Abstract
C4 photosynthesis is an evolutionary solution to high rates of photorespiration and low kinetic efficiency of Rubisco in CO2-depleted atmospheres of recent geologic time. About 7500 plant species are C4, in contrast to 30 000 CAM and 250 000 C3 species. All C4 plants occur in approximately 90 genera from 18 angiosperm families. In all of these families, the C4 pathway evolved independently. In many, multiple independent origins have occurred, such that over 30 distinct evolutionary origins of the C4 pathway are recognized. Fossil and carbon isotope evidence show that the C4 syndrome is at least 12 to 15 million years old, although estimates based on molecular sequence comparisons indicate it is over 20 million years old. The evolutionary radiation of herbaceous angiosperms may have been required for C4 plant evolution. All C4 species occur in advanced angiosperm families that appeared in the fossil record in the past 70 million years. Most of these families diversified in terms of genera and species numbers between 20 to 40 million years ago, during a period of global cooling, atmospheric CO2 reduction and aridification. During the period of diversification, numerous traits arose in the C3 flora that enhanced their performance in arid environments and atmospheres of reduced CO2. Some of these traits may have predisposed certain taxa to develop the C4 pathway once atmospheric CO2 levels declined to a point where the ability to concentrate CO2 had a selective advantage. Leading traits in C3 plants that may have facilitated the initial transition to C4 photosynthesis include close vein spacing and an enlargement of the bundle sheath cell layer to form a Kranz-like anatomy. Ecological factors not directly connected with photosynthesis probably also played a role. For example, extensive ecological disturbance may have been needed to convert C3-dominated woodlands into open, high-light habitats where herbaceous C4 plants could succeed. Disturbances in the form of fire, and browsing by large mammals, increase during the time of C4 plant evolution and diversification. Fire increased because of the drying climate, while browsing increased with the evolutionary diversification of the mammalian megafauna in the Oligocene and Miocene epochs. In summary, the origin of C4 plants is hypothesized to have resulted from a novel combination of environmental and phylogenetic developments that, for the first time, established the preconditions required for C4 plant evolution.
Abbreviations
Rubisco: Ribulose-1,5-bisphosphate carboxylase/oxygenase
Key words
Plant evolution - C3
- C4
- CAM - photosynthesis
References
-
01
Belsky, A. J.,, Amundson, R. G.,, Duxbury, J. M.,, Riha, S. J.,, Ali, A. R.,, and Mwonga, S. M..
(1989);
The effects of trees on their physical, chemical, and biological environments in a semi-arid savanna in Kenya.
J. Appl. Ecol..
26
1005-1024
-
02
Berner, R. A..
(1994);
3Geocarb II: a revised model of atmospheric CO2 over Phanerozoic time.
Amer. J. Sci..
291
339-376
-
03
Bird, M. I.,, Haberle, S. G.,, and Chivas, A. R..
(1994);
Effect of altitude on the carbon-isotope composition of forest and grassland soils from Papua New Guinea.
Global Biogeochem. Cycles.
8
13-22
-
04
Black, C. C..
(1973);
Photosynthetic carbon fixation in relation to net CO2 uptake.
Annu. Rev. Plant Physiol..
24
253-286
-
05
Bond, W. J..
(2000);
A proposed CO2-controlled mechanism of woody plant invasion in grasslands and savannas.
Global Change Biol..
6
865-869
-
06 Bond, W. J., and Wilgen, B. W.. (1996) Fire and Plants. London; Chapman & Hall
-
07
Bray, J. R..
(1958);
The distribution of savanna species in relation to light intensity.
Can. J. Bot..
36
671-681
-
08 Brown, R. H.. (1999) Agronomic implications of C4 photosynthesis. C4 Plant Biology. Sage, R. F. and Monson, R. K., eds. San Diego; Academic Press pp. 473-507
-
09
Brown, W. V..
(1977);
The Kranz syndrome and its subtypes in grass systematics.
Mem. Torrey Bot. Club.
23
1-97
-
10
Brown, J. R., and Archer, S..
(1989);
Woody plant invasion of grasslands: establishment of honey mesquite (Prosopis glandulosa var. glandulosa) on sites differing in herbaceous biomass and grazing history.
Oecologia.
80
19-26
-
11 Carter, P. J.,, Fewson, C. A.,, Nimmo, G. A.,, Nimmo, H. G.,, and Wilkins, M. B.. (1996) Roles of circadian rhythms, light and temperature in the regulation of phosophenolpyruvate carboxylase in Crassulacean Acid Metabolism. Crassulacean Acid Metabolism, Biochemistry, Ecophysiology and Evolution. Winter, K. and Smith, J. A. C., eds. Berlin; Springer-Verlag pp. 46-52
-
12 Cerling, T. E.. (1999) Paleorecords of C4 plants and ecosystems. C4 Plant Biology. Sage, R. F. and Monson R. K., eds. San Diego; Academic Press pp. 445-469
-
13
Cerling, T. E.,, Harris, J. M.,, MacFadden, B. J.,, Leacey, M. G.,, Quade, J.,, Eisenmann, V.,, and Ehleringer, J. R..
(1997);
Global vegetation change through the Miocene/Pliocene boundary.
Nature.
389
153-158
-
14
Cochrane, M. A., and Schulze, M. D..
(1999);
Fire as a recurrent event in tropical forests of the eastern Amazon: effects on forest structure, biomass, and species composition.
Biotropica.
31
2-16
-
15
Cockburn, W..
(1983);
Stomatal mechanism as the basis of the evolution of CAM and C4 photosynthesis.
Plant, Cell Environ..
6
275-279
-
16
Collatz, G. J.,, Berry, J. A.,, and Clark, J. S..
(1998);
Effects of climate and atmospheric CO2 partial pressure on the global distribution of C4 grasses: present, past and future.
Oecologia.
114
441-454
-
17 Collinson, M. E.,, Boulter, M. C.,, and Holmes, P. L.. (1993) Magnoliophyta (“Angiospermae”). “The Fossil Record 2”. Benton, M. J., ed. London; Chapman and Hall pp. 809-841
-
18 Dengler, N. G., and Nelson, T.. (1999) Leaf structure and development in C4 plants. C4 Plant Biology. Sage, R. F. and Monson, R. K., eds. San Diego; Academic Press pp. 133-172
-
19
Dengler, N. G.,, Dengler, R. E.,, and Hattersley, P. W..
(1985);
Differing ontogenetic origins of PCR (“Kranz”) sheaths in leaf blades of C4 plants.
Amer. J. Bot..
72
284-302
-
20
Dugas, M. J., and Retallack, G. J..
(1993);
Middle Miocene fossil grasses from Fort Ternan, Kenya.
J. Paleon..
67
113-128
-
21 Dublin, H.. (1995) Vegetation dynamics in the Serengeti-Mara ecosystem: the role of elephants, fire and other factors. Serengeti II: Dynamics, Management and Conservation of an Ecosystem. Sinclair, A. R. E. and Arcese, P., eds. Chicago; Chicago Univ. Press pp. 71-90
-
22 Edwards, G. E., and Walker, D. A.. (1983) C3, C4: Mechanism, and Cellular and Environmental Regulation, of Photosynthesis. Oxford; Blackwell Scientific Publications
-
23
Ehleringer, J. R., and Pearcy, R. W..
(1983);
Variation in quantum yield for CO2 uptake among C3 and C4 plants.
Plant Physiol..
73
555-559
-
24
Ehleringer, J. R.,, Cerling, T. E.,, and Helliker, B. R..
(1997);
C4 photosynthesis, atmospheric CO2 and climate.
Oecologia.
112
285-299
-
25
Ehleringer, J. R.,, Sage, R. F.,, Flanagan, L. B.,, and Pearcy, R. W..
(1991);
Climate change and the evolution of C4 photosynthesis.
Trends Ecol. Evol..
6
95-99
-
26 Frohlich, M. W.. (1978) Systematics of Heliotropium section Orthistachys in Mexico. Cambridge, Mass.; Ph.D. Thesis. Harvard University
-
27
Gaut, B. S., and Doebley, J. F..
(1997);
DNA sequence evidence for the segmental allotetraploid origin of maize.
Proc. Nat. Acad. Sci. U.S.A.
94
6809-6814
-
28
Gillon, J., and Yakir, D..
(2001);
Influence of carbonic anhydrase activity in terrestrial vegetation on the 18O content of atmospheric CO2.
Science.
291
2584-2587
-
29 Goldammer, J. G.. (1993) Historical biogeography of fire: tropical and subtropical. The Ecological, Atmospheric, and Climatic Importance of Vegetation Fire. Crutzen, P. J. and Goldammer, J. G., eds. New York; John Wiley and Sons pp. 297-314
-
30 Goldstein, G., and Sarmiento, G.. (1987) Water relations of trees and grasses and their consequences for the structure of savanna vegetation. Determinations of Tropical Savannas. Walker, B. H., ed. Oxford; IRL Press pp. 13-38
-
31
Hatch, M. D..
(1987);
C4 photosynthesis: a unique blend of modified biochemistry, anatomy and ultrastructure.
Biochim. Biophys. Acta.
895
81-106
-
32 Hopkins, B.. (1983) Successional processes. Ecosystems of the World 13: Tropical Savannas. Bourliere, F., ed. Amsterdam; Elsevier pp. 605-616
-
33 Janis, C.. (1993) Victors by default: the mammalian succession. The Book of Life. Gould, S. J., ed. New York; Viking Publ. pp. 169-217
-
34
Johnson, H. B.,, Polley, H. W.,, and Mayeux, H. S..
(1993);
Increasing CO2 and plant-plant interactions: effects on natural vegetation.
Vegetatio.
104/105
157-170
-
35 Jones, M. B.. (1986) Wetlands. Photosynthesis in Contrasting Environments. Baker, N. R. and Long, S. P., eds. London; Elsevier pp. 103-138
-
36
Jordan, D. B., and Ogren, W. L..
(1984);
The CO2/O2 specificity of ribulose 1,5-bisphosphate carboxylase/oxygenase.
Planta.
161
308-313
-
37 Judd, W. S.,, Campbell, C. S.,, Kellogg, E. A.,, and Stevens, P. F.. (1999) Plant systematics: a phylogenetic approach. Sunderland, Massachusetts; Sinauer Assoc. Inc.
-
38 Junk, W. J.. (1983) Ecology of swamps on the middle Amazon. Ecosystems of the World 4 B: MIRES: Swamp, Bog, Fen and Moor. Gore, A. J. P., ed. Amsterdam; Elsevier pp. 269-294
-
39 Kanai, R., and Edwards, G. E.. (1999) The biochemistry of C4 photosynthesis. C4 Plant Biology. Sage, R. F. and Monson, R. K., eds. San Diego; Academic Press pp. 49-87
-
40 Kellogg, E. A.. (1999) Phylogenetic aspects of the evolution of C4 photosynthesis. C4 Plant Biology. Sage, R. F. and Monson, R. K., eds. San Diego; Academic Press pp. 411-444
-
41
Koch, K., and Kennedy, R. A..
(1980);
Characteristics of Crassulacean acid metabolism in the succulent C4 dicot, Portulaca oleracea L.
Plant Phsyiol..
65
193-197
-
42 Leegood, R. C., and Walker, R. P.. (1999) Regulation of the C4 pathway. C4 Plant Biology. Sage, R. F. and Monson, R. K., eds. San Diego; Academic Press pp. 89-131
-
43 Long, S. P.. (1999) Environmental responses. C4 Plant Biology. Sage, R. F. and Monson, R. K., eds. San Diego; Academic Press pp. 215-249
-
44
MacFadden, B. J..
(1997);
Origin and evolution of grazing guild in new world terrestrial mammals.
Trends Ecol. Evol..
12
182-187
-
45 Metcalfe, C. R., and Chalk, L.. (1979) Anatomy of the dicotyledons. Vol. 1. Systematic Anatomy of the leaf and stem. Oxford; Oxford Science Publ. pp. 276
-
46 Monson, R. K.. (1999) The origins of C4 genes and evolutionary pattern in the C4 metabolic phenotype. C4 Plant Biology. Sage, R. F.and Monson, R. K., eds. San Diego; Academic Press pp. 377-410
-
47 Monson, R. K., and Rawsthorne, S.. (2000) CO2 assimilation in C3-C4 intermediate plants. Photosynthesis: Physiology and Metabolism. Leegood, R. C., Sharkey, T. D., and von Caemmerer, S. C., eds. Dordrecht; Kluwer Academic Publ. pp. 533-550
-
48
Muller, J..
(1981);
Fossil pollen records of extant angiosperms.
Bot. Rev..
47
1-146
-
49 Osmond, C. B.,, Winter, K.,, and Ziegler, H.. (1982) Functional significance of different pathways of CO2 fixation in photosynthesis. Encyclopedia of Plant Physiology, New Series Vol. 12 B. Physiological Plant Ecology II. Water Relations and Carbon Assimilation. Lange, O. L., Nobel, P. S., Osmond, C. B., and Ziegler, H., eds. Berlin; Springer-Verlag pp. 479-547
-
50
Owen-Smith, N..
(1989);
Megafaunal extinctions: the conservation message from 11 000 years ago.
Conserv. Biol..
3
405-412
-
51 Patterson, D. T., and Flint, E. P.. (1990) Implications of increasing carbon dioxide and climate change for plant communities and competition in natural and managed ecosystems. Impact of Carbon Dioxide, Trace Gases, and Climate Change on Global Agriculture. Special publication 53. Madison, WI; Amer. Soc. Agron. pp. 83-109
-
52
Pearcy, R. W., and Calkin, H. W..
(1983);
Carbon dioxide exchange of C3 and C4 tree species in the understory of a Hawaiian forest.
Oecologia.
58
26-32
-
53
Pearcy, R. W., and Ehleringer, J..
(1984);
Comparative ecophysiology of C3 and C4 plants.
Plant Cell Environ..
7
1-13
-
54
Pittermann, J., and Sage, R. F..
(2000);
Photosynthetic performance at low temperature of Bouteloua gracilis Lag., a high altitude C4 grass from the Rocky Mountains, USA.
Plant Cell Environ..
23
811-823
-
55
Pearson, P. N., and Palmer, M. R..
(2000);
Atmospheric carbon dioxide concentrations over the past 60 million years.
Science.
406
695-699
-
56 Prothero, D. R.. (1994) The Eocene-Oligocene transition: paradise lost. New York; Columbia University Press
-
57
Pyankov, V. I.,, Black, C. C. Jr.,, Artyusheva, E. G.,, Voznesenskaya, E. V.,, Ku, M. S. B.,, and Edwards, G. E..
(1999);
Features of photosynthesis in Haloxylon species of Chenopodiaceae that are dominant plants in central Asian deserts.
Plant Cell Physiol..
40
125-134
-
58
Robichaux, R. H., and Pearcy, R. W..
(1980);
Photosynthetic responses of C3 and C4 species from cool shaded habitats in Hawaii.
Oecologia.
47
106-109
-
59 Roth, I.. (1992) Leaf Structure: Coastal vegetation and mangroves of Venezuela. Encycl. Plant Anatomy. Vol. 14, part 2. Berlin; G. Borntraeger. Publ.
-
60 Roth, I.. (1996) Microscopic venation patterns of leaves and their importance in the distinction of (tropical) species. Encycl. Plant Anatomy. Vol. 17. Part 4. Berlin; G. Borntraeger. Publ.
-
61
Sage, R. F..
(1994);
Acclimation of photosynthesis to increasing atmospheric CO2: the gas exchange perspectives.
Photosyn. Res..
39
351-368
-
62
Sage, R. F..
(1995);
Was low atmospheric CO2 during the Pleistocene a limiting factor for the origin of agriculture?.
Global Change Biology.
1
93-106
-
63 Sage, R. F.. (1999) Why C4 Plants?. C4 Plant Biology. Sage, R. F. and Monson, R. K., eds. San Diego; Academic Press pp. 3-16
-
64
Sage, R. F..
(2001);
C4 Plants.
Encyclopedia of Biodiversity.
1
575-598
-
65
Sage, R. F., and Pearcy, R. W..
(1987);
The nitrogen use efficiency of C3 and C4 plants. II. Leaf nitrogen effects on the gas exchange characteristics of Chenopodium album L. and Amaranthus retroflexus L.
Plant Physiol..
84
959-963
-
66 Sage, R. F., and Pearcy, R. W.. (2000) The physiological ecology of C4 photosynthesis. Photosynthesis: Physiology and Metabolism. Leegood, R. C., Sharkey, T. D., and von Caemmerer, S., eds. Dordrecht; Kluwer Academic pp. 497-532
-
67
Sage, R. F., and Seemann, J. R..
(1990);
Humidity acclimation in C3 plants.
Bull. Ecol. Soc. Amer..
71
311
-
68 Sage, R. F.,, Li, M.-R.,, and Monson, R. K.. (1999 a) The taxonomic distribution of C4 photosynthesis. C4 Plant Biology. Sage, R. F. and Monson, R. K., eds. San Diego; Academic Press pp. 551-584
-
69 Sage, R. F.,, Wedin, D. A.,, and Li, M.-R.. (1999 b) The biogeography of C4 photosynthesis: patterns and controlling factors. C4 Plant Biology. Sage, R. F. and Monson, R. K., eds. San Diego; Academic Press pp. 313-373
-
70
Shields, L. M..
(1950);
Leaf xeromorphy as related to physiological and structural influences.
Bot. Rev..
16
299-440
-
71
Shields, L. M..
(1951);
The involution mechanism in leaves of certain xeric grasses.
Phytomorphology.
1
225-241
-
72
Shoshani, J..
(1998);
Understanding proboscidean evolution: a formidable task.
Trends Ecol. Evol..
13
480-487
-
73 Sinclair, A. R. E.. (1995) Equilibria in plant-herbivore interactions. Serengeti II: Dynamics, Management and Conservation of an Ecosystem. Arcese, P. and Sinclair, A. R. E., eds. Chicago; University of Chicago press pp. 91-113
-
74 Soares, R. V.. (1990) Fire in some tropical and subtropical South American vegetation types: An overview. Fire in the Tropical Biota - Ecosystem Processes and Global Challenges. Goldammer, J. G., ed. Berlin; Springer-Verlag pp. 63-81
-
75
Scholes, R. J., and Archer, S. R..
(1997);
Tree-grass interactions in savannas.
Annu. Rev. Ecol. Syst..
28
517-544
-
76 Smith, J. A. C.,, Ingram, J.,, Tsiantis, M. S,, Barkla, B. J.,, Bartholomew, D. M.,, Bettey, M.,, Pantoja, O.,, and Pennington, A. J.. (1996) Transport across the vacoular membrane in CAM plants. Crassulacean Acid Metabolism, Biochemistry, Ecophysiology and Evolution. Winter, K. and Smith, J. A. C., eds. Berlin; Springer-Verlag pp. 53-71
-
77
Tieszen, L. L.,, Senyimba, M. M.,, Imbamba, S. K.,, and Troughton, J. H..
(1979);
The distribution of C3 and C4 grasses and carbon isotope discrimination along an altitudinal and moisture gradient in Kenya.
Oecologia.
37
337-350
-
78
Tieszen, L. L.,, Reed, B. C.,, Bliss, N. B.,, Wylie, B. K.,, and DeJong, D. D..
(1997);
NDVI, C3 and C4 production, and distributions in Great Plains grassland land cover classes.
Ecol. Appl..
7
59-78
-
79
Tissue, D. T.,, Griffen, K. L.,, Thomas, R. B.,, and Strain, B. R..
(1995);
Effects of low and elevated CO2 on C3 and C4 annuals. II. Photosynthesis and leaf biochemistry.
Oecologia.
101
21-28
-
80
Tschudy, R. H.,, Pillmore, C. L.,, Orth, C. J.,, Gilmore, J. S.,, and Knight, J. D..
(1984);
Disruption of the terrestrial plant ecosystem at the Cretaceous-Tertiary boundary, Western Interior.
Science.
225
1030-1032
-
81 Von Caemmerer, S., and Furbank, R. T.. (1982) Modeling C4 Photosynthesis. C4 Plant Biology. Sage, R. F. and Monson, R. K., eds. San Diego; Academic Press pp. 173-211
-
82 Walter, H.,, Harnickell, E.,, and Mueller-Dombois, D.. (1975) Climate-Diagram Maps of the Individual Continents and the Ecological Climatic Regions of the Earth - Supplement to the Vegetation Monographs. Berlin; Springer-Verlag
-
83
Welkie, G. W., and Caldwell, M. M..
(1970);
Leaf anatomy of species in some dicotyledon families as related to the C3 and C4 pathways of carbon fixation.
Can. J. Bot..
48
2135-2146
-
84
Westhoff, P. D.,, Svensson, P.,, Ernst, K.,, Blasing, O.,, Burscheidt, J.,, and Stockhaus, J..
(1997);
Molecular evolution of C4 phosphoenolpyruvate carboxylase in the genus Flaveria.
.
Aust. J. Plant Physiol..
24
429-436
-
85
Wolfe, J. A..
(1990);
Palaeobotanical evidence for a marked temperature increase following the Cretaceous/Tertiary boundary.
Nature.
343
153-156
-
86 Wolfe, J. A.. (1997) Relations of environmental change to angiosperm evolution during the late Cretaceous and Tertiary. Evolution and Diversification of Land Plants. Iwatsuki, K. and Raven, P. H., eds. Tokyo; Springer-Verlag pp. 269-290
R. F. Sage
Department of Botany
University of Toronto
25 Willcocks Street
Toronto, On M5S3B2
Canada
eMail: Rsage@botany.utoronto.ca
Section Editor: U. Lüttge
