Angiosperm responses to a low-CO2 world: CAM and C4 photosynthesis as Parallel evolutionary trajectories

International Journal of Plant Sciences

Volumn 173, Issue 6, 2012, Pages 724-733

  Edwards, Erika J ^a   Ogburn, R Matthew ^a  

^a BROWN UNIVERSITY   (United States)

Author keywords

Angiosperm evolution; C4; CAM; CO2; Photosynthesis

Indexed keywords

ADAPTATION; ANGIOSPERM; BIOCHEMICAL COMPOSITION; CARBON DIOXIDE; CONCENTRATION (COMPOSITION); METABOLISM; PHOTOSYNTHESIS; PHYLOGENETICS; PHYLOGENY;

CRASSULACEAE; MAGNOLIOPHYTA;

EID: 84863666188     PISSN: 10585893     EISSN: None     Source Type: Journal    
DOI: 10.1086/666098     Document Type: Article

References (69)

1. Applequist WL, RS Wallace 2001 Phylogeny of the portulacaceous cohort based on ndhF sequence data. Syst Bot 26:406-419.
2. Arakaki M, PA Christin, R Nyffeler, A Lendel, U Eggli, RM Ogburn, E Spriggs, MJ Moore, EJ Edwards 2011 Contemporaneous and recent radiations of the world's major succulent plant lineages. Proc Natl Acad Sci USA 108:8379-8384.
3. Aubry S, NJ Brown, JM Hibberd 2011 The role of proteins in C3 plants prior to their recruitment into the C4 pathway. J Exp Bot 62:3049-3059.
4. Beerling D, D Royer 2011 Convergent Cenozoic CO2 history. Nat Geosci 4:418-420.
5. Berner RA 1994 GEOCARB II: a revised model of atmospheric CO2 over Phanerozoic time. Am J Sci 294:56-91.
6. Borland AM, VA Barrera Zambrano, J Ceusters, K Shorrock 2011 The photosynthetic plasticity of crassulacean acid metabolism: an evolutionary innovation for sustainable productivity in a changing world. New Phytol 191:619-633.
7. Bowes G 2011 Single-cell C4 photosynthesis in aquatic plants. Pages 63-80 in A Raghavendra, R Sage, eds. C4 photosynthesis and related CO2 concentrating mechanisms. Springer, Dordrecht.
8. Brodribb T, T Feild, G Jordan 2007 Leaf maximum photosynthetic rate and venation are linked by hydraulics. Plant Physiol 144:1890-1898.
9. Bruyns PV, C Klak, P Hanacek 2011 Age and diversity in Old World succulent species of Euphorbia (Euphorbiaceae). Taxon 60:1717-1733.
10. Cerling TE, JM Harris, BJ MacFadden, MG Leakey, J Quade, V Eisenmann, JR Ehleringer 1997 Global change through the Mio-cene/Pliocene boundary. Nature 389:153-158.
11. Christin P, C Osborne, R Sage, M Arakaki, E Edwards 2011a C4 eudicots are not younger than C4 monocots. J Exp Bot 62:3171-3181.
12. Christin P, T Sage, E Edwards, R Ogburn, R Khoshravesh, R Sage 2011b Complex evolutionary transitions and the significance of C3-C4 intermediate forms of photosynthesis in Molluginaceae. Evolution 65:643-660.
13. Cockburn W 1985 Variation in photosynthetic acid metabolism in vascular plants: CAM and related phenomena. New Phytol 101: 3-24.
14. Cushman JC 2001 Crassulacean acid metabolism: a plastic photosynthetic adaptation to arid environments. Plant Physiol 127: 1439-1448.
15. Dodd AN, A Borland, R Haslam, H Griffiths, K Maxwell 2002 Crassulacean acid metabolism: plastic, fantastic. J Exp Bot 53:569-580.
16. Edwards EJ, M Diaz 2006 Ecological physiology of Pereskia guamacho, a cactus with leaves. Plant Cell Environ 29:247-256.
17. Edwards EJ, R Nyffeler, MJ Donoghue 2005 Basal cactus phylogeny: implications of Pereskia paraphyly for the transition to the cactus life form. Am J Bot 92:1177-1188.
18. Edwards EJ, CP Osborne, CAE Stromberg, SA Smith, C4 Grasses Consortium 2010 The origins of C4 grasslands: integrating evolutionary and ecosystem science. Science 328:587-591.
19. Ehleringer J, R Monson 1993 Evolutionary and ecological aspects of photosynthetic pathway variation. Annu Rev Ecol Syst 24:411-439.
20. Farquhar G, T Sharkey 1982 Stomatal conductance and photosynthesis. Annu Rev Plant Physiol 33:317-345.
21. Feild TS, TJ Brodribb, A Iglesias, DS Chatelet, A Baresch, GR Upchurch, B Gomez, et al 2011 Fossil evidence for Cretaceous escalation in angiosperm leaf vein evolution. Proc Natl Acad Sci USA 108:8363-8366.
22. Fritz SA, A Purvis 2010 Selectivity in mammalian extinction risk and threat types: a new measure of phylogenetic signal strength in binary traits. Conserv Biol 24:1042-1051.
23. Furbank RT, MD Hatch 1987 Mechanism of C4 photosynthesis: the size and composition of the inorganic carbon pool in bundle sheath cells. Plant Physiol 85:958-964.
24. Givnish T, K Millam, P Berry 2007 Phylogeny, adaptive radiation, and historical biogeography of Bromeliaceae inferred from ndhF sequence data. Aliso 23:3-26.
25. Good-Avila SV, V Souza, BS Gaut, LE Eguiarte 2006 Timing and rate of speciation in Agave (Agavaceae). Proc Natl Acad Sci USA 103: 9124-9129.
26. GPWG (Grass Phylogeny Working Group) II 2012 New grass phylogeny resolves deep evolutionary relationships and discovers C4 origins. New Phytol 193:304-312.
27. Guralnick LJ, A Cline, M Smith, RF Sage 2008 Evolutionary physiology: the extent of C4 and CAM photosynthesis in the genera Anacampseros and Grahamia of the Portulacaceae. J Exp Bot 59: 1735-1742.
28. Guralnick LJ, MD Jackson 2001 The occurrence and phylogenetics of crassulacean acid metabolism in the Portulacaceae. Int J Plant Sci 162:257-262.
29. Hershkovitz MA, EA Zimmer 1997 On the evolutionary origins of the cacti. Taxon 46:217-232.
30. Hijmans R, S Cameron, J Parra 2005 Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25:1965-1978.
31. Hunt S, AM Smith, HW Woolhouse 1987 Evidence for a lightdependent system for reassimilation of photorespiratory CO2, which does not include a C4 cycle, in the C3-C4 intermediate species Moricandia arvensis. Planta 171:227-234.
32. Huxman T, R Monson 2003 Stomatal responses of C3, C3-C4 and C4 Flaveria species to light and intercellular CO2 concentration: implications for the evolution of stomatal behaviour. Plant Cell Environ 26:313-322.
33. Keeley J 1998a C4 photosynthetic modifications in the evolutionary transition from land to water in aquatic grasses. Oecologia 116:85-97.
34. Keeley J 1998b CAM photosynthesis in submerged aquatic plants. Bot Rev 64:121-175.
35. Keeley J, P Rundel 2003 Evolution of CAM and C4 carbonconcentrating mechanisms. Int J Plant Sci 164(suppl):S55-S77.
36. Keeley JE 1990 Photosynthetic pathways in freshwater aquatic plants. Trends Ecol Evol 5:330-333.
37. Klak C, G Reeves, T Hedderson 2004 Unmatched tempo of evolution in southern African semi-desert ice plants. Nature 427: 63-65.
38. Martin C, M Higley 1988 Ecophysiological significance of CO2-recycling via crassulacean acid metabolism in Talinum calycinum Engelm. (Portulacaceae). Plant Physiol 86:562-568.
39. Miziorko H, G Lorimer 1983 Ribulose-1, 5-bisphosphate carboxylaseoxygenase. Annu Rev Biochem 52:507-535.
40. Monson R 1989 On the evolutionary pathways resulting in C4 photosynthesis and crassulacean acid metabolism (CAM). Adv Ecol Res 19:57-110.
41. Monson R, B Moore 1989 On the significance of C3-C4 intermediate photosynthesis to the evolution of C4 photosynthesis. Plant Cell Environ 12:689-699.
42. Monson R, S Rawsthorne 2000 CO2 assimilation in C3-C4 intermediate plants. Pages 533-550 in R Leegood, T Sharkey, S von Caemmerer, eds. Photosynthesis: physiology and metabolism. Kluwer Academic, Dordrecht.
43. Monson RK 1999 The origins of C4 genes and evolutionary pattern in the C4 metabolic phenotype. Pages 377-410 in RF Sage, RK Monson, eds. C4 plant biology. Academic Press, San Diego, CA.
44. Nyffeler R, U Eggli 2010 Disintegrating Portulacaceae: a new familial classification of the suborder Portulacineae (Caryophyllales) based on molecular and morphological data. Taxon 59: 227-240.
45. Nyffeler R, U Eggli, RM Ogburn, EJ Edwards 2008 Variations on a theme: repeated evolution of succulent life forms in the Portulacineae (Caryophyllales). Haseltonia 14:26-36.
46. Ogburn RM, EJ Edwards 2010 The ecological water-use strategies of succulent plants. Adv Bot Res 55:179-225.
47. Ogburn RM, EJ Edwards 2012 Quantifying succulence: a rapid, physiologically meaningful metric of plant water storage. Plant Cell Environ, doi:10.1111/j.1365-3040.2012.02503.x.
48. Pagani M, K Caldeira, R Berner, DJ Beerling 2009 The role of terrestrial plants in limiting atmospheric CO2 decline over the past 24 million years. Nature 460:85-88.
49. Raven JA, RA Spicer 1996 The evolution of crassulacean acid metabolism. Pages 360-385 in K Winter, JAC Smith, eds. Crassulacean acid metabolism: biochemistry, ecophysiology and evolution. Ecological Studies 114. Springer, Berlin.
50. Retallack G 1997 Earliest Triassic origin of Isoetes and quillwort evolutionary radiation. J Paleontol 71:500-521.
51. Royer D 2006 CO2-forced climate thresholds during the Phanerozoic. Geochim Cosmochim Acta 70:5665-5675.
52. Sage RF 2002 Are crassulacean acid metabolism and C4 photosynthesis incompatible? Funct Plant Biol 29:775-785.
53. Sage RF 2004 The evolution of C4 photosynthesis. New Phytol 161: 341-370.
54. Sage RF, PA Christin, EJ Edwards 2011 The C4 plant lineages of planet Earth. J Exp Bot 62:3155-3169.
55. Sayre R, R Kennedy 1977 Ecotypic differences in the C3 and C4 photosynthetic activity in Mollugo verticillata, a C3-C4 intermediate. Planta 134:257-262.
56. Sayre R, R Kennedy 1979 Photosynthetic enzyme activities and localization in Mollugo verticillata populations differing in the levels of C3 and C4 cycle operation. Plant Physiol 64:293-299.
57. Schneider H, E Schuettpelz, KM Pryer, R Cranfill, S Magallón, R Lupia 2004 Ferns diversified in the shadow of angiosperms. Nature 428:553-557.
58. Silvera K, KM Neubig, WM Whitten, NH Williams, K Winter, JC Cushman 2010 Evolution along the crassulacean acid metabolism continuum. Funct Plant Biol 37:995-1010.
59. Smith JAC, K Winter 1996 Taxonomic distribution of crassulacean acid metabolism. Pages 427-436 in JAC Smith, K Winter, eds. Crassulacean acid metabolism: biochemistry, ecophysiology and evolution. Springer, Berlin.
60. Smith SA, JM Beaulieu, MJ Donoghue 2009 Mega-phylogenies for comparative biology: an alternative to supertree and supermatrix approaches. BMC Evol Biol 9:37.
61. Steinmann V, J Porter 2002 Phylogenetic relationships in Euphorbieae (Euphorbiaceae) based on ITS and ndhF sequence data. Ann Mo Bot Gard 89:453-490.
62. Taylor T, E Taylor, M Krings 2009 Paleobotany: the biology and evolution of fossil plants. Academic Press, San Diego, CA.
63. Tripati AK, CD Roberts, RA Eagle 2009 Coupling of CO2 and ice sheet stability over major climate transitions of the last 20 million years. Science 326:1394-1397.
64. von Willert DJ, N Armbruster, T Drees, M Zaborowski 2005 Welwitschia mirabilis: CAM or not CAM-what is the answer? Funct Plant Biol 32:389.
65. Voznesenskaya EV, NK Koteyeva, GE Edwards, G Ocampo 2010 Revealing diversity in structural and biochemical forms of C4 photosynthesis and a C3-C4 intermediate in genus Portulaca L. (Portulacaceae). J Exp Bot 61:3647-3662.
66. West-Eberhard MJ, JAC Smith, K Winter 2011 Photosynthesis, reorganized. Science 332:311-312.
67. 13C values of crassulacean acid metabolism plants reflect the proportion of CO2 fixed during day and night? Plant Physiol 129:1843-1851.
68. Winter K, MJ Schramm 1986 Analysis of stomatal and nonstomatal components in the environmental control of CO2 exchange in leaves of Welwitschia mirabilis. Plant Physiol 82: 173-178.
69. Zachos J, M Pagani, L Sloan, E Thomas, K Billups 2001 Trends, rhythms, and aberrations in global climate 65 Ma to present. Science 292:686-693.