. Effects of arbuscular mycorrhizal
to biochar in soil-concepts and mechanisms. Plant Soil 300, 9e20. fungi, biochar and cadmium on the yield and element uptake of Medicago
Warnock, D.D., Mummey, D.L., McBride, B., Major, J., Lehmann, J., Rillig, M.C., 2010. sativa. Sci. Total Environ. 655, 1150e1158.
Influences of non-herbaceous biochar on arbuscular mycorrhizal fungal abun- Zhang, X., Zhang, Y., Ngo, H.H., Guo, W., Wen, H., Zhang, D., Li, C., Qi, L., 2020.
dances in roots and soils: results from growth-chamber and field experiments. Characterization and sulfonamide antibiotics adsorption capacity of spent cof-
Appl. Soil Ecol. 46, 450e456. fee grounds based biochar and hydrochar. Sci. Total Environ. 716, 137015.
Weber, K., Quicker, P., 2018. Properties of biochar. Fuel 217, 240e261. Zheng, H., Wang, X., Chen, L., Wang, Z., Xia, Y., Zhang, Y., Wang, H., Luo, X., Xing, B.,
Wei, X., Chen, J., Zhang, C., Pan, D., 2016. Differential gene expression in Rhodo- 2018. Enhanced growth of halophyte plants in biochar-amended coastal soil:
dendron fortunei roots colonized by an ericoid mycorrhizal fungus and increased roles of nutrient availability and rhizosphere microbial modulation. Plant Cell
nitrogen absorption and plant growth. Front. Plant Sci. 7, 1594. Environ. 41 (3), 517e532.
Wei, L., Vosa tka, M., Cai, B., Ding, J., Lu, C., Xu, J., Yan, W., Li, Y., Liu, C., 2019. The role Zhou, C., Heal, K., Tigabu, M., Xia, L., Hu, H., Yin, D., Ma, X., 2020. Biochar addition to
of arbuscular mycorrhiza fungi in the decomposition of fresh residue and soil forest plantation soil enhances phosphorus availability and soil bacterial com-
organic carbon: a mini-review. Soil Sci. Soc. Am. J. 83 (3), 511e517. munity diversity. For. Ecol. Manage. 455, 117635.
Wilkinson, T.D., Ferrari, J., Hartley, S.E., Hodge, A., 2019. Aphids can acquire the Zhuo, F., Zhang, X.F., Lei, L.L., Yan, T.X., Lu, R.R., Hu, Z.H., Jing, Y.X., 2020. The effect of
nitrogen delivered to plants by arbuscular mycorrhizal fungi. Funct. Ecol. 33 (4), arbuscular mycorrhizal fungi and biochar on the growth and Cd/Pb accumu-
576e586. lation in Zea mays L. Int. J. Phytoremediation 1e10.
Woolf, D., Amonette, J.E., Street-Perrot, F.A., Lehmann, J., Joseph, S., 2010. Sustain- Zuccarini, P., 2010. Biological and technological strategies against soil and water
able biochar to mitigate global climate change. Nat. Commun. 1, 1e9. salinization rhizosphere. J. Plant Nutr. 33, 1287e1300.
Wu, A., Yan, J., Xu, W., Li, X., 2016. Fabrication of waste biomass derived carbon by Zwetsloot, M.J., Lehmann, J., Bauerle, T., Vanek, S., Hestrin, R., Nigussie, A., 2016.
pyrolysis. Mater. Lett. 173, 60e63. Phosphorus availability from bone char in a P-fixing soil influenced by root-
Xiao, Y., Liu, M., Chen, L., Ji, L., Zhao, Z., Wang, L., Wei, L., Zhang, Y., 2020. Growth and mycorrhizae-biochar interactions. Plant Soil 408 (1e2), 95e105.
17

AMFReview

Uploaded by

Copyright:

Available Formats

AMFReview

Uploaded by

Document Information

Original Title

Copyright

Available Formats

Share this document

Share or Embed Document

Sharing Options

Did you find this document useful?

Is this content inappropriate?

Copyright:

Available Formats

AMFReview

Uploaded by

Copyright:

Available Formats

Environmental Pollution 268 (2021) 115549

Contents lists available at ScienceDirect

Sustainable improvement of soil health utilizing biochar and

1. Introduction example, humungous pressure is brought to bear on 2.4% of land

Fig. 1. Impact of biochar amendment on soil dynamics.

Characteristic of Biochar PT HR BY MC FC AC VC C H N O pH ABS BET PV References

Biochar from cereal feedstocks

Fig. 3. Biochar as potential habitat for soil fauna.

Fig. 4. Relationship of AMF with various biotic components of soil ecosystem.

Fig. 5. Biochar enhances the soil amelioration capacity of AMF.

Mycorrhiza’s dependency on different crops

Winter crops (Scientiﬁc name) Summer crops (Scientiﬁc name)

Linseed Linum usitatissimum þþþþþ Cotton Gossypium hirsutum þþþþþ

Dependency legends: High ¼ þþþþþ; Moderate ¼ þþþþ; Low ¼ þþþ; Independent ¼

You might also like

AMFReview

Uploaded by

Copyright:

Available Formats

AMFReview

Uploaded by

Document Information

Original Title

Copyright

Available Formats

Share this document

Share or Embed Document

Sharing Options

Did you find this document useful?

Is this content inappropriate?

Copyright:

Available Formats

AMFReview

Uploaded by

Copyright:

Available Formats

Environmental Pollution 268 (2021) 115549

Contents lists available at ScienceDirect

Sustainable improvement of soil health utilizing biochar and

1. Introduction example, humungous pressure is brought to bear on 2.4% of land

Fig. 1. Impact of biochar amendment on soil dynamics.

Characteristic of Biochar PT HR BY MC FC AC VC C H N O pH ABS BET PV References

Biochar from cereal feedstocks

Fig. 3. Biochar as potential habitat for soil fauna.

Fig. 4. Relationship of AMF with various biotic components of soil ecosystem.

Fig. 5. Biochar enhances the soil amelioration capacity of AMF.

Mycorrhiza’s dependency on different crops

Winter crops (Scientiﬁc name) Summer crops (Scientiﬁc name)

Linseed Linum usitatissimum þþþþþ Cotton Gossypium hirsutum þþþþþ

Dependency legends: High ¼ þþþþþ; Moderate ¼ þþþþ; Low ¼ þþþ; Independent ¼ 

You might also like

Dependency legends: High ¼ þþþþþ; Moderate ¼ þþþþ; Low ¼ þþþ; Independent ¼