C₄ plant biology

583 Pages·1999·32.818 MB·English

by  Rowan Frederick Sage, R K Monson

Contributors
Numbers in parentheses indicate the pages on which the authors' contributions begin.
R. Harold Brown (473), Department of Crop and Soil Sciences, University
of Georgia, Athens, Georgia 30602
Thure E. Ceding (445), Department of Geology and Geophysics, University
of Utah, Salt Lake City, Utah 84112
James s. Coleman (285), Department of Biology, Syracuse University, -aryS
cuse, New York, 13244; and Desert Research Institute, Reno, Nevada
89512
Nancy G. Dengler (133), Department of Botany, University of Toronto,
Toronto, Ontario S5M 3B2, Canada
Gerald E. Edwards (49), Department of Botany, Washington State Univer-
,ytis Pullman, Washington 99164
Robert T. Furbank (173), Division of Plant Industry, Commonwealth Scien-
tific and Industrial Research Organization, Canberra 2601, Australia
Marshall D. Hatch (17), CSIRO Plant Industry, Canberra 2601, Australia
Scott .A Heckathorn (285), Department of Biology, Syracuse University,
Syracuse, New York, 13244
Ryuzi Kanai (49), Department of Biochemistry and Molecular Biology,
Saitama University, Urawa 388, Japan
Elizabeth .A Kellogg (411), Department of Biology, University of Missouri,
.tS Louis, Missouri 68121
Alan .K Knapp (251), Division of Biology, Kansas State University, Manhat-
tan, Kansas 66506
Richard C. Leegood (89), Robert Hill Institute and Department of Animal
and Plant Science, University of Sheffield, Sheffield 01S 2UQ, United
Kingdom
Meirong Li (313, 551), Department of Botany, University of Toronto, To-
ronto, Ontario S5M 3B2, Canada
Steve P. Long (215), Department of Biological and Chemical Sciences,
John Tabor Laboratories, University of Essex, Colchester CO4 2SQ,
United Kingdom
Samuel J. McNaughton (285), Department of Biology, Syracuse University,
Syracuse, New York 13244
iix Contributors
Ernesto Medina (251), Centro de Ecologia, Instituto Venezolano de Investi-
gaciones Cientificas, Caracas, Venezuela
Russell K. Monson (377, 551), Department of E.P.O. Biology, University
of Colorado, Boulder, Colorado 80309
Timothy Nelson (133), Biology Department, Yale University, New Haven,
Connecticut 06520
Rowan F. Sage (3, 313, 551), Department of Botany, University of Toronto,
Toronto, Ontario M5S 3B2, Canada
Hartmut Tschauner (509), Department of Anthropology, Peabody Mu-
seum, Harvard University, Cambridge, Massachusetts 02138
Nikolaas J. van tier Merwe (509), Department of Anthropology, Peabody
Museum, Harvard University, Cambridge, Massachusetts 02138
Susanne yon Caemmerer (173), Research School of Biological Sciences,
Australian National University, Canberra 2601, Australia
Robert P. Walker (89), Robert Hill Institute and Department of Animal
and Plant Science, University of Sheffield, Sheffield $10 2UQ, United
Kingdom
David A. Wedin (313), School of Natural Resources, University of Nebraska,
Lincoln, Nebraska 68583
Preface
The spinach is a 3C plant
It has a Nobel pathway
Its compensation point is high
From early morn till noon-day.
It has carboxydismutase
But has no malate transferase;
The spinach is a regal plant
But lacks the Hatch-Slack pathway.
F. .A Smith, H. Beevers, and others
Sung to the tune of "O Tannenbaum"
Reprinted from Photosynthesis and Photorespiration
(1971" John Wiley & Sons, Inc., New York)
The eclectic mixture of seasonal frivolity and glee of scientific discovery
was obvious when 14 esteemed scientists took the floor to sing this musical
postscript to the Conference on Photosynthesis and Photorespiration in
Canberra, Australia, in early December 1970. The occasion marked the
close of one of the most influential conferences in the 20th century dealing
with the topic of photosynthesis. For the first time, scientists from around
the world had come together to synthesize the biochemistry, physiology,
anatomy, systematics, ecology, and economic significance of plants possess-
ing a unique pathway of photosynthetic CO2 assimilation. As one revisits
the proceedings from this meeting (Hatch et al., 1971), it is obvious, even
to those of us who were too young to attend the sessions, that the integrative
spirit of this group of scientists was seminal to the wave of understanding
of 4C photosynthesis that has been achieved in the almost 30 years since.
This book, although the product of a couple of 4C "baby-boomers," was
conceived and created as a salute to the seminal sessions of that 1970
meeting in Canberra and as means of restating the integrative necessity of
understanding 4C photosynthesis.
Three modes of photosynthesis predominate in terrestrial plants: the 3C
mode, which is employed by most higher plant species; the Crassulacean
XlII
xiv Preface
acid metabolism (CAM) mode, employed by 20,000 or more succulents
and epiphytes; and the 4C mode, employed by approximately 8000 of the
estimated 250,000 higher plant species. Although far fewer species use the
4C pathway, their ecological and economic significance si substantial. 4C
plants dominate all tropical and subtropical grasslands, most temperate
grasslands, and most disturbed landscapes in warmer regions of the world.
Major 4C crops include maize, sorghum, millets, and amaranths, and 8 of
the world's 01 most invasive weeds possess 4C photosynthesis. In addition
to its current economic significance, recent work indicates that the appear-
ance of 4C species in the vast grassland ecosystems of eastern Africa and
southwestern Asia in the past 10-20 million years greatly influenced evolu-
tionary patterns in many faunal lineages, including Homo sapiens. The spread
and domestication of 4C species in that region in the more recent past
have had major impacts on the timing and development of human societies.
The anthropological and ecological significance of 4C plants may increase
in the future, as C4-dominated savannas are thought to significantly influ-
ence the long-term carbon dynamics of the soil and atmosphere. The
responses of 4C savannas to future increases in atmospheric 2OC concentra-
tions and climate change lie at the foundation of any attempts to understand
and predict dynamics in the global carbon cycle. Because of these issues,
an improved understanding of the biology of 4C photosynthesis will be
required by more than the traditional audience of crop scientists, plant
physiologists, and plant ecologists. Land managers, paleoecologists, com-
munity and ecosystem ecologists, systematists, and anthropologists are some
of the specialists who could be well served by a comprehensive volume
summarizing our current knowledge of 4C plant biology.
This book has been produced with the aim of providing a broad overview
of the subject of 4C photosynthesis, while retaining enough scientific depth
to engage those scientists who specialize in 4C photosynthesis and to further
catalyze the integration that was begun at the Canberra conference. In
Chapter ,1 Sage provides a brief overview of why the 2OC concentrating
mechanism, which si a hallmark of 4C photosynthesis, may exist, focusing
on the evolutionary constraints imposed by more than 3 billion years of
photosynthetic existence in the ~C mode. In Chapter 2, Hal Hatch, one of
the discoverers of 4C photosynthesis, provides a firsthand account of the
events surrounding that incipient recognition that not all plants assimilate
2OC in the same way as Chlorella or spinach. The personal recollections
that Hal offers and the broad historical perspective that he provides to the
more recent discoveries associated with 4C photosynthesis are invaluable
parables to anyone wishing to understand the development of important
scientific disciplines. In the chapters following Hatch's historical overview,
the book takes on a loose hierarchy of scale, beginning at the level of
organelles and cells and progressing to communities and ecosystems. In
ecaferP
XV
chapters of the second section, including those by Ryuzi Kanai and Gerald
Edwards, Richard Leegood and Robert Walker, Nancy Dengler and Timothy
Nelson, and Susanne von Caemmerer and Robert Furbank, strong themes
of coordinated structure and function are developed. In chapters of the
third section, including those by Steve Long, Alan Knapp and Ernesto
Medina, Scott Heckathorn, Samuel McNaughton, and James Coleman, and
Rowan Sage, David Wedin, and Meirong Li, the dominant theme si that
of ecological performance and its translation into the geographic distribu-
tion of 4C plants. In chapters of the fourth section, including those by
Russell Monson, Elizabeth Kellogg, and Thure Cerling, 4C evolutionary
patterns are considered. These patterns include the evolutionary patterns
within the biochemistry of 4C photosynthesis, within the phylogenetic rec-
ord of 4C photosynthesis, and within the fossil record of 4C photosynthesis.
In the fifth group of chapters, the topic of 4C photosynthesis in relation
to human societies si developed. This section includes chapters by Harold
Brown and by Nicolaas van der Merwe and Hartmut Tschauner, who focus
on the relevance of 4C photosynthesis to agriculture and the role of 4C
photosynthesis in the development of agrarian human societies. The final
chapter of the book, by Rowan Sage, Meirong Li, and Russell Monson, si
devoted to the known systematic distribution of 4C photosynthesis, including
a comprehensive list of 4C taxa.
The production of this book required the energy and wisdom of many
collaborators. We especially acknowledge the encouragement of Jim Ehler-
inger and Bob Pearcy, who initially approached us with the idea of putting
together a book like this. Our editor at Academic Press, Chuck Crumly,
was both encouraging and patient as we worked through the complexities
of soliciting and editing the various chapter manuscripts. We thank the
many reviewers of the chapters for their valuable input. We especially thank
our families for their patience, support, and understanding during long
hours of writing and editing. Above all, we thank those authors who contrib-
uted chapters to the book. These individuals represent some of the most
enthusiastic students of 4C photosynthesis, and those that are carrying the
spirit of the Canberra conference forward into the next 30 years of research.
NAWOR F. EGAS
LLESSUR ~ NOSNOM
Reference
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Rowan F. Sage
I. Introduction
The net acquisition of carbon by photosynthetic organisms si catalyzed
by ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) through the
carboxylation of RuBP, forming two phosphoglyceric acid (PGA) molecules.
In addition to RuBP carboxylation, Rubisco catalyzes a second reaction, the
oxygenation of RuBP, producing phosphoglycolate (Fig. 1). Oxygenation si
considered a wasteful side reaction of Rubisco because it uses active sites
that otherwise would be used for carboxylation, it consumes RuBP, and
the recovery of carbon in phosphogylcolate consumes ATP and reducing
equivalents while releasing previously fixed 2OC (Sharkey, 1985). Oxygen-
ation may be inevitable, given similarities in the reaction sequence for
oxygenation and carboxylation of RuBP (Andrews et al., 1987). From an
evolutionary standpoint, oxygenation could be considered a design flaw
that reduces Rubisco performance under a specific set of conditions. Should
those conditions ever arise and persist, then opportunities may exist for
alternative physiological modes to evolve. 4C photosynthesis appears to be
one such alternative, appearing in response to the prehistoric advent of
atmospheric conditions that allowed for significant oxygenase activity and
photorespiration (Ehleringer et al., 1991).
II. The Problem with Rubisco
Rubisco evolved early in the history of life, more than 3 billion years ago
(Hayes, 1994). The 2OC content of the atmosphere at this time was orders
Copyright (cid:14)9 1999 by Academic Press
4C Plant ygoloiB 3 All rights of reproduction in any form reserved.
4 Rowan .F Sage
Photorespiration Photosynthesis
20 20C
.%-s/ \it"
PTA PTA
NADPH NADPH
Figure I A schematic of eht /notaripserotohp elcyc and .sisehtnysotohp sisehtnysotohP
occurs when RuBP si carboxylated by Rubisco, and the products (two phosphoglyceric acid
molecules; PGA) are processed into carbohydrates and used to regenerate RuBP in reaction
sequences requiring ATP and NADPH. Photorespiration begins with the oxygenation of
RuBP to form one phosphoglycolate (PG) and PGA, in a side reaction catalyzed by Rubisco.
Processing the phosphoglycolate to PGA and eventually RuBP requires ATP and reducing
power (indicated by NADPH).
of magnitude greater than now, and 0 2 was rare (Fig. ;A2 Kasting, 1987;
Holland, 1994). In this environment, oxygenase activity was uncommon,
probably less than one oxygenation per billion carboxylations (Fig. 2C).
Atmospheric 02 level remained low and was unable to support an oxygen-
ation rate that was more than 1% of the carboxylation rate until approxi-
mately 2 billion years ago. At this time, atmospheric 2O began to rise,
eventually surpassing 200 mbar (20%) about 0.6 billion years ago (Kasting,
1987; Berner and Canfield, 1989; Holland, 1994). Atmospheric CO2 level
continuously declined prior to 1 billion years ago, yet at the advent of
the first land plants some 450 million years ago, atmospheric CO2 was still
high enough to saturate Rubisco and minimize oxygenase activity (Fig.
2C). Coal-forming forests of the Carboniferous period (360 to 280 million
years ago) contributed to a reduction in CO2 partial pressures to less than
500 mbar and a rise in 02 partial pressures to more than 300 mbar (Berner
and Canfield, 1989; Berner, 1994). As a consequence, Rubisco oxygenase
activity is predicted to have become significant (>20% of the carboxylation
rate at 30~ for the first time in nonstressed plants at the prevailing
atmospheric conditions (Fig. 2B,D). After the Carboniferous period, CO2
levels are modeled to have risen to more than five times current levels for
about 200 million years, and the rate of RuBP oxygenation was again a
small percentage of the carboxylation rate. Over the past 100 million years,
atmospheric CO2 levels declined from more than 1,000/zbar, eventually
.1 yhW Q sisehtnysotohP ? 5
(cid:14)9 ~
j,--. 1 000 , , , , , , , A , , , , , , , , , , , 10
Rubisco appears ""
D(
800 - _ 8
i-
o
D.: 600
_k
Di
13_
o 400
...k
D(
:C_. 20
200 - - 2
3o
o
E
-~ 0 = ' I ' ' ~ I ' ,--K "T- "- C ~ ~ ' ~ D- o
< 0.5 O.5
0.4 - "" C 4 plants appearx \ _ 0.4
~. --
o
>o 0.3 - ? o *\ ~ 0.3
>' ~ ~" _ F kandplants / i _
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/\+ >o ;>o :..... I
0.1
0.0 , , , , , T - -*-~'**' ' ' ' ' ' ' 0.0
4 3 2 1 00.6 0.4 0.2 0.0
Time before present, years
billion
The modeled change ni cirehpsomta zOC dna 02 laitrap serusserp over )A( eht
Figure 2
tsap 4 billion years (adapted from ,gnitsaK 1987, dna Berner dna Canfield, 1989); dna
)B( eht past 006 million years (according ot Berner, 1994). C dna D present eht modeled
change in ocsibuR esanegyxo ytivitca )0v( ot esalyxobrac ytivitca )cv( ta ~03 rof eht -dnopserroc
ing 2OC dna zO levels presented ni A dna ,B ,ylevitcepser calculated assuming a spinach -sC
epyt ocsibuR according ot Jordan dna Ogren, .4891
falling below 200 /xbar during the Pleistocene epoch (2 to 0.01 million
years ago). In the last 15 million years, Rubisco oxygenase activity is modeled
to have risen above 20% of carboxylase activity at 30~ eventually surpassing
40% of carboxylase activity at the low CO2 levels (180/xbar) experienced
during the late Pleistocene (Fig. 2D). It is only after atmospheric CO2 levels
are low enough to allow the rate of RuBP oxygenation to exceed 20% to
30% of the carboxylation potential that 4C plants appear in the fossil record
(Cerling, Chapter 13). No evidence exists for 4C photosynthesis during the
Carboniferous (Cerling, Chapter 13).
Above 200 mbar oxygen, CO2 partial pressures of less than 500 /xbar
pose two problems. First, as a substrate for Rubisco carboxylation, CO2
availability becomes strongly limiting, reducing the turnover of the enzyme
in vivo and imposing a limitation on photosynthesis by reducing the capacity
of Rubisco to consume RuBP (Fig. 3A; Sage, 1995). Second, 2O competition
becomes significant at warmer temperature (> 30~ and this causes a high
rate of photorespiration (Fig. 3B; Sharkey, 1988; Sage, 1995). Whereas a
6 Rowan .F egaS
x E
o 50 A' '200 mbar '02 ' ' ~ ' '20~9 m'ber'O 2 ' 'B 100 Q..:D. _ O
_c
4-- o 40 /Ca=200 /l, rnol mo1-1 O8 ._ c
,//%=270 t
3O 6O o
._ > \! o~=oC o4 _S"o b
(cid:12)9 - 20 lff
o
< )1(
L
o 10 0
o ffl 0
c-
m 0 0OI i i 200 i,, i. 300 i i 400 i i 100 i ' 200 ' ' 300 ' ' 400 ' JO cl
231
Chloroplost /zmol mol -1
C02,
Figure 3 ehT modeled esnopser of )A( ocsibuR ytivitca sa( a percent of )~amV sa a noitcnuf
of stromal 2OC concentration, and (B) the percent of photorespiratory inhibition of photosyn-
thesis (0.5Vo/Vc x 100%). Modeled according to Sage (1995) using equations from Farquhar
and von Caemmerer (1982). aC indicates atmospheric 2OC content corresponding to indicated
chloroplast 2OC concentrations. (Note: at sea level,/imol mo1-1 =/lbar.)
CO2-substrate deficiency occurs only when the capacity for Rubisco to con-
sume RuBP limits the rate of CO2 assimilation in plants, photorespiration
is inhibitory regardless of whether Rubisco capacity or the capacity of the
leaf to regenerate RuBP limits photosynthesis (Sharkey, 1985). At current
CO2 levels, photorespiration can reduce photosynthesis by more than 40%
at warmer temperatures (Sharkey, 1988; Ehleringer et al., 1991).
The rise in photorespiratory potential triggered by the increase in the
atmospheric O2:CO2 over the past 50 million years created high evolutionary
pressure for dealing with the consequences of Rubisco oxygenation (Ehler-
inger et al., 1991). In all higher photosynthetic organisms, however, an
elaborate biochemical edifice was already built around Rubisco, such that
substantial barriers likely prevented the evolution of a novel carboxylase
to replace Rubisco. Not only would the new carboxylase be required, but the
accompanying biochemistry to regenerate acceptor molecules and process
photosynthetic products would likely have to change as well. Such new
photosynthetic systems would then have to compete against preexisting
Rubisco-based systems, which though inefficient, would have had the advan-
tage of working reasonably well and of being integrated into the associated
cellular, organismal, and ecological systems. To a large degree, the potential
for RuBP oxygenation represents a systematic constraint around which
evolution must work, an evolutionary spandrel sensu Gould and Lewontin
(1979) (Somerville et al., 1983). In a situation similar to that of a restoration
architect who is constrained by preexisting structures, evolution is con-
strained by preexisting enzymes, genes, and regulatory systems in dealing
1. Why 4C Photosynthesis ? 7
with novel challenges (Gould and Lewontin, 1979). In plants and algae,
the evolutionary response to declining atmospheric CO2 levels was to modify
existing leaf physiology to create CO2 concentrating systems ("CO2
pumps") that were coupled to preexisting Rubisco-based biochemistry. In
land plants, the most elaborate and successful of these modifications is aC
photosynthesis.
III. How 40 Photosynthesis Solves the Rubisco Problem
The options for dealing with photorespiration are limited in plants em-
ploying only 3C photosynthesis. This can be demonstrated using Eq. ,1
which describes the relationship between Rubisco kinetic parameters and
the ratio of photorespiratory CO2 release to photosynthetic CO2 fixation
(Andrews and Lorimer, 1987; Sharkey, 1988).
Ph~176176 - 0"5v~ - 0.5 (1 (cid:141) O ) (1)
Photosynthesis cV
The term oV is the rate of RuBP oxygenation, cv is the rate ofRuBP carboxyla-
tion, S is the specificity of Rubisco for CO2 relative to 02, C is the CO2
concentration in the chloroplast stroma, and O is the 02 concentration in
the stroma. According to Eq. 1, photorespiration can be reduced by chang-
ing Rubisco properties to increase ,S increasing ,C or reducing .O There
has been an increase in S from less than 10 mol CO2 per mol 02 in primitive
bacteria to near 80 in ~C plants (Table I). In ~C plants, S shows at most
elbaT I Range of Rubisco Specificity for 2OC Relative to 02 from
Various Classes of Organisms b,a
Organism type Rubisco specificity factor
Photosynthetic bacteria (single subunit) 9 to 15
Cyanobacteria 40 to 60
Green algae 50 to 70
Ca plants 55 to 85
3C plants 75 to 85
a Values reported here summarize work from the early 1980s. Other groups
report specificity factors that are 20% higher, on average, because of different
assumptions concerning the pK for the 2OC to bicarbonate equilibrium (Andrews
and Lorimer, 1987).
b It has been reported that thermophilic red algae have specificity factors as
high as 238 (Uemura te al., 1997). Although this represents an improvement over
terrestrial plants, these algae have a very low Rubisco turnover rate, indicating the
range of Rubisco specificity in 3C plants may reflect a balance between photorespira-
tion potential and turnover capacity in the terrestrial environment.
Data from Pierce,J. (1988). Prospects for manipulating the substrate specificity
of ribulose bisphosphate carboxylase/oxygenase. Physiol. Plant 72, 690-698.