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Chapter 1 Sir Jagadish Chandra Bose (1858–1937): A Pioneer in Photosynthesis

Research and Discoverer of Unique Carbon Assimilation in Hydrilla

Article · August 2010

DOI: 10.1007/978-90-481-9407-0_1

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 Chapter 1
Sir Jagadish Chandra Bose (1858–1937): A Pioneer
in Photosynthesis Research and Discoverer of Unique
Carbon Assimilation in Hydrilla

Agepati S. Raghavendra*
Department of Plant Sciences, School of Life Sciences, University of Hyderabad,
Hyderabad 500046, India

Govindjee
Department of Plant Biology, University of Illinois, 265 Morrill Hall, MC-116,
505 South Goodwin Avenue, Urbana, IL 61801-3707, USA

Summary������������������������������������������������������������������������������������������������������������������������������������������������������������������   3
I. Introduction.........................................................................................................................................................   4
II. Life of Sir J.C. Bose............................................................................................................................................   4
III. Out of Box Concepts and Innovative Instruments for Biological Experiments....................................................   5
IV. Classic and Comprehensive Monographs on Physiology of Plants...................................................................   6
V. Work on Photosynthesis and Focus on Hydrilla.................................................................................................   6
VI. Importance of Malate and Operation of C4-like Pathway....................................................................................   7
VII. Contemporary View of his Observations on Hydrilla..........................................................................................   7
VIII. Observations on Inhibitors/Stimulants on Photosynthesis in Hydrilla.................................................................   8
IX. Concluding Remarks: Inspiration for Biology Research in India and a Pioneer of Photosynthesis
Research on Hydrilla ����������������������������������������������������������������������������������������������������������������������������������������   9
Acknowledgments..................................................................................................................................................... 10
References................................................................................................................................................................10

Summary

Sir Jagadish Chandra Bose (1858–1937) is acknowledged as the greatest interdisciplinary scientist in
India; he was a pioneer of not only Physics, but of Plant Biology. Essentially, he was the father of Bio-
physics, long before it became a field. He was almost 60 years ahead of his time in his ideas, research
and analysis. Bose had several out-of-box concepts and designed his own innovative instruments to
facilitate his research. He made several discoveries during his studies on physiology and biophysics of
plants, particularly the electrical nature of conduction of various stimuli. His interest shifted during early
1920s from physics towards the physiology of plant movements and then photosynthesis. He fabricated
and used a unique photosynthesis recorder to study extensively the carbon assimilation pattern, actually
measured through oxygen evolution, in an aquatic plant, Hydrilla verticillata. Bose made a phenomenal
discovery that a unique type of carbon fixation pathway operated in Hydrilla. The plants of Hydrilla dur-
ing summer time were more efficient in utilizing CO2 and light. The summer-type plants used malate as

* Author for Correspondence, e-mail: [email protected]

Agepati S. Raghavendra and Rowan F. Sage (eds.), C4 Photosynthesis and Related CO2 Concentrating Mechanisms, pp. 3–11. 3
© Springer Science+Business Media B.V. 2011
4 Agepati S. Raghavendra and Govindjee

a source of CO2 and appeared to be different from Crasulacean Acid Metabolism (CAM) plants. These
findings of Bose appeared anomalous at his time but are now known to illustrate an instance of non-
Kranz single cell type C4-mechanism. In view of his major research contributions, we consider J.C. Bose
as a pioneer of photosynthesis research not only in India but also in the world.

I. Introduction University in 1896 for his work on the determi-

nation of wavelength of electric radiation by dif-
Two prominent names come up when we consider fraction grating (Ray and Bhattacharya, 1963).
the scientific research in contemporary India: Sir Bose retired from the Presidency College in
Jagadish Chandra Bose (also known as Jagdish 1915 and joined in the same year as an Emeri-
Chander Basu; November 30, 1858 to November tus Professor in the newly founded Department
23, 1937), popularly known as J.C. Bose and Sir of Physics in the University College of Science,
Chandrasekhara Venkata Raman (November 7, Calcutta. He utilized his scholarly background in
1888 to November 21, 1970), who was a 1930
Nobel laureate in Physics, for the discovery of the
Raman Effect. In biology, the contributions of Sir
J.C. Bose (Fig.  1) are awesome and outstand-
ing. Bose was an outstanding physicist as well
as a biologist, a pioneer of Biophysics. With his
initial interest in electromagnetism and exploita-
tion of electromagnetic waves, he invented sev-
eral devices for radio-communication with short
waves. Later, his attention turned towards the
movements and electrical responses in biologi-
cal systems, mainly of plants. He was a rare gen-
ius who was highly versatile and contributed to
diverse fields of not only science (physics/biol-
ogy/botany/biophysics/ archaeology) but also the
Bengali literature; he also wrote science fiction in
Bengali. See Geddes (1920), Ray and Bhattach-
arya (1963) and Salwi (2002) for his biography.

II. Life of Sir J.C. Bose

Sir Jagadish Chandra Bose was born on 30 Novem-

ber 1858, at Mymensingh, now in Bangladesh. He
had a graduate degree in science from St. Xaviers
College, Calcutta (now Kolkata) and obtained an
honors degree, as well as a National Science Tri-
pos in Physics, from Cambridge University, UK,
in 1884. Soon after his return from Cambridge in
Fig. 1. (a) Portrait of J.C. Bose. (b) J.C. Bose at the Royal
1885, he was appointed a Professor of Physics in Institution, London, with his radio equipment. The date is
Presidency College, Calcutta. Here, he initiated 1897, prior to his plant research. (c) The Museum located in
his experiments in various areas in physics and Bose institute, displaying the work and several innovative
botany. He received the D.Sc. degree of London instruments developed by J.C. Bose. (d)  Bust of Sir J.C.
Bose, in the Museum; on the right of the bust, a potted plant
of Mimosa pudica can be seen. (e) Plaque of J.C. Bose, in the
museum, Bose Institute, Kolkata. (f) Samadhi (holy grave) of
Abbreviations: CAM – Crassulacean acid metabolism; Sir J.C. Bose, in the courtyard of the main campus of the Bose
J.C. Bose – Sir Jagadish Chandra Bose Institute (Courtesy: Bose Institute).
1  Sir Jagadish Chandra Bose (1858–1937) 5

Physics to initiate path-breaking work in Plant contemporarily with Marconi of Italy, Bose did
Biology, specifically Plant Physiology. He could not get proper recognition, as he did not patent the
unequivocally demonstrate scientifically that device. One of the innovative concepts of Bose was
plants had life, something everyone knew, and that plants and metals have ‘life’ on the basis of
responded to stimuli, as in the case of animals their electrical responses. We, of course, know that
(Sen, 1997). Bose was conferred the Knight- life, as we understand it today, is not in ‘metals’: it
hood in 1916 and was elected a Fellow of the was only a way of expressing himself at that time
Royal Society, England, in 1920. He is respected because he was trying to bridge physics and biol-
throughout India as ‘Acharya’, meaning the most ogy! He proved that plants as well as animals use
revered teacher. He established the Bose Institute electric signals to carry and convey information.
(then called Basu Bigyan Mandir) in 1917. The
Bose Institute (Fig. 2) was then devoted mainly
to the study of plants. The Institute’s research III.  Out of Box Concepts
interests expanded gradually into several other and Innovative Instruments
related subjects. At present, Bose Institute is one for Biological Experiments
of the pioneering research institutions in India
(for further details of the Bose Institute, visit their Several of the concepts/explanations pro-
website: http://www.boseinst.ernet.in). J.C. Bose posed by Sir J.C. Bose were all of out-of-box
passed away on 23 November 1937 at Giridih in approach at those times. His comprehensive
Bihar, India. experiments in photosynthesis, physiology,
The extensive studies of J.C. Bose on the pho- physics, his monumental monographs and his
tosynthetic characteristics of Hydrilla, and his innovative work on plant physiology, made him
leading contributions to photosynthesis research a pioneer and an icon of biological research in
in India are highlighted in several articles (see India. His contributions to the communication
S. Bose, 1982; S. Bose and Rao, 1988; Raghav- systems in biology as well as physics are amaz-
endra et al., 2003; Mukherjee and Sen, 2007). ing. He devoted strong attention to studies on
His basic approach was to study electromag- the biology of movements, feelings and nervous
netic waves, their properties and their practical system. The word ‘feelings’ was used for plants,
applications in both living and nonliving objects. but clearly this is a matter of semantics; plants
This approach of applying physical principles to react both chemically and physically to touch,
biological system developed into the exciting field but to use the word ‘feeling’ or ‘sensation’ as we
of biophysics. Despite his inventing the radio, know it is quite different. The simple experiments

Fig. 2. Bose Institute, Kolkata. On the left (a) is the Main Campus, started in 1917 and located on Acharya Prafulla Chandra Road,
near Raja Bazaar in Kolkata. On the right (b) is New Building, in the “Acharya J.C. Bose Centenary Campus” at Kankurgachi,
Kolkata. This campus was built to commemorate the birth centenary of Sir J.C. Bose (Courtesy: Bose Institute, Kolkata, 2008).
6 Agepati S. Raghavendra and Govindjee

of Bose revealed a high degree of similarity in

the responses of plant and animal tissues to
external stimuli. This principle was amply dem-
onstrated later by biophysicists, using highly
sophisticated instruments (Shepherd, 1999, 2005).
The areas of Bose’s research included electro-
physiology, physiology of ascent of sap, move-
ment in plants, mechanisms of plant response to
varieties of stimuli, and physiology of photosyn-
thesis. Three notable features/objectives of his
research were: (a) to measure the responses quan-
titatively; (b) to design and to build the physical
instruments required for the purpose; and (c) to
interpret the results quantitatively in terms of the
physicochemical principles known at that time to
him. During his research career, Bose designed
and utilized several innovative instruments, which
looked simple, but were very sensitive and capa-
ble of measuring minute changes (Table 1). Only
some of these instruments were patented. One
of these most fascinating instruments was the
Photosynthesis Recorder that can detect the for-
mation of carbohydrate as a millionth of a gram Fig. 3. The Photosynthesis Recorder fabricated by J.C .Bose
per minute, and record the rate of photosynthetic and used extensively for his experiments on photosynthesis
in Hydrilla (Bose, 1924). This photograph is that of an
activity (Fig. 3). exhibit in the J.C. Bose Museum in Kolkota, taken by one of
us (Govindjee) in January, 2008.

IV.  Classic and Comprehensive

Monographs on Physiology prehensively in the form of books – monographs.
of Plants This apparently had the disadvantage of his research
being not in a format for scrutiny by the peers since
Sir J.C. Bose was never in a hurry to publish small often experimental details were not available. One
scientific articles. He studied the phenomena in of his books was on “Responses in the Living and
detail and then published his observations com- Non-living”, published by Longman in 1902. This
monograph made him a celebrity in the world of
Table  1. A partial list of the novel and innovative instru- science. His other important publications again
ments fabricated by Sir J.C. Bose. were mostly monographs, including the one on
Instrument Purpose/parameter of measurement “Physiology of Photosynthesis”, published in 1924
Oscillating recorder Ascent of sap (Table  2). His observations have been published
Photosynthetic Rate of carbon assimilation by in several volumes by Longmans, Green and Co.
recorder plants Ltd., England during 1902–1928.
Crescograph Growth of a plant
Magnetic Movements beyond the magnifying
Crescograph capacity of light microscope V.  Work on Photosynthesis and Focus
Transpirograph Quantity of water transpired by a on Hydrilla
single stoma of the leaf
Magnetic radiometer Measure energy of every ray in the
solar spectrum During his research life, Bose carried out impor-
Resonant recorder Determination of the latent period tant and thought-provoking experiments on pho-
of the plant within millisecond tosynthesis, particularly on its physiological
Conductivity balance Determine the effect of various aspects. In the simplest terms, photosynthesis in
drugs on electrical impulse plants may be described as the process by which
1  Sir Jagadish Chandra Bose (1858–1937) 7

Table 2. Books written by J.C. Bose on physiology and coefficient of Hydrilla in winter was about 40,
physics of plant cells, including photosynthesis. which nearly doubled in summer (Table 3). This
Bose JC (1902) Response in the living and nonliving. was a clear demonstration of the marked increase
Longmans, Green & Co., London in the photosynthetic efficiency of carbon assimi-
Bose JC (1906) Plant response as a means of physiological lation in Hydrilla during summer time.
investigation. Longmans, Green & Co., London
Bose JC (1907) Comparative electrophysiology.
Longmans, Green & Co., London
Bose JC (1913) Researches on the irritability of plants.
VI.  Importance of Malate and Operation
Longmans, Green & Co. London of C4-like Pathway
Bose JC (1923) The physiology of the ascent of sap.
Longmans, Green & Co., London In the early 1920s, Sir J.C. Bose showed that in
Bose JC (1924) The physiology of photosynthesis. the aquatic plant, Hydrilla, the photosynthetic
Longmans, Green & Co., London characteristics in summer were quite different
Bose JC (1926) The nervous mechanism of plants. from those in winter. Some of his major obser-
Longmans, Green & Co., London
Bose JC (1927) The plant autographs and their
vations are summarized in Table 3. Bose (1924)
revelations. The Macmillan Company, New York further observed that ‘while the juice of the plant
Bose JC (1928a) The motor mechanism of plants. was practically neutral in winter and spring, it
Longmans, Green & Co., London was very strongly acid in summer’. Furthermore,
Bose JC (1928b) Growth and tropic movements of plants. ‘the acidity of the plants was found to be due to
Longmans, Green & Co. London the presence of malic and oxalic acids, the latter
Bose JC (1985) Life movements in plants. Reprinted and
distributed by D.K. Publishers’ Distributors, Kolkata in small quantities’.
Bose (1924) observed that photosynthesis
in Hydrilla was unique, because of the follow-
CO2 and H2O are taken up, forming carbohydrate ing features: (a) Acids, mainly malate, accumu-
and releasing oxygen, using Light. Bose presented lated; (b) Malic acid was a source/substitute for
the results of his comprehensive studies on photo- CO2; and (c) Photosynthesis could occur without
synthesis, in the form of a book, ‘The Physiology external addition of CO2. Hydrilla plants, at high
of Photosynthesis’ (Bose, 1924). The comparative temperatures of summer, became acidic. Photo-
results and discussion of Bose’s investigation with synthesis, measured by the evolution of oxygen,
Hydrilla in summer and winter seasons are avail- apparently, occurred also in the complete absence
able in the articles of S. Bose (1982) and S. Bose of externally added CO2. Bose studied the assimi-
and Rao (1988). During J.C. Bose’s time, biochem- lation of organic acids by substituting malic acid
ical interpretations were not available. Subsequent for CO2 and found that the photosynthesis curves
work provided detailed explanations of unique of Hydrilla under increasing concentration of
photosynthetic characteristics of Hydrilla, which CO2 or of malic acid solutions were quite similar
could be ascribed to a variant of carbon assimila- (Bose, 1924; see S. Bose and Rao, 1988). Thus, he
tion or CO2 concentra­ting mechanism called C4- demonstrated that during photosynthesis, Hydrilla
pathway (Leegood et al., 2000). assimilated malate instead of CO2 and that uptake
J.C. Bose had selected the aquatic plant Hydrilla of CO2 by these plants is less than normal. It is
and used it extensively for his studies. He ascribed quite astonishing that as early as 1924, Bose had
the following reasons for selecting the plant (Bose, visualized the idea of the operation, in Hydrilla,
1924): (a) The plant can be maintained under of a quite different photosynthetic pathway, which
normal conditions in a vessel of water; (b) The utilizes malate.
leaves have no stomata and there is no transpira-
tion, making the system very simple; and (c) The
oxygen released into intercellular species can VII.  Contemporary View
easily escape out into the medium. Bose (1924) of his Observations on Hydrilla
investigated the relation between CO2 supply and
photosynthesis and defined the coefficient for The primary route of carbon assimilation through
CO2 concentration as a measure of the efficiency Calvin-Benson-Bassham cycle or C3-pathway
of CO2 utilization. The average value of CO2 was established by the research group of Melvin
8 Agepati S. Raghavendra and Govindjee

Table 3. Photosynthetic characteristics of winter and summer Hydrilla.

Form of hydrilla
Characteristic Winter Summer
Optimum temperature of photosynthesis (°C) 28   33
Light-saturated rate of photosynthesis (arbitrary units, cm m−1 h−1) a 147 362
Light compensation point (in lux) 205   25
Relative quantum yield (initial slope of photosynthesis versus light intensity curve) 12   25
Efficiency of CO2 utilization (initial slope of photosynthesis versus CO2 concentration curve) 40   71
CO 2 compensation point (mg CO 2 water (100 mL)−1) 1.2   0
Data adapted from Bose (1924); average values are shown
a
Displacement of air column by O2

Calvin and Andy Benson and their coworkers were studied in detail after more than 50 years,
(Bassham and Calvin, 1957; Benson, 2002; by the research group of George Bowes. Their
­Bassham, 2003). The variant of carbon assimila- results offered a candid explanation of several of
tion through C-4 acids was identified and charac- the observations made by J.C. Bose (Table  4).
terized more than a decade later (see e.g., Hatch, The carbon assimilation pathway in Hydrilla
2002). The third type of carbon assimilation is turned out to be quite unique and is now being
Crassulacean Acid metabolism (CAM) that also termed as an example of non-Kranz single cell
uses malate and other acids for concentrating CO2 C4-pathway operating in aquatic angiosperms
inside the cells during darkness (or night); they (see Chapter 5, by Bowes, this volume).
use these acids up during subsequent day time
(Black and Osmond, 2003).
Bose was aware that his observation with
summer Hydrilla was different from the phe- VIII.  Observations on Inhibitors/
nomenon of acid accumulation by many succu- Stimulants on Photosynthesis
lent or CAM plants. He said: ‘The organic acids in Hydrilla
stored during the night (in succulent plants) pro-
vide indirect material for photosynthesis dur- J.C. Bose examined the effects of several com-
ing the day in the form of CO2. The Hydrilla pounds which either stimulated or inhibited
plant appeared to be most suitable for further the rate of photosynthesis depending on the
investigation on the subject that the organic nature and concentration of the compounds
acid served directly for photosynthesis’ (Bose, (Bose, 1923). His observations on the stimula-
1924). Although he proposed that malic acid was tory effects by almost infinitesimal quantities
used directly as a substitute of CO2 by summer of different chemical agents were triggered by
plants, Bose’s observations and the available a casual observation that the rate of photosyn-
biochemistry were not detailed enough to sug- thesis of certain water plants increased sharply
gest any C4-mechanism in Hydrilla. Although during a thunderstorm. Bose attributed this phe-
the knowledge of biochemistry of photosyn- nomenon to the oxides of nitrogen produced by
thesis was almost nonexistent in the 1920s, his electric discharges in the atmosphere; this con-
observations and inference, nevertheless, clearly clusion induced him to investigate the effects on
indicated a mechanism different from CAM and photosynthesis of various stimulants. He found
which is now known as the C4-pathway (Bowes that the photosynthesis of Hydrilla verticillata
et al., 2002). was tripled by nitric acid and doubled by thy-
The physiology, biochemistry and molecular roid gland extract. Iodine and formaldehyde
biology of photosynthetic carbon assimilation in increased the photosynthetic rate 60% and 80%,
aquatic plants, including Hydrilla verticillata, respectively.
1  Sir Jagadish Chandra Bose (1858–1937) 9

Table 4. The simple observations by J.C. Bose and the independent biochemical characterization of photosynthesis in
Hydrilla, made by the group of George Bowes.
Observation by J.C. Bosea Biochemical basis Referenceb
Low light compensation in summer Low light compensation point compared to Van et al., 1976
other hydrophytes, such as Myriophyllum or
Ceratophyllum
Summer/winter type Result of daylength and the temperature. Summer type Holaday and Bowes, 1980
at 27°C/14-h photoperiod and winter type at 11°C/9-h
photoperiod
Malate is a major product Over 50% of carbon assimilated into malate, as shown Salvucci and Bowes, 1983
of photosynthesis by the incorporation of 14CO2
CO2 compensation point Measured precisely; CO2 compensation points Magnin et al., 1997
of >50 mL L−1 in summer type and 1–25 mL L−1
in winter type
Photosynthetic rate in summer type Activity of PEP (phospho-enol pyruvate)carboxylase, Rao et al., 2006
plants is 2.5 times greater than that of the key enzyme for carbon fixation, is enhanced nearly
winter type 10 times in summer forms (C4-type), compared to winter
form (C3-type)
Malate is a source of CO2 for Efficient utilization of malate leading to a reduction Estavillo et al., 2007
photosynthesis in photorespiration; Malate decarboxylated by NADP
malic enzyme
From Bose (1924)
a

Arranged in chronological order

b

IX.  Concluding Remarks: Inspiration early pioneer in research in the field of photosyn-
for Biology Research in India thesis, particularly carbon assimilation. It seems
and a Pioneer of Photosynthesis that Eugene Rabinowitch did not discuss Bose’s
Research on Hydrilla work, perhaps because it was not published in reg-
ular journals, yet Rabinowitch (1951, p. 1079) did
The observations of Sir Jagadish Chandra Bose on mention his 1924 book.
“feelings” and movements in plants can be treated Bose’s thoughts and vision have illuminated
as the earliest studies on the “intelligence” of plants, the path of research since 1920s and they became
which is being termed by some as ‘plant neurobiol- a source of inspiration to several of his students,
ogy’ (Brenner et al., 2006). As mentioned earlier, who all became great scientists in either physics
the use of the words “feelings” and “intelligence” or biology. Among these stalwarts are: Meghnad
for plants is a matter of semantics, and we need to Saha, J.C. Ghosh, S. Dutta, Satyendra Nath Bose,
caution the readers against their misinterpretation. D.M. Bose, N.R. Sen, J.N. Mukherjee and N.C.
However, the experiments of J.C. Bose to measure Nag, to name a few. Among his students, Saty-
minute electrical signals in plants have been recog- endra Nath Bose (January 1, 1891 to February 4,
nized and have paved the way for the biophysics of 1974) was the most famous as he is known the
plant cells (Shepherd, 1999, 2005). The anomalies world-over for the Bose-Einstein’s statistics, and
recorded by Bose in the patterns of plant growth for the particle ‘Boson’ named after him. The
are now confirmed to be due to their oscillatory (J.C.) Bose Institute in Kolkata is keeping up his
behavior, found by much sophisticated computer motto and is training several young Indian sci-
based image analysis system (Jaffe et  al., 1985). entists and offering state-of-the-art facilities in
The biological significance of seasonal and diur- physics and biology. The Bose Institute organ-
nal adaptation became the subject matter of mod- ized an year-long celebrations of the 150th birth
ern research in chronobiology (Chandrasekharan, anniversary of its founder during 2008 (Fig. 4).
1998). Bose’s, 1924 work on photosynthesis with It is no wonder that Sir J.C. Bose is treated as
Hydrilla is a landmark in photosynthetic research. the first Modern Scientist and a pioneer in India
Sir J.C. Bose is therefore rightly considered as an (Salwi, 2002; Yadugiri, 2010).
10 Agepati S. Raghavendra and Govindjee

Fig. 4. One of us (Govindjee) honoring Sir J.C. Bose by lighting a lamp on November 24, 2008, in front of his statue, located
at the entrance of Acharya Jagadish Chandra Bose’s Museum, on the Main campus of Bose Institute, Kolkata. This photograph
was taken on the occasion of the Inaugural function of an International Symposium, commemorating the 150th birth year of Sir
J.C. Bose. Prof. Arun Lahiri Majumder and three Ph. D. students, of the Bose Institute, are also in the picture (Courtesy: Arun
Lahiri Majumder and Sampa Das, 2008).

Acknowledgments Bose JC (1924) Physiology of Photosynthesis. Longmans,

Green & Co., London
The preparation of this chapter was supported by Bose S (1982) J.C. Bose’s work on plant life 1. Comparative
studies of the photosynthetic characteristics of summer
a grant from J.C. Bose National Fellowship (No.
and winter Hydrilla specimens. Discovery of C4 charac-
SR/S2/JCB-06/2006, to ASR) of the Department teristics in 1924? Trans Bose Res Inst 45: 63–70
of Science and Technology (DST), New Delhi, Bose S and Rao PK (1988) History of photosynthesis
India. Govindjee was supported by the Depart- research in India. In: Sen SP (ed) Plant Physiological
ment of Plant Biology of the University of Illinois Research in India, pp 43–74. Society for Plant Physiology
at Urbana-Champaign. and Biochemistry, New Delhi
Bowes G, Rao SK, Estavillo GM and Reiskind JB (2002)
C4 mechanisms in aquatic angiosperms: comparisons with
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