Evolution of leaf anatomy and photosynthetic pathways in Portulacaceae

American Journal of Botany

Volumn 100, Issue 12, 2013, Pages 2388-2402

  Ocampo, Gilberto ^a,e   Koteyeva, Nuria K ^b   Voznesenskaya, Elena V ^b   Edwards, Gerald E ^c   Sage, Tammy L ^d   Sage, Rowan F ^d   Travis Columbus, J ^a  

^a RANCHO SANTA ANA BOTANIC GARDEN   (United States)

^b KOMAROV BOTANICAL INSTITUTE   (Russian Federation)

^c WASHINGTON STATE UNIVERSITY   (United States)

^d UNIVERSITY OF TORONTO   (Canada)

^e CALIFORNIA ACADEMY OF SCIENCES   (United States)

Author keywords

C3 C4 Intermediacy; C4 Photosynthesis; Cactineae; Kranz anatomy; Leaf anatomy; Portulaca; Portulacaceae; Portulacineae

Indexed keywords

ANATOMY; ANCESTRY; C4 PLANT; CARBON ISOTOPE; CLADISTICS; DIVERGENCE; EVOLUTIONARY BIOLOGY; PHOTOSYNTHESIS; PHYLOGENY; PHYTOCHEMISTRY;

CARBON; MALIC ACID; MALIC ACID DERIVATIVE; NICOTINAMIDE ADENINE DINUCLEOTIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE;

ARTICLE; BAYES THEOREM; C3-C4 INTERMEDIACY; C4 PHOTOSYNTHESIS; CACTINEAE; CARBON CYCLE; EVOLUTION; GENETICS; HISTOLOGY; KRANZ ANATOMY; LEAF MORPHOLOGY; METABOLISM; PHOTOSYNTHESIS; PHYLOGENY; PHYSIOLOGY; PLANT LEAF; PORTULACA; PORTULACACEAE; PORTULACINEAE;

C3-C4 INTERMEDIACY; C4 PHOTOSYNTHESIS; CACTINEAE; KRANZ ANATOMY; LEAF ANATOMY; PORTULACA; PORTULACACEAE; PORTULACINEAE;

BAYES THEOREM; BIOLOGICAL EVOLUTION; CARBON; CARBON CYCLE; CARBON ISOTOPES; MALATES; NAD; NADP; PHOTOSYNTHESIS; PHYLOGENY; PLANT LEAVES; PORTULACACEAE;

EID: 84890051589     PISSN: 00029122     EISSN: None     Source Type: Journal    
DOI: 10.3732/ajb.1300094     Document Type: Article

References (86)

1. AKAIKE, H. 1974. A new look at the statistical model identification. IEEE Transactions on Automatic Control 19: 716-723.
2. ARAKAKI, M., P. A. CHRISTIN, R. NYFFELER, A. LENDEL, U. EGGLI, R. M. OGBURN, E. SPRIGGS, M. J. MOORE, and E. J. EDWARDS. 2011. Contemporaneous and recent radiations of the world's major succulent plant lineages. Proceedings of the National Academy of Sciences, USA 108: 8379-8384.
3. 12C ratio changes in Crassulacean acid metabolism plants. Plant Physiology 52: 427-430.
4. BESNARD, G., A. M.M UASYA, F. RUSSIER, E. H. ROALSON, N. SALAMIN, and P. A. CHRISTIN. 2009. Phylogenomics of C4 photosynthesis in sedges (Cyperaceae): Multiple appearances and genetic convergence. Molecular Biology and Evolution 26: 1909-1919.
5. BOLLBACK, J. P. 2006. Simmap: Stochastic character mapping of discrete traits on phylogenies. BMC Bioinformatics 7: 88.
6. BOLLBACK, J. P. 2009. Simmap version 1.5. [computer program]. Website http://www.simmap.com/pgs/docs.html [accessed 30 April 2012].
7. Bouchenak-Khelladi, Y., G. A. VERBOOM, T. R.H ODKINSON, N. SALAMIN, O. FRANCOIS, G. N.C HONGHAILE, and V.S AVOLAINEN. 2009. The origins and diversification of C4 grasses and savanna-adapted ungulates. Global Change Biology 15: 2397-2417.
8. BRAÜTIGAM, A., S. Hoffmann-Benning, and A. P. M. WEBER. 2008. Comparative proteomics of chloroplast envelopes from C3 and C4 plants reveals specific adaptations of the plastid envelope to C4 photosynthesis and candidate proteins required for mantaining C4 metabolite fluxes. Plant Physiology 148: 568-579.
9. BRITTON, T., C. L. ANDERSON, D. JAQUET, S. LUNDQVIST, and K. BREMER. 2007. Estimating divergence times in large phylogenetic trees. Systematic Biology 56: 741-752.
10. BROWN, H. R., and P. W. HATTERSLEY. 1989. Leaf anatomy of C3-C4 species as related to evolution of C4 photosynthesis. Plant Physiology 91: 1543-1550.
11. CAROLIN, R. C., S. W. L. JACOBS, and M. VESK. 1978. Kranz cells and mesophyll in the Chenopodiales. Australian Journal of Botany 26: 683-698.
12. CHRISTIN, P. A., R. P. FRECKLETON, and C. P. OSBORNE. 2010. Can phylogenetics identify C4 origins and reversals? Trends in Ecology & Evolution 25: 403-409.
13. CHRISTIN, P. A., C. P. OSBORNE, R. F. SAGE, M. ARAKAKI, and E. J. EDWARDS. 2011a. C4 eudicots are not younger than C4 monocots. Journal of Experimental Botany 62: 3171-3181.
14. CHRISTIN, P. A., T. L. SAGE, E. J. EDWARDS, R. M. OGBURN, R. KHOSHRAVESH, and R. F. SAGE. 2011b. Complex evolutionary transitions and the significance of C3-C4 intermediate forms of photosynthesis in Molluginaceae. Evolution; International Journal of Organic Evolution 65: 643-660.
15. COELHO, A. A. O. P., and A. M.G IULIETTI. 2010. O gênero Portulaca L. (Portulacaceae) no Brasil. Acta Botânica Brasilica 24: 655-670.
16. DENGLER, N. G., and T. NELSON. 1999. Leaf structure and development in C4 plants. In R. F. Sage & R. K. Monson [eds.], C4 plant biology, 133-172. Academic Press, San Diego, California, USA.
17. EDGAR, R. C. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32: 1792-1797.
18. EDWARDS, E. J., R. NYFFELER, and M. J. DONOGHUE. 2005. Basal cactus phylogeny: Implications of Pereskia (Cactaceae) paraphyly for the transition to the cactus life form. American Journal of Botany 92: 1177-1188.
19. EDWARDS, G. E., and M. S. B. KU. 1987. The biochemistry of C3-C4 intermediates. In M. D. Hatch and N. K. Boardman [eds.], The biochemistry of plants, vol. 10, Photosynthesis, 275-325. Academic Press, New York, New York, USA.
20. EDWARDS, G. E., and E. V. VOZNESENSKAYA. 2011. C4 photosynthesis: Kranz forms and single-cell C4 in terrestrial plants. In A. S. Raghavendra and R. F. Sage [eds.], C4 photosynthesis and related CO2 concentrating mechanisms, 29-61. Springer, Dordrecht, The Netherlands.
21. EDWARDS, G. E., and D. A. WALKER. 1983. C3, C4: mechanisms, and cellular regulation, of photosynthesis. Blackwell Scientific, Oxford, UK.
22. EHLERINGER, J. R., T. E. CERLING, and B. R. HELLIKER. 1997. C4 photosynthesis, atmospheric CO2, and climate. Oecologia 112: 285-299.
23. EHLERINGER, J. R., and R. K. MONSON. 1993. Evolutionary and ecological aspects of photosynthetic pathway variation. Annual Review of Ecology and Systematics 24: 411-439.
24. FELSENSTEIN, J. 1973. Maximum likelihood and minimum-steps methods for estimating evolutionary trees from data on discrete characters. Systematic Zoology 22: 240-249.
25. FELSENSTEIN, J. 1985. Confidence limits on phylogenies: An approach using the bootstrap. Evolution; International Journal of Organic Evolution 39: 783-791.
26. FURBANK, R. T. 2011. Evolution of the C4 photosynthetic mechanism: Are there really three C4 acid decarboxylation types? Journal of Experimental Botany 62: 3103-3108.
27. GURALNICK, L. J., A. CLINE, M. SMITH, and R. F. SAGE. 2008. Evolutionary physiology: the extent of C4 and CAM photosynthesis in the genera Anacampseros and Grahamia of the Portulacaceae. Journal of Experimental Botany 59: 1735-1742.
28. GURALNICK, L. J., G. E. EDWARDS, M. S. B. KU, B. HOCKEMA, and V. FRANCESCHI. 2002. Photosynthetic and anatomical characteristics in the C4-Crassulacean acid metabolism-cycling plant Portulaca grandiflora. Functional Plant Biology 29: 763-773.
29. GURALNICK, L. J., and M. D. JACKSON. 2001. The occurrence and phylogenetics of crassulacean acid metabolism in the Portulacaceae. International Journal of Plant Sciences 162: 257-262.
30. GUTIÉRREZ, M., V. E. GRACEN, and G. E. EDWARDS. 1974. Biochemical and cytological relationships in C4 plants. Planta 119: 279-300.
31. HATCH, M. D. 1987. C4 photosynthesis, a unique blend of modified biochemistry, anatomy, and ultrastructure. Biochimica et Biophysica Acta 895: 81-106.
32. KADEREIT, G., D. ACKERLY, and M. D. PIRIE. 2012. A broader model for C4 photosynthesis evolution in plants inferred from the goosefoot family (Chenopodiaceae s.s.). Proceedings of the Royal Society of London. Series B, Biological Sciences 279: 3304-3311.
33. KADEREIT, G., T. BORSCH, K. WEISING, and H. FREITAG. 2003. Phylogeny of Amaranthaceae and Chenopodiaceae and the evolution of C4 photosynthesis. International Journal of Plant Sciences 164: 959-986.
34. KANAI, R., and G. E. EDWARDS. 1999. The biochemistry of C4 photosynthesis. In R. F. Sage and R. K. Monson [eds.], C4 plant biology, 49-87. Academic Press, San Diego, California, USA.
35. KENNEDY, R. A., and W. M. LAETSCH. 1974. Plant species intermediate for C3, C4 photosynthesis. Science 184: 1087-1089.
36. KIM, I. 1993. Biosystematics of Portulaca species in northeast Asia. Korean Journal of Plant Taxonomy 23: 71-96.
37. KIM, I., and D. G. FISHER. 1990. Structural aspects of the leaves of seven species of Portulaca growing in Hawaii. Canadian Journal of Botany 68: 1803-1811.
38. KU, M. S. B., R. K. MONSON, R. O. LITTLEJOHN Jr., H. NAKAMOTO, D. B. FISHER, and G. E. EDWARDS. 1983. Photosynthetic characteristics of C3-C4 intermediate Flaveria species. Plant Physiology 71: 944-948.
39. KU, M. S. B., Y. J. SHIEH, B. J. REGER, and C. C. BLACK. 1981. Photosynthetic characteristics of Portulaca grandiflora, a succulent C4 dicot. Plant Physiology 68: 1073-1080.
40. LANDRUM, J. V. 2002. Four succulent families and 40 million years of evolution and adaptation to xeric environments: what can stem and leaf anatomical characters tell us about their phylogeny? Taxon 51: 463-473.
41. LEGRAND, D. 1953. Desmembración del género Portulaca. Comunicaciones Botánicas del Museo de Historia Natural de Montevideo 31: 1-14.
42. LEGRAND, D. 1962. Las especies americanas de Portulaca. Anales del Museo de Historia Natural de Montevideo, Ser. 2 7: 1-147.
43. LI, S., D. K. PEARL, and H. DOSS. 2000. Phylogenetic tree construction using Markov chain Monte Carlo. Journal of the American Statistical Association 95: 493-508.
44. LIN, C., J. HSUE, and J. TSAY. 1982. The anatomy of the noxious weeds on cultivated land of Taiwan. Proceedings of the National Science Council, Republic of China. Part B, Life Sciences 6: 452-460.
45. MATTHEWS, J. F. 2003. Portulaca. In Flora of North America Editorial Committee [eds.], Flora of North America, vol. 4, 496-501. Oxford University Press, New York, USA.
46. MCKOWN, A. D., and N. G. DENGLER. 2007. Key innovations in the evolution of Kranz anatomy and C4 vein pattern in Flaveria (Asteraceae). American Journal of Botany 94: 382-399.
47. MONSON, R. K. 1999. The origins of C4 genes and evolutionary pattern in the C4 metabolic phenotype. In R.F. Sage and R.K. Monson [eds.], C4 Plant Biology, 377-410. Academic Press. San Diego, California, USA.
48. MONSON, R. K., G. E. EDWARDS, and M. S. B. KU. 1984. C3-C4 intermediate photosynthesis in plants. Bioscience 34: 563-574.
49. MONSON, R. K., and B. D. MOORE. 1989. On the significance of C3-C4 intermediate photosynthesis to the evolution of C4 photosynthesis. Plant, Cell & Environment 12: 689-699.
50. MONSON, R. K., and S. RAWSTHORNE. 2000. CO2 assimilation in C3-C4 intermediate plants. In R. C. Leegod, T. D. Sharkey, and S. C. von Caemmerer [eds.], Photosynthesis: physiology and metabolism, 553-550. Kluwer, Dordrecht, Netherlands.
51. MUHAIDAT, R., R. F. SAGE, and N. G. DENGLER. 2007. Diversity of Kranz anatomy and biochemistry in C4 eudicots. American Journal of Botany 94: 362-381.
52. MUHAIDAT, R., T. L. SAGE, M. W. FROHLICH, N. G. DENGLER, and R. F. SAGE. 2011. Characterizarion of C3-C4 intermediate species in the genus Heliotropium L. (Boraginaceae): Anatomy, ultrastructure and enzyme activity. Plant, Cell & Environment 34: 1723-1736.
53. NYANANYO, B. L. 1988. Leaf anatomical studies in the Portulacaceae (Centrospermae) with regards to photosynthetic pathways. Folia Geobotanica et Phytotaxonomica 23: 99-101.
54. NYFFELER, R., and U. EGGLI. 2010. Disintegrating Portulacaceae: A new familial classification of the suborder Portulacineae (Caryophyllales) based on molecular and morphological data. Taxon 59: 227-240.
55. NYLANDER, J. A. A. 2004. MrModeltest, version 2 [computer program]. Website http://www.abc.se/~nylander/mrmodeltest2/mrmodeltest2 [accessed 30 April 2012].
56. OCAMPO, G., and J. T. COLUMBUS. 2010. Molecular phylogenetics of suborder Cactineae (Caryophyllales), including insights into photosynthetic diversification and historical biogeography. American Journal of Botany 97: 1827-1847.
57. OCAMPO, G., and J. T. COLUMBUS. 2012. Molecular phylogenetics, historical biogeography, and chromosome number evolution in Portulaca (Portulacaceae). Molecular Phylogenetics and Evolution 63: 97-112.
58. O'Leary, M. H. 1988. Carbon isotopes in photosynthesis. Bioscience 38: 328-336.
59. PRABHAKAR, M., and N. RAMAYYA. 1979. Anatomical studies in the Indian Portulacaceae. II. Leaf lamina. In Histochemistry, Developmental and Structural Anatomy of Angiosperms: a Symposium, 159-69. P & H Publications, Tiruchirapalli, India.
60. PYANKOV, V. I., E. G. ARTYUSHEVA, G. E. EDWARDS, C. C. BLACK Jr., and P. S. SOLTIS. 2001. Phylogenetic analysis of tribe Salsoleae (Chenopodiaceae) based on ribosomal ITS sequences: Implications for the evolution of photosynthesis types. American Journal of Botany 88: 1189-1198.
61. R DEVELOPMENT CORE TEAM. 2006. R: A language and environment for statistical computing [computer program]. Website www.R-project.org [accessed 30 April 2012].
62. RAJENDRUDU, G., J. S. R. PRASAD, and V. S.R AMA DAS. 1986. C3-C4 intermediate species in Alternanthera (Amaranthaceae). Plant Physiology 80: 409-414.
63. RAMBAUT, A. 2002. Se-Al. Sequence alignment editor [computer program]. Website http://tree.bio.ed.ac.uk/software/seal/ [accessed 21 March 2012].
64. RANNALA, B., and Z. H. YANG. 1996. Probability distribution of molecular evolutionary trees: A new method of phylogenetic inference. Journal of Molecular Evolution 43: 304-311.
65. RAVEN, J. A., C. S. COCKELL, and C. L. DE LA ROCHA. 2008. The evolution of inorganic carbon concentrating mechanisms in photosynthesis. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 363: 2641-2650.
66. RAWSTHORNE, S. 1992. C3-C4 intermediate photosynthesis: linking physiology to gene expression. The Plant Journal 2: 267-274.
67. REEVES, J. H. 1992. Heterogeneity in the substitution process of amino acid sites of proteins coded for by mitochondrial DNA. Journal of Molecular Evolution 35: 17-31.
68. RONQUIST, F., M. TESLENKO, P. VAN DER MARK, D. L. AYRES, A. DARLING, S. HÖHNA, B. LARGET, ET AL. 2012. MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61: 539-542.
69. RUZIN, S. E. 1999. Plant microtechnique and microscopy. Oxford University Press, New York, New York, USA.
70. SAGE, R. F. 2004. The evolution of C4 photosynthesis. The New Phytologist 161: 341-370.
71. SAGE, R. F., P. A. CHRISTIN, and E. J. EDWARDS. 2011. The C4 plant lineages of planet Earth. Journal of Experimental Botany 62: 3155-3169.
72. SAGE, R. F., T. L. SAGE, and F. KOCACINAR. 2012. Photorespiration and the evolution of C4 photosynthesis. Annual Review of Plant Biology 63: 19-47.
73. SAGE, R. F., T. L. SAGE, R. W. PEARCY, and T. BORSCH. 2007. The taxonomic distribution of C4 photosynthesis in Amaranthaceae sensu stricto. American Journal of Botany 94: 1992-2003.
74. STAMATAKIS, A. 2006. RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics (Oxford, England) 22: 2688-2690.
75. TAVARÉ, S. 1986. Some probabilistic and statistical problems on the analysis of DNA sequences. Lectures on Mathematics in the Life Sciences 17: 57-86.
76. THOLEN, D., C. BOOM, and X.-G. ZHU. 2012. Opinion: Prospects for improving photosynthesis by altering leaf anatomy. Plant Science 197: 92-101.
77. THORNE, R. F., and J. L. REVEAL. 2007. An updated classification of the class Magnoliopsida ("Angiospermae"). Botanical Review 73: 67-181.
78. VOZNESENSKAYA, E. V., E. G. ARTYUSHEVA, V. R. FRANCESCHI, V. I. PYANKOV, O. KIIRATS, M. S. B. KU, and G. E. EDWARDS. 2001. Salsola arbusculiformis, a C3-C4 intermediate in Salsoleae (Chenopodiaceae). Annals of Botany 88: 337-348.
79. VOZNESENSKAYA, E. V., N. K. KOTEYEVA, H. AKHANI, E. H. ROALSON, and G. E. EDWARDS. 2013. Structural and physiological analyses in Salsoleae (Chenopodiaceae) indicate multiple transitions among C3, intermediate and C4 photosynthesis. Journal of Experimental Botany 64: 3583-3604.
80. VOZNESENSKAYA, E. V., N. K. KOTEYEVA, G. E.E DWARDS, and G.O CAMPO. 2010. Revealing diversity in structural and biochemical forms of C4 photosynthesis and a C3-C4 intermediate in genus Portulaca L. (Portulacaceae). Journal of Experimental Botany 61: 3647-3662.
81. WELKIE, G. W., and M. CALDWELL. 1970. Leaf anatomy of species in some dicotyledon families as related to the C3 and C4 pathways of carbon fixation. Canadian Journal of Botany 48: 2135-2146.
82. WIENS, J. J. 2011. Re-evolution of lost mandibular teeth in frogs after more than 200 million years, and re-evaluating Dollo's law. Evolution; International Journal of Organic Evolution 65: 1283-1296.
83. WIENS, J. J., C. A. KUCZYNSKI, W. E. DUELLMAN, and T. W. REEDER. 2007. Loss and re-evolution of complex life cycles in marsupial frogs: Does ancestral trait reconstruction mislead? Evolution; International Journal of Organic Evolution 61: 1886-1899.
84. 13C values of Crassulacean acid metabolism plants reflect the proportion of CO2 fixed during day and night? Plant Physiology 129: 1843-1851.
85. YANG, Z. 1993. Maximum-likelihood estimation of phylogeny from DNA sequences when substitution rates differ over sites. Molecular Biology and Evolution 10: 1396-1401.
86. YANG, Z., and B. RANNALA. 1997. Bayesian phylogenetic inference using DNA sequences: a Markov Chain Monte Carlo Method. Molecular Biology and Evolution 14: 717-724.