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Photosynthesis research in India: Transition from yield physiology into

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 Photosynthesis Research 76: 435–450, 2003.
© 2003 Kluwer Academic Publishers. Printed in the Netherlands.
435

Minireview

Photosynthesis research in India: transition from yield physiology into

molecular biology∗

Agepati S. Raghavendra1,∗∗ , Prafullachandra Vishnu Sane2 & Prasanna Mohanty3

1 Department of Plant Sciences, School of Life Sciences, University of Hyderabad, Hyderabad 500046, India;
2 NationalBotanical Research Institute, Rana Pratap Marg, Lucknow 226001, India; 3 Regional Plant Resource
Center, Nayapalle, Bhubaneshwar 751015, India, and School of Life Sciences, Jawaharlal Nehru University, New
Delhi 110067, India; ∗∗ Author for correspondence (e-mail: asrsl@uohyd.ernet.in; as_raghavendra@yahoo.com;
fax: +91-40-23010145)

Received 14 September 2002; accepted in revised form 14 February 2003

Key words: R.D. Asana, Sir J.C. Bose, Crop physiology, V.S.R. Das, R.H. Dastur, A. Gnanam, P. Mohanty, A.S.
Raghavendra, S. Ranjan, P.V. Sane, B.N. Singh, R. Singh, G.S. Singhal, S.K. Sinha

Abstract
Photosynthesis research in India can be traced back several thousand years, with the mention of the Sun energizing
the plants, which form food for all living creatures on the earth (from the Mahabharata, the great epic, ca. 2600
B.C.) and the report of Sage Parasara (ca. 100 B.C.) on the ability of plants to make their own food, due to their
pigments. With the pioneering studies by Sir Jagdish Chandra Bose, work on photosynthesis proceeded steadily
during the first half of the 20th century. Some of the classic reports during this period are: malate metabolism in
Hydrilla, spectrophotometric estimation of chlorophylls, importance of spectral quality for photosynthesis – an
indication of two photosystems, photoinactivation of photosynthesis, and importance of flag leaf photosynthesis to
grain yield. After the 1960s, there was a burst of research in the areas of physiology and biochemistry of carbon
assimilation and photochemistry. A significant transition occurred, before the beginning of new millennium, into
the area of molecular biology of chloroplasts, regulation of photosynthesis and stress tolerance. Future research
work in India is geared to focus on the following aspects of photosynthesis: elucidation/analysis of genes, molecular
biology/evolution of enzymes, development/use of transgenics and modeling.

Abbreviations: CAM – crassulacean acid metabolism; Chl – chlorophyll; LHC – light harvesting complex; ME –
malic enzyme; OEC – oxygen-evolving complex; PEPC – phosphoenolpyruvate carboxylase; PS – photosystem;
Rubisco – ribulose-1,5-bisphosphate carboxylase oxygenase; TL – thermoluminescence

‘If the photosynthetic process takes place in more than one

photochemical stage it is probable that for one stage a partic-
ular wave-length of light is more efficient than for the other.’
– R.H. Dastur and R.J. Mehta (Annals of Botany, Vol. XLIX,
No. CXCVI. October, 1935)

Introduction and Susruta Samhita (D.M. Bose et al. 1971). A ref-

erence to the photosynthetic process is found in ‘The
References to plants are abundant in ancient Indian Mahabharata’, an epic more than 4600 years old (Fig-
Sanskrit scriptures: Vedas, Epics, Charaka Samhita ure 1). The report by Sage Parasara (ca. 100 BC), on
plant pigments and their ability to make food, is note-
∗ Dedicated to the memory of Professor Suresh Kumar Sinha
worthy (Majumdar and Banerji 1960). Sage Parasara
(1934–2002).
436

Figure 1. A shloka (poem) in Sanskrit from ‘The Mahabharata,’ one of the ancient Indian epics (dating back to ca. 2600 BC), describing the
role of plants in harnessing the solar energy into food, and being the source of energy for other living beings on the earth. The physiology of
plants (‘Vriksh-Ayurveda’) is discussed in Rig-Veda, one of the four Indian Vedas, more than 5000 years back.

is called ‘the father of Botany,’ because he classified Jawaharlal Nehru University (JNU) and Indian Agri-
flowering plants into various families, nearly 2000 cultural Research Institute (IARI) (both at New Delhi),
years before Linnaeus. Parasara also described plant Madurai Kamaraj University (Madurai, Tamilnadu),
cells (the outer/inner walls and sap coloring matter), Sri Venkateswara University (Tirupati, Andhra Pra-
which were rediscovered by Robert Hooke, with the desh) and Haryana Agricultural University (Hisar,
help of microscope. Photosynthesis research in In- Haryana). Their success led to additional centers at
dia has been reviewed by S. Bose and Rao (1988), National Botanical Research Institute (Lucknow, Ut-
Bhagwat (1990) and R. Singh (1990). tar Pradesh), University of Delhi (Delhi), Sambalpur
The earliest studies during the modern period were University (Sambalpur, Orissa), University of Hydera-
by Sir J.C. Bose and others, at Calcutta (now called bad (Hyderabad, Andhra Pradesh), and a few other
Kolkata), Banaras (Varanasi) in Uttar Pradesh, and places. The locations of the current centers are indic-
New Delhi. These are described below. Studies on ated in Figure 2, where research on a variety of aspects
photosynthesis intensified with the return of young of photosynthesis (from primary photochemistry to
Indian scientists trained abroad (see the section on ecology and global environment), is being carried out.
‘Photochemical reactions’). Soon, international level Although several Indians have contributed sig-
research progressed at Bhabha Atomic Research Cen- nificantly to photosynthesis research while working
ter in Bombay (now called Mumbai) in Maharashtra, abroad, this article describes only their work done in
 437

Figure 2. Some of the active centers of photosynthesis research

in India (in alphabetical order): Bangalore (University of Agricul-
tural Sciences), Bhubaneshwar (Regional Plant Resource Centre,
Utkal University, Institute of Life Sciences), Delhi (Indian Agri-
cultural Research Institute, Jawaharlal Nehru University, University
of Delhi, International Centre for Genetic Engineering and Biotech- Figure 3. Some of the pioneers of photosynthesis research in India
nology), Goa (University of Goa), Hisar (Haryana Agricultural Uni- during the pre-1960 period. A. Sir J.C. Bose (1858–1937); B. Bhola
versity), Hyderabad (University of Hyderabad), Indore (University Nath Singh (1898–1984); C. R.H. Dastur (1896–1961); D. R.D.
of Indore), Jodhpur (Jodhpur University) , Kolkata/Calcutta/Kalyani Asana (1908–1999).
(Bose Institute, University of Kalyani), Lucknow (National Botan-
ical Research Institute), Madurai (Madurai Kamaraj University),
Mumbai/Bombay (Bhabha Atomic Research Centre), Pondicherry
(Pondicherry University), Pune (University of Pune), Sambalpur vilinear pattern. He recorded action spectra, as well as
(Sambalpur University), Tirupati (Sri Venkateswara University) and quantum yields (using an ingenious CS2 prism), and
Varanasi (Banaras Hindu University). malate metabolism in summer grown Hydrilla (J.C.
Bose 1923, 1924). These findings are amazing, as
India. Among those of Indian origin, and who work simple instruments were fabricated and used to record
abroad, we list P.N. (Dan) Avadhani, Parag Chitnis, novel responses.
Henry Daniell, Govindjee, Arun Goyal, Autar Mattoo, Ghosh and Sen-Gupta (1931) analyzed the absorb-
Himadri Pakrasi, Krishna Rao, Sabeeha Merchant, ance of chlorophyll (Chl) in acetone and developed
Krishna Niyogi, Bijay K. Singh, A.R. Subramanian, formulae to determine the content of Chl a as well as
Krishna K. Tiwari and Vittal Yachandra. Chl b, based on their absorption at 650 and 460 nm.
In view of the overwhelming literature, references It was not until 1941 and 1949 that G. Mackinney and
are made to selected publications that originated in Daniel Arnon developed the formulae for Chl determ-
work done in India. However, we mention some ination (for a minireview, see Porra 2002). Rustom
collaborative research wherever pertinent. Hormusji Dastur and co-workers (K.M. Samant, R.Y.
Mehta, and S. Solomon), of the Botany Department
of the Royal Institute of Science, Bombay, studied the
Classic work during the pre-1960 era effect of monochromatic red and blue-violet, obtained
by filtering lights with carmine and copper sulph-
Sir Jagdish Chandra1 Bose, a pioneer in photosyn- ate solutions; they concluded that photosynthesis was
thesis (as well as plant physiology) research in India dependent not only on the intensity, but also had co-
(Figure 3A) demonstrated, early in 1924,2 that the rate operative and specific effects of different colors on
of photosynthesis versus light intensity followed a cur- photosynthesis (see Dastur and Mehta 1935; Figure
438

3C). This seems to be one of the earliest indications Rama Das (Sri Venkateswara University, Tirupati
of the two light effect in photosynthesis (see quota- and later University of Hyderabad, Hyderabad; both
tion at the beginning of this paper). Although Eugene in Andhra Pradesh), Arumugham Gnanam (Madurai
Rabinowitch (1951, p. 1167) had raised concerns Kamaraj University, Madurai, Tamilnadu), late G.V.
based on the use of optically dense tissues, and it Joshi (Shivaji University, Kolhapur, Maharashtra),
is not clear if the light intensities were in the linear Renu Khanna-Chopra (Indian Agricultural Research
range of the ‘light curves’, the observations were clear, Institute, New Delhi), Aditya N. Purohit (Garhwal
and, perhaps, much ahead of the time. B.N. Singh and University, Garhwal, Uttar Pradesh), Agepati S.
Kumar (1935) observed inactivation of carbon assim- Raghavendra (Ragha to his friends; see Figures 4E and
ilation in leaves at high light, obviously an indication 4F) (University of Hyderabad, Hyderabad), Prafulla-
of the phenomenon of photoinhibition (see Adir et al., chandra Vishnu Sane (Raj to his friends; see Fig-
this issue). (See Figure 3B for a photograph of B.N. ures 4B and 4C) (Bhabha Atomic Research Centre,
Singh.) Mumbai, Maharashtra), Randhir Singh (Haryana
Other classic contributions during the pre-1960 Agricultural University, Hisar, Haryana), late Suresh
period are: a sigmoidal type curve of photosynthetic K. Sinha (Indian Agricultural Research Institute, New
response to light, suggesting a saturation kinetic rather Delhi) and M. Udaya Kumar (University of Agricul-
than the Blackman’s break (B.N. Singh and Lal 1935), tural Sciences, Bangalore, Karnataka) These studies
and the importance of flag leaf photosynthesis to grain focused on C3 -, C4 -, and Crassulacean Acid Metabol-
yield (Rustom Darasha Asana and Mani 1949, see ism (CAM) photosyntheses as well as C3 –C4 interme-
Figure 3D). diates (see C.C. Black and B. Osmond, this issue, for
The studies of Shri Ranjan (University of Alla- a history of CAM).
habad), on the importance of mineral nutrition to
photosynthesis and modulation of respiration in light, C3 -, C4 - and CAM plants
were of great vision (Ranjan 1940; Ranjan et al. 1962).
In 1940, he also worked on the temperature coefficient Despite being a C3 plant, the leaves of rice incorpor-
of photosynthesis in Eugenia jambolana (cited by ate CO2 into C4 acids under blue light (V.S.R. Das
Rabinowitch 1956). He was instrumental in encour- and Raju 1965) or during leaf development. Photo-
aging and molding the career of the editor of this spe- synthetically active mesophyll cells were isolated from
cial issue, Govindjee (University of Illinois, Urbana, leaves of several C3 plants (Gnanam and Kulandaivelu
USA), a pioneer of photosynthesis research. 1969; Kulandaivelu and Gnanam 1974). Carbon fixa-
tion in autotrophic cultures of C3 (Arachis hypogaea),
C4 (Gisekia pharnacoides) and CAM (Chamaecereus
Research during the post-1960 period sylvestrii) species was studied by Seeni and Gnanam
(1980, 1982).
Most of the work in early 1960s was related to the Several C4 plants were discovered among the In-
physiology of photosynthesis, mineral nutrition and dian flora (V.S.R. Das and Raghavendra 1973; Sankhla
crop yields (Asana et al. 1969) and later diversified et al. 1975; Raghavendra and Das 1976). A check-list
into biochemistry, photochemistry and molecular bio- of C4 plants, based on these reports (Raghavendra and
logy. The consolidation of photosynthesis research Das 1978a) is highly cited. The PhD thesis of Age-
was facilitated by the interaction of Indian Scientists pati Raghavendra (advisor: V.S. Rama Das) presented
with others in India as well as from abroad (Figures a comprehensive study of carbon assimilation in a se-
4A–G). lected range of C3 and C4 plants, chosen from Indian
flora.
The carbon assimilation during C4 pathway was
Carbon metabolism: physiology and biochemistry elucidated in detail in millet crops, such as Eleusine
coracana, Pennisetum typhoides and Setaria italica
The physiology and biochemistry of carbon fixation (Rathnam and Das 1975; Raghavendra and Das
have been studied by several groups led by (in al- 1978b). A shift from C4 to C3 type photosynthesis
phabetical order): Yash P. Abrol (Indian Agricultural after anthesis was discovered in leaves of sorghum
Research Institute, New Delhi), Anil S. Bhagwat (Khanna and Sinha 1973). The activities of photosyn-
(Bhabha Atomic Research Centre, Mumbai), V.S. thetic enzymes in both C3 and C4 plants were shown
 439

Figure 4. The authors of this review, photographed with the other photosynthesis scientists from
India and abroad. (A) Prasanna Mohanty (sitting in the center). Standing (from left to right):
George Papageorgiou, Alan Stemler, Eugene Rabinowitch, Pat Breen and Govindjee. Photograph
taken in Urbana, Illinois, USA (1968); (B) P.V. Sane (left) with V.G. Tatake (center) and Gunther
Hauska (right). Photograph taken in Lucknow, India (1989); (C) P.V. Sane (second from left) is
flanked by A. Gnanam (first from left), Shikha Roy (third from left), and Govindjee (extreme
right). Photograph taken in Stockholm, Sweden (1989); (D) From left to right: George Papageor-
giou, Christa Chritchley, Danny Blubaugh, William Coleman, Jack van Rensen, Tom Wydrzynski,
Prasanna Mohanty and Alan Stemler. Photograph taken in Montpellier, France (1993); (E) Agepati
Raghavendra (left) with Gerry Edwards (center) and Carlos Andreo (right). Photograph taken in
Rosario, Argentina (1999); (F) Agepati Raghavendra (right) with Hans Heldt (left). Photograph
taken in Hyderabad, India (2002). (G) A recent photograph of T.S. Desai, courtesy of Samar Desai.
440

to be influenced by altitude and growth temperatures PEPC and NADP-ME were purified and characterized
(Pandey et al. 1980). by S. Das et al. (1986) and Singal and Singh (1986).
C3 –C4 intermediates, discovered in the genera of Alternative pathways of CO2 fixation were repor-
Mollugo and Alternanthera (Raghavendra et al. 1978; ted. The chloroplasts of greening potatoes fixed carbon
Rajendrudu et al. 1986), provided a model system into formate (through CO2 reductase) and channeled
to study the mechanism of reduced photorespiration it into mevalonate (Ramaswamy et al. 1976; Arora et
(Raghavendra 1980). The C3 –C4 intermediates have al. 1985). This phenomenon is highly interesting and
imperfect Kranz anatomy, low activities of photores- needs to be studied further.
piratory enzymes and predominant localization of en-
zymes such as glycine decarboxylase in bundle sheath Interaction of carbon assimilation with other
cells (Devi et al. 1995). Further studies on these C3 – metabolic processes
C4 intermediates are crucial and are promising for the
understanding of the mechanism and evolution of not Mesophyll protoplasts from pea leaves provided a
only C3 –C4 intermediacy but also C4 photosynthesis. model system to demonstrate the dependence of
Studies on CAM date back to 1924, with the photosynthetic carbon assimilation on mitochondrial
reports of acidification and malate accumulation in metabolism. Mitochondrial oxidative electron trans-
leaves of Hydrilla, particularly at warm temperatures port helps to dissipate excess reductants from chloro-
(J.C. Bose 1924). The phenomenon of CAM was de- plasts (Raghavendra et al. 1994), optimizes pho-
tected in several plants, including some nonsucculents tosynthesis (Padmasree et al. 2002) and protects
(Rao et al. 1979). chloroplasts against photoinhibition (Saradadevi and
The properties of selected C3 - or C4 -enzymes, Raghavendra 1992). This work attracted consider-
e.g., ribulose 1,5-bisphosphate carboxylase/oxygenase able attention and the phenomenon of mitochondrial
(Rubisco), phosphoenolpyruvate carboxylase (PEPC) influence on photosynthesis is now widely accepted
and NADP malic enzyme (ME), were studied and the (Gardeström et al. 2002).
enzymes purified (Bhagwat and Sane 1975; Bhagwat Carbon metabolism is essential for fatty acid bio-
1981; Jawali and Bhagwat 1987; Rajagopalan et al. synthesis, particularly in plastids of oilseeds (Gupta
1994). Fluorescence probes indicated the importance and Singh 1996). Glycolate also supports second-
of tryptophan and histidine residues in the active site ary metabolism, by enhanced rubber (polyisoprene)
of spinach Rubisco (N.C. Verma and Bhagwat 1985). formation in guayule (Parthenium argentatum) (A.R.
Protein phosphorylation mediates the light activation Reddy et al. 1987).
of C4 -PEPC (Rajagopalan et al. 1994; Parvathi et al. The availability and mode of nitrogen has a pro-
2000) and regulates small subunit of Rubisco (Kaul found influence on photosynthesis and photorespira-
et al. 1986). Some of the Calvin–Benson cycle en- tion (Kumar et al. 1993). Besides nitrogen, sulphur
zymes can exist as multienzyme complexes (Sainis et also modulates photosynthesis, as in Brassica (Ahmad
al. 2003), a phenomenon which warrants further at- and Abdin 2000). There has been renewed interest
tention. During ageing, marked changes occur in the in the interaction between photosynthesis and nitro-
activities of rubisco and PEPC in even the submerged gen metabolism and the relevant literature has been
aquatic angiosperms (Jana and Chaudhuri 1982). reviewed recently (Kumar et al. 2002).

Carbon metabolism in tissues other than leaves Crop productivity and stress responses

It may be surprising, but the fruiting structures con- Photosynthesis by flag leaf is crucial for grain yield
tribute significantly to the crop yield, as they are (Asana and Mani 1949). The photosynthetic effi-
capable of photosynthetic CO2 fixation (Sinha and ciency varies among cultivars. However, high rates of
Sane 1976) and can also reassimilate respiratory CO2 . photosynthesis alone would not increase crop yields.
The reproductive parts of wheat, chickpea (Cicer Heterotic hybrids of sorghum or wheat produce high
arientinum) and rapeseed (Brassica campestris) con- biomass, despite their low photosynthesis (Khanna-
tain high activities of C4 -enzymes, but exhibit in- Chopra 2000). Conventional breeding for water use
termediate status between C3 -, and C4 /CAM photo- efficiency could not improve crop performance, be-
synthesis (Singal et al. 1987; R. Singh 1993). Key cause stomatal closure limits photosynthetic carbon
enzymes of carbon metabolism in these pods, such as assimilation too (Udayakumar et al. 1998).
 441

Accumulation of proline, induced by heat or salt QA -related chlorophyll fluorescence changes through
stress, protects thylakoids against membrane peroxid- the use of various uncouplers, electron carriers, and
ation by scavenging singlet oxygen species (Alia et inhibitors of electron transfer, also in cyanobacteria (P.
al. 1997). Proline also seems to promote the disso- Mohanty and Govindjee 1973a, b; see P. Mohanty et
ciation of the small subunits of rubisco and suppress al., 1971, for the site of hydroxylamine action in red
its activity (Sivakumar et al. 2001) suggesting that algae).
proline accumulation during stress may have multiple P.V. Sane obtained his PhD from the Univer-
functions. sity of Alberta, Edmonton, Canada (advisor: Saul
The effects of water stress, heavy metals and el- Zalik). Sane’s work for PhD was a detailed biochem-
evated CO2 on carbon fixation and related enzymes ical analysis of carbon assimilation and reactions of
were studied by several groups. These stress factors Chl biosynthesis in a mutant of Gateway barley, in
(e.g., water, heat and light) interact while modulat- comparison with those of wild type (Sane and Zalik
ing photosynthesis (Jagtap et al. 1998). Differential 1970). Later, working with Roderick Park, Sane
degradation of rubisco has been observed, in heat- analyzed the ultrastructure and biochemistry of the
sensitive and heat-tolerant rice varieties, on exposure chloroplast membranes, employing a novel method of
to thermal stress (A. Bose et al. 1999). Heavy metals, isolating PS I and PS II without detergents (Sane et al.
such as Cd2+ and Ni2+ , affect the enzymes of Calvin– 1970). On the basis of these studies, they proposed a
Benson cycle in chickpea leaves (Sheoran et al. 1990). model for the distribution of two photosystems in the
Exposure to elevated CO2 reduces photorespiration chloroplast lamellar structure, in an article of Annual
and increases photosynthesis in Brassica (Uprety and Reviews of Plant Physiology (Park and Sane 1971),
Mahalakshmi 2000). Further research on these aspects which has become a citation classic.
is essential to understand the adaptive mechanisms and
to evolve a strategy of exploiting plants for alleviating
the effects of heavy metals and elevated CO2 . Thermoluminescence (TL)

Using a novel homemade setup, P.V. Sane, V.G. Tatake

Photochemical reactions and their co-workers, particularly T.S. Desai (Figure
4G), at Bhabha Atomic Research Centre (Mumbai),
As in the case of carbon assimilation, several research discovered 7 distinct TL-glow peaks from oxygenic
groups in India studied the photochemical reactions photosynthetic membranes, originating from PS II
of photosynthesis, that involved light emission, ex- (Desai et al 1975, 1983; Sane et al. 1977; Tatake
citation energy distribution, state changes, electron et al. 1980). Thermoluminescence was discovered by
transport, photoinhibition and stress responses of pho- the late William Arnold, and some fundamental work
tosystems. Sane (1977) suggested the most likely was already known (for a historical minireview on
locations of electron transport components along and TL, see Imre Vass, this issue). Using inhibitors, ar-
across the thylakoid membranes resulting in vectorial tificial electron donors/acceptors and excitation of PS
electron transport, based on his earlier studies and II/PS I, the origin of TL-peaks in the back reactions
from several other research groups. of electron transport was identified: the one at −20 ◦ C
One of the strengths of several Indian scientists has (due to Z+ QA − ), 0 ◦ C (S2 /S3 QA − ), 10 ◦ C (S3 QB − ),
been the training received in laboratories abroad. The 25 ◦ C (S2 QB − ) and 50 ◦ C (PS I). The report of light
excellent training received from abroad was then com- emission from PS I at high temperature (Sane et al.
plemented with ingenious adaptation to local environ- 1980) was interesting and stimulated further work in
ment. Prasanna Mohanty, one of the authors of this other laboratories around the world. A major spin off
review, received his PhD degree from the University of the activation energy calculations of the TL peaks
of Illinois at Urbana, USA (advisor: Govindjee). His by Tatake et al. (1980), that led to unusual numbers,
PhD thesis was one of the first studies on the regulation was the theory for TL proposed by Don DeVault et
of excitation energy distribution and redistribution in al. (1983). Anoxygenic bacterium Rhodopseudomo-
intact algal cells through the use of Chl fluorescence. nas also exhibits interesting TL peaks (Govindjee et
A major contribution of Mohanty was the first obser- al. 1977). The research on TL was reviewed by Sane
vation of the ‘O-I-D-P’ Chl fluorescence (Kautsky) and Rutherford (1986). Sane’s interest in TL work
curve in cyanobacteria, and the analysis of the non- continues (see, e.g., Sane et al. 2002).
442

The thermoluminescence technique has provided a The group of Gauri S. Singhal studied extensively
very useful tool in understanding the mechanism of the synergistic responses of photosynthesis in wheat
delayed light emission. Further work on thermolumin- leaves to stresses, such as high light and low temper-
escence was initiated in India by Pandit Vidyasagar ature. On exposure to high light, there was not only
and his colleagues at the University of Pune, Pune an increase in lipid peroxidation but also de novo syn-
(Maharashtra), using a setup similar to that developed thesis of protective antioxidant enzymes (R.K. Mishra
by Tatake et al. (1971). Vidyasagar et al. (1993) and Singhal 1992; N.P. Mishra et al. 1993; Sharma and
developed mathematical models, based on the gen- Singhal 1992). They observed also that high temperat-
eral order kinetics of thermoluminescence peaks, to ure or water stress alters the membrane organization
provide acceptable values of activation energy and and the absorbance/fluorescence properties of chloro-
frequency factor. They suggested that the events of plasts (Bharadwaj and Singhal 1981; B.R. Singh and
retrapping of electrons during TL peak formation are Singhal 1984).
important while considering the acceptor side but not Udaya Biswal (Sambalpur University) studied the
so dominant on the donor side (Thomas et al. 1996). oxygen evolving complex (OEC) of PS II and pro-
posed one of the earliest models for the Mn-cluster
(Raval and Biswal 1985). Salil Bose (Madurai Kama-
Photosystems: structure, function and responses to raj University, MKU) studied changes in photochem-
stress ical reactions due to cation induced stacking and en-
ergy distribution between PS II and PS I (Ramanujam
Several research groups in India are interested in and Bose 1983). Like inorganic cations, anions were
the function and regulation of photosystems, elec- shown, at the University of Indore, India, to induce
tron transport, and their responses to abiotic or biotic state changes in spinach thylakoids (Jajoo et al. 1998).
stresses. The group of P.V. Sane discovered heat- Lack of usual cation effects on the electron transport
induced state changes (Sane et al. 1984). The devel- activity in thylakoids of Hydrilla verticillata has been
opment of state I was dependent on phosphorylation, reported (S.R. Mishra and Sabat 1998). This could be
whereas the state II development was associated with due to altered stacking characteristics of chloroplasts
the redox levels of electron transport components loc- in Hydrilla.
ated between the two pigment systems of photosyn- Because of the threats of heavy metal pollution to
thesis (Sane et al. 1982). In a recent report, P. Mohanty agriculture, several workers in India studied the mode
et al. (2002) provided the final evidence demonstrating of action and sensitivity to heavy metals of photosyn-
that elevated temperature treatment enhances the phos- thesis in vivo as well as in vitro. In higher plant chloro-
phorylation of light-harvesting complex IIb (LHC IIb) plasts, Zn2+ affected reversibly the donor side (OEC)
and physically increases the transfer of LHC IIb from of PS II, while Ni2+ affected light-harvesting anten-
PS II region to PS I region. (For a historical account of nae irreversibly (Tripathy and Mohanty 1980; Tripathy
the discovery of such changes, see Allen 2002.) et al. 1981). These authors elucidated three types of
The research groups of Prasanna Mohanty and heavy metal ion specific changes in chloroplast struc-
Gauri Singhal at Jawaharlal Nehru University (JNU, ture and function. Subsequent work elucidated the
New Delhi) studied several aspects of electron trans- effects of Hg2+ , Al3+ and Na+ on the electron trans-
port, energy transfer and transduction processes of PS port (Tripathy et al. 1983; Wavare and Mohanty 1985;
II/PS I under a variety of stresses. Among the findings Murthy et al. 1989). Similar inhibition of photosyn-
of Mohanty’s group are: non-circadian out-of-phase thetic reactions by heavy metals has been observed in
oscillations in electron transport activities of PS II algae and cyanobacteria (D.P. Singh and Singh 1987).
and PS I and the association of these oscillations with G. Kulandaivelu (MKU) observed that UV-B ra-
phosphorylation (Sayeed and Mohanty 1987), in vivo diation affected the PS II reaction center of Phase-
multiphasic dark relaxation kinetics of Chl a fluores- olus leaves (Noorudeeen and Kulandaivelu 1982) and
cence, related to Q− oxidation (Bukhov et al. 1992), changed the pattern of PS II polypeptides (Nedun-
elevated temperature induced alterations in PS II ac- chezian and Kulaindaivelu 1991). UV-B changed
ceptor side (Bukhov et al. 1990), subsequent recovery levels of D1 protein and psbA transcripts in wheat
of this phenomenon (N. Mohanty et al. 1987), and use leaves (Chaturvedi et al. 1998).
of crown ethers as PS II inhibitors and the site of their
action (Sabat et al. 1991).
 443

Changes during leaf senescence over-production of singlet oxygen (Tripathy and

Chakraborthy 1991). Prolonged exposure to sub-lethal
Another area of studies initiated by Mohanty’s lab doses of Sandoz 9785 (a herbicide, decreasing mem-
in JNU is photosynthesis during senescence, using brane fatty acids) affects the energy distribution pro-
chloroplasts as well as leaves of barley, wheat and cess but makes wheat seedlings heat-tolerant (Mannan
Cucumis. The OEC was damaged and the activit- and Bose 1986).
ies of key enzymes, such as rubisco were affected
during senescence (U.C. Biswal and Mohanty 1976,
1978). Further, senescence induces not only loss of
Chl-protein complexes, with differential sensitivity of Molecular biology of chloroplasts
various forms of Chl a (A. Grover et al. 1986), but also
causes the migration (due to phosphorylation) of LHC The molecular biology of the chloroplast, includ-
II to PS I in stromal region (Prakash et al. 2001). The ing photosynthetic genes, is studied by three groups:
group of Udaya Biswal continued to study leaf senes- Akhilesh K. Tyagi (University of Delhi), P.V. Sane
cence and the chloroplast stability in vitro (Panigrahi (National Botanical Research Institute, Lucknow)
and Biswal 1979; U.C. Biswal and Biswal 1988; B. and the team at International Centre for Genetic
Biswal 1997a). Engineering and Biotechnology (ICGEB, New Delhi,
Several groups in India have contributed towards earlier led by Krishna Tewari, and now by Sudhir
our understanding of changes in chloroplast structure Sopory). A historical account on the molecular bio-
function relationships by a variety of stresses, such as logy of chloroplasts is provided by L. Bogorad, this
light, UV-B, temperature and drought (e.g., B. Biswal issue, and of the chloroplast genome by M. Sugiura
1997b). These studies have now been extended to (also in this issue).
several crop species. The research group of Tyagi has characterized
the chloroplast genome of indica rice, Vigna and
Arabidopsis; they have cloned and sequenced nuc-
Protein synthesis and chlorophyll development lear genes encoding the precursors of 33, 23 and 16
kDa polypeptides of OEC from Arabidopsis thaliana
The group of A. Gnanam (MKU) reconstituted an (Kochhar et al. 1996; Jain et al. 1998). They have stud-
in vitro translation system using isolated mesophyll ied the promoters of spinach psaF and petH (Tyagi et
chloroplasts of sorghum (Geetha and Gnanam 1980). al. 1999), developmental control (Kapoor et al. 1994)
The isolated chloroplasts were able to synthesize pro- and the role of secondary messengers in the plastidic
teins using ATP generated by photophosphorylation; gene expression (M. Grover et al. 1998). In a recent
thus, a very unique protein synthesizing machinery study, Tyagi’s group has achieved salt tolerance in in-
was demonstrated. They studied the synthesis of heat- dica rice by introducing the gene of choline oxidase,
shock proteins by isolated chloroplasts (Krishnasamy which produces glycine betaine (A. Mohanty et al.
et al. 1988). 2002).
Baishnab Tripathy (JNU) studied the Chl biosyn- The group of P.V. Sane has sequenced about 80%
thesis and its regulation. The biosynthesis of Chl of the chloroplast genome, including several PS II/PS
was regulated by chloroplast envelope (Manohara and I and house keeping genes, from Populus deltoides.
Tripathy 2000) and was impaired during temperature They have studied several psb operons (B to F, L, J)
stress or senescence (Tewari and Tripathy 1998). The (Naithani et al. 1997; Dixit et al. 1999), as well as
regulation of Chl biosynthesis by intraplastidic dis- seasonal and diurnal changes in the expression of PS
tribution is interesting and has recently been further II genes (Trivedi et al. 2000).
validated by the distribution of biosynthetic interme- Among the findings by the group at ICGEB are:
diates (Mohapatra and Tripathy 2003). A novel proto- the presence of two cis-elements, in the light regu-
chlorophyllide oxidoreductase C (porC) gene, cloned lated promoter of psaF, chloroplast replication in vitro,
from Arabidopsis, mediates chlorophyll biosynthesis stimulation of DNA polymerase activity by a gly-
(Pattanayak and Tripathy 2002). coprotein, cloning of genes encoding topoisomerases
5-Aminolevulinic acid acts as a photodynamic I/II and their promoters (Mukherjee et al. 1994; M.K.
herbicide by accumulating tetrapyrroles and hyper- Reddy et al. 2001; for further details, see Sopory and
sensitizing the plant tissue to light due to the Maheswari 2001).
444

Figure 5. Participants at the International Satellite Conference on Chloroplasts, held in Indian National Science Academy, New Delhi during
August 13–15, 2001. This conference was organized in conjunction with the International Photosynthesis Congress held at Brisbane, Australia
during August 18–23, 2001. There were 87 participants from India and 26 from abroad, including scientists from Canada, Finland, Germany,
Japan, Sweden, Switzerland, UK and USA. Many Indian scientists referred in this article are indicated with numbers: Sitting (from left to
right): [1] B. C. Tripathy, [2] V. S. Rama Das, [3] S. K. Sopory, [4] P. V. Sane, [5] A. Gnanam, [6] A. S. Raghavendra, [7] K. C. Bansal, [8] P.
Mohanty. Standing (from left to right and bottom to top): [9] S. K. Mukherjee, [10] B. Biswal, [11] J. K. Sainis, [12] G. Kulandaivelu, [13] V.
Jagtap, [14] U.C. Biswal, [15] A. S. Bhagwat, [16] R. Khanna-Chopra, [17] A. N. Misra, [18] N. K. Ramaswamy, [19] A. R. Reddy, [20] M. Z.
Abdin, [21] H. S. Misra. The readers may also recognize several photosynthesis experts from countries other than India. Photograph taken in
New Delhi, India (2001).

Tree photosynthesis the temporal separation of photosynthesis and nitrogen

fixation in Plectonema boryanum (Misra and Mahajan
Photosynthesis in trees was studied, e.g., in mango 2000). (For a historical account on energy transfer in
(Shivashankara and Mathai 2000), rubber (Devakumar plants and algae, see M. Mimuro 2002.) In a recent
et al. 1999), tea (Joshi and Palni 1998), and Populus and very interesting report, Misra et al. (2003) ob-
(Pathre et al. 1998). Sucrose phosphate synthase in the served an alternate photosynthetic donor system for
leaves of Prosopis juliflora was activated on illumin- PS I supported light dependent nitrogen fixation in P.
ation, due to protein dephosphorylation (Pathre et al. boryanum.
2000). (The work on chloroplast genome in Populus High light causes photooxidative damage due to
has already been mentioned in the previous section on rise in lipid peroxidation (D.P. Singh et al. 1995).
‘Molecular biology of chloroplasts.’) PS II was found to be susceptible to NaCl stress (K.
Verma and Mohanty 2000), UV-B (Pandey et al. 1997;
Rajagopal et al. 1998) or heavy metals (Murthy et
Cyanobacterial photosynthesis al. 1989; D.P. Singh and Singh 1987). Cobalt ions
enhanced the light tolerance and altered the energy
Joseph Thomas (while at BARC, Mumbai) provided distribution in Synechocystis (Tiwari and Mohanty
the first evidence that heterocysts of cyanobacteria 1993). Besides quinones, phycobilisomes serve as the
lack PS II and maintain the anaerobic milieu essen- primary targets of UV-B triggered dissociation of PS
tial for their nitrogen fixation (Thomas 1970). He II in intact cyanobacteria (Rajagopal et al. 1998).
also measured the absorption spectrum of a single Mutants have been found which are tolerant to high
cyanobacterial cell. Several groups studied the charac- light and other stresses (D.P. Singh and Singh 1997;
teristics of phycobilisomes and photosystems and their D.P. Singh and Verma 1995). These mutants would
responses to a variety of stresses in cyanobacteria. be very useful to further examine the mechanism of
(For a historical account on phycobilisomes, see N. tolerance of photosynthesis to different stresses.
Tandeau de Marsac, this issue.) One of the important
findings is the existence of variable long wavelength
77K fluorescence emission originating from PS I, the Concluding remarks
yield of which was linked to the reduced state of
P700, the primary electron donor of PS I (Shubin et Besides several original significant and interesting
al. 1991). Excitation energy transfer from phycobil- contributions, the Indian researchers have edited and
isomes to photosystems was an important link during authored several books, conference proceedings and
 445

special issues of journals, which serve as excellent Notes

additions to the international photosynthesis literat-
1 In the 1924 book, the first and the middle names of J. C. Bose
ure (see Appendix). Despite being from a developing
are listed as Jagdis and Chunder instead of Jagdish and Chandra.
country, Indian Scientists have thrived hard to excel 2 At about the same time as J.C. Bose, Dastur (1924) studied
in research. A major part of the research in Indian the importance of water content in aging leaves. This work was fol-
laboratories is carried out by the PhD students. For lowed by Dastur in 1925, and, then with N.A. Buhariwalla in 1928.
example, the doctoral students, from several Indian Several scientists from the Indian subcontinent, however, studied
respiration under the English plant physiologist F. F. Blackman
laboratories, have contributed immensely to the pro- (1866–1947), known since 1905 for the ‘law of limiting factors’
gress of photosynthesis research in India. As an ex- in photosynthesis. These included T. Ekambaram, R.S. Inamdar,
ample, we list here the past PhD students3 of the Rafique Ahmad Khan, P. Parija, Shri Ranjan and S.B. Singh (see
Blackman 1954, pp. 230–231). This book was actually produced
authors of this paper. by G.E. Briggs after Blackman’s death, and shows the extensive
Most of the early research was on the physiology contributions of Parija to Blackman’s research.
and biochemistry of photosynthesis. During recent 3 A partial list of PhD (graduate) students of the authors

years, focus has shifted onto the molecular biology of of this article: Students of A.S. Raghavendra: Thurumella Vani,
Rita Ghosh, Madhumanchi T. Devi, A.V. Rajagopalan, Kanak-
chloroplasts (Sopory and Maheswari 2001) and this agiri Saradadevi, Jagannath Gayathri, Kota Parvathi and Kollipara
was evident at an International Conference held in Padmasree. Students of P.V. Sane: Jayashree K. Sainis, Anuj K.
New Delhi (Figure 5). Such approach is appropriate to Singh, Munna Singh, Jaspreet Arora, Vidhu Bijola, Prabodh K.
strengthen research in plant biotechnology, including Trivedi, Pankaj Jaiswal, Purnima Seth, Rekha Sharma, M.S.S.
Reddy, Aashish Srivastava, Puneet Dhawan, Sangeeta Saxena, Vi-
areas such as chloroplast transformation and genom- pin Hallan, Nidhi Agarwal, Alok K. Sinha and Promod A. Shirke.
ics/proteomics of photosynthesis (Raghuram 2002). Students of P. Mohanty: Baishnab C. Tripathy, Sabeer A. Sayeed,
India is an agriculturally important country and Ramakrishna A. Wavare, Narendra Mohanty, S.D. Srinivasa Murthy,
photosynthesis research in India has always found sup- Bagawatula Vani, Jogadhenu S.S. Prakash, Manoj Joshi, Madhulika
Srivastava, Swati Tiwari, Neelima Atal, Sangeeta Dawar and Jerome
port from the people and the government. We envisage F. Sah.
that the research on this unique aspect of plant science
would make further progress.
Appendix

Books, conference proceedings and special issues of scientific

Acknowledgments journals on photosynthesis edited by Indian scientists (in chrono-
logical order)

We acknowledge with thanks the reprints from sev- Books

eral colleagues. We thank and appreciate Govindjee
for his advice and help in several ways. Photosyn- Biswal UC and Britton G (eds) (1989) Trends in Photosynthesis
Research. Agrobotanical Publishers, Bikaner, India
thesis research in India is supported by generous
funding from several agencies, particularly Council Abrol YP, Mohanty P and Govindjee (eds) (1993) Photosynthesis:
Photoreactions to Plant Productivity. IBH Publishing Co. Pvt.
of Scientific and Industrial Research (CSIR), Depart- Ltd, New Delhi, India / Kluwer Academic Publishers, Dordrecht,
ment of Atomic Energy (DAE), Department of Bio- The Netherlands
technology (DBT), Department of Non-conventional
Raghavendra AS (ed) (1998) Photosynthesis: a Comprehensive
Energy Sources (DNES), Department of Environ- Treatise. Cambridge University Press, Cambridge, UK
ment (DOEN), Department of Science and Techno-
Singhal GS, Renger G, Sopory SK, Irrgang K-D and Govindjee
logy (DST), Indian Council of Agricultural Research (eds) (1999) Concepts in Photobiology: Photosynthesis and Pho-
(ICAR), Indian National Science Academy (INSA), tomorphogenesis. Narosa Publishing House, New Delhi, India /
University Grants Commission (UGC), US Depart- Kluwer Academic Publishers, Dordrecht, The Netherlands
ment of Agriculture (USDA), and Rockefeller Found- Yunus M, Pathre U and Mohanty P (eds) (2000) Probing Photo-
ation. Professor M. Siddiqi, Director, Bose Institute, synthesis: Mechanisms, Regulation and Adaptation. Taylor &
Kolkata, has kindly provided photographs of Sir J.C. Francis, London
Bose. We thank Professor C. Kannan and Dr. K. Conference proceedings and special issues of journals
Subrahmanyam, University of Hyderabad, for help in Mohanty P (ed) (1987) Indo-USSR Symposium on Photosynthesis
transliterating the shloka from Sanskrit into English. under Environmental Stress. Proc Indian National Sci Acad B53:
The preparation of this review is supported by a grant 369–574
to ASR (No. SP/SO/A22/98) from DST, New Delhi. Singhal GS, Barber J, Dilley RA, Govindjee, Haselkorn R and
This manuscript was edited by Govindjee. Mohanty P (eds) (1989) Photosynthesis: Molecular Biology
446

and Bioenergetics. Proceedings of International Workshop on triphosphatase and ribulose diphosphate carboxylase of chloro-
Application of Molecular Biology and Bioenergetics of Photo- plasts isolated from barley leaves senescing in darkness. Physiol
synthesis. Narosa Publishing House, New Delhi, India Plant 44: 127–133
Black CC and Osmond CB (2003) Crassulacean acid metabolism
Singhal GS and Bhagwat AS (eds) (1993) Proceedings of DAE photosynthesis: ‘working the night shift.’ Photosynth Res 76:
Symposium on Photosynthesis and Plant Molecular Biology. 329–341 (this issue)
Department of Atomic Energy, Bombay & Jawarharlal Nehru Blackman FF (1954) Analytic Studies in Plant Respiration. Cam-
University, New Delhi bridge University Press, Cambridge, UK
Chitnis PR and Mohanty P (eds) (2000) Photosynthesis Research in Bogorad L (2003) Photosynthesis research: advances through mo-
the Post-Genomic Era. Indian J Biochem Biophys 37: 351–520 lecular biology – the beginnings, 1975–1980s and on.... Photo-
synth Res 76: 13–33 (this issue)
Mohanty P and Raghavendra AS (eds) (2003) Special Issue on Bose A, Tiwari BS, Chattopadhyay MK, Gupta S and Ghosh B
Chloroplast Function. J Plant Physiol 160: 1–96 (1999) Thermal stress induces differential degradation of rubisco
in heat sensitive and heat tolerant rice. Physiol Plant 105: 89–94
Bose DM, Sen SN and Subbarayappa BV (1971) (eds) A Concise
History of Science in India. Indian National Science Academy,
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