Shared origins of a key enzyme during the evolution of C4 and CAM metabolism

Journal of Experimental Botany

Volumn 65, Issue 13, 2014, Pages 3609-3621

  Christin, Pascal Antoine ^a,b   Arakaki, Monica ^b,c   Osborne, Colin P ^a   Bräutigam, Andrea ^d   Sage, Rowan F ^e   Hibberd, Julian M ^f   Kelly, Steven ^g   Covshoff, Sarah ^f   Wong, Gane Ka Shu ^h,i,j   Hancock, Lillian ^b   Edwards, Erika J ^b  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

^b BROWN UNIVERSITY   (United States)

^c UNIVERSIDAD NACIONAL MAYOR DE SAN MARCOS   (Peru)

^d HEINRICH HEINE UNIVERSITY   (Germany)

^e UNIVERSITY OF TORONTO   (Canada)

^f UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^g UNIVERSITY OF OXFORD   (United Kingdom)

^h UNIVERSITY OF ALBERTA   (Canada)

ⁱ UNIVERSITY OF ALBERTA   (Canada)

^j BGI SHENZHEN   (China)

more..

Author keywords

CAM photosynthesis; Co option; Evolution; Phosphoenolpyruvate carboxylase (PEPC); Phylogenetics

Indexed keywords

PHOSPHOENOLPYRUVATE CARBOXYLASE; TRANSCRIPTOME; VEGETABLE PROTEIN;

ENZYMOLOGY; EVOLUTION; GENETICS; HIGH THROUGHPUT SEQUENCING; MULTIGENE FAMILY; PHENOTYPE; PHOTOSYNTHESIS; PHYLOGENY; PORTULACA; SEQUENCE ANALYSIS;

BIOLOGICAL EVOLUTION; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; MULTIGENE FAMILY; PHENOTYPE; PHOSPHOENOLPYRUVATE CARBOXYLASE; PHOTOSYNTHESIS; PHYLOGENY; PLANT PROTEINS; PORTULACA; SEQUENCE ANALYSIS, RNA; TRANSCRIPTOME;

EID: 84911449534     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/eru087     Document Type: Article

References (83)

1. Arakaki M, Christin PA, Nyffeler R, Lendel A, Eggli U, Ogburn RM, Spriggs E, Moore MJ, Edwards EJ. 2011. Contemporaneous and recent radiations of the world's major succulent plant lineages. Proceedings of the National Academy of Sciences USA 108, 8379-8384.
2. 4 pathway. Journal of Experimental Botany 62, 3049-3059.
3. 4 intermediate species of Flaveria (Asteraceae). Plant Physiology 82, 695-699.
4. 4 photosynthesis in sedges (Cyperaceae): multiple appearances and genetic convergence. Molecular Biology and Evolution 26, 1909-1919.
5. 4-specifc characteristics. Journal of Biological Chemistry 275, 27917-27923.
6. Borland AM, Taybi T. 2004. Synchronization of metabolic processes in plants with Crassulacean acid metabolism. Journal of Experimental Botany 55, 1255-1265.
7. 4 species. Plant Physiology 155, 142-156.
8. Brockington SF, Alexandre R, Ramdial J, Moore MJ, Crawley S, Dhingra A, Kilu K, Soltis DE, Soltis PS. 2009. Phylogeny of the Caryophyllales sensu lato: revisiting hypotheses on pollination biology and perianth differentiation in the core Caryophyllales. International Journal of Plant Sciences 170, 627-643.
9. 4 origins in Aristidoideae (Poaceae) revealed by the recruitment of distinct phosphoenolpyruvate carboxylase genes. American Journal of Botany 96, 2234-2239.
10. Christin PA, Besnard G, Edwards EJ, Salamin N. 2012. Effect of genetic convergence on phylogenetic inference. Molecular Phylogenetics and Evolution 62, 921-927.
11. 4 photosynthesis. Genome Biology and Evolution 5, 2174-2187.
12. 4 origins and reversals? Trends in Ecology and Evolution 25, 403-409.
13. 4 photosynthesis, an evolutionary tale. Photosynthesis Research 117, 163-175.
14. 4 photosynthesis in grasses. Proceedings of the National Academy of Sciences USA 110, 1381-1386.
15. 4 intermediate forms of photosynthesis in Molluginaceae. Evolution 65, 643-660.
16. 4 photosynthesis evolved in grasses via parallel adaptive genetic changes. Current Biology 17, 1241-1247.
17. Crayn DM, Winter K, Smith JAC. 2004. Multiple origins of crassulacean acid metabolism and the epiphytic habit in the Neotropical family Bromeliaceae. Proceedings of the National Academy of Sciences USA 101, 3703-3708.
18. 4-form enzyme. Plant and Cell Physiology 39, 865-873.
19. Dunn CW, Howison M, Zapata F. 2013. Agalma: an automated phylogenomics workfow. BMC Bioinformatics 14, 300.
20. Edgar RC. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32, 1792-1797.
21. Edwards EJ, Donoghue MJ. 2013. Is it easy to move and easy to evolve? Evolutionary accessibility and adaptation. Journal of Experimental Botany 64, 4047-4052.
22. 4 photosynthesis as parallel evolutionary trajectories. International Journal of Plant Sciences 173, 724-733.
23. 4 phosphoenolpyruvate carboxylase of Flaveria trinervia. FEBS Letters 524, 11-14.
24. 4 monocot Urochloa panicoides is encoded by four differentially expressed genes. Plant Physiology 120, 1033-1041.
25. Gehrig H, Heute V, Kluge M. 2001. New partial sequences of phosphoenolpyruvate carboxylase as molecular phylogenetic markers. Molecular Phylogenetics and Evolution 20, 262-274.
26. Goodstein DM, Shu S, Howson R et al. 2012. Phytozome: a comparative platform for green plant genomics. Nucleic Acids Research 40, D1178-D1186.
27. 4? Plant Cell 23, 2087-2105.
28. 4 Alternantheras. Planta 223, 359-368.
29. 2 concentrating mechanisms. Advances in Photosynthesis and Respiration, Vol. 32. Dordrecht: Springer, 257-275.
30. Grabherr MG, Haas BJ, Yassour M et al. 2011. Full-length transcriptome assembly from RNA-seq data without a reference genome. Nature Biotechnology 29, 644-652.
31. 4 plants. Plant Cell and Environment 36, 249-261.
32. Guindon S, Gascuel O. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52, 696-704.
33. 4 and CAM photosynthesis in the genera Anacampseros and Grahamia of the Portulacaceae. Journal of Experimental Botany 59, 1735-1742.
34. 4-crassulacean acid metabolism-cycling plant Portulaca grandifora. Functional Plant Biology 29, 763-773.
35. Guralnick LJ, Jackson M. 2001. The occurrence and phylogenetics of CAM in the Portulacaceae. International Journal of Plant Sciences 162, 257-262.
36. Guralnick LJ, Ting IP. 1987. Physiological changes in Portulacaria afra (L.) Jacq. during a summer drought and rewatering. Plant Physiology 85, 481-486.
37. Hancock L, Edwards EJ. 2014. Phylogeny and the inference of evolutionary trajectories. Journal of Experimental Botany 65, 3491-3498.
38. 4 photosynthesis: a unique blend of modifed biochemistry, anatomy and ultrastructure. Biochimica et Biophysica Acta 895, 81-106.
39. 4 type leaf anatomy in grasses (Poaceae), mesophyll-bundle sheath area ratios. Annals of Botany 53, 163-179.
40. 4 and Crassulacean Acid Metabolism plants. Plant Physiology 95, 981-985.
41. Johnson MTJ, Carpenter EJ, Tian Z et al. 2012. Evaluating methods for isolating total RNA and predicting the success of sequencing phylogenetically diverse plant transcriptomes. PLOS ONE 7, e50226.
42. 4 photosynthesis evolution in plants inferred from the goosefoot family (Chenopodiaceae s.s.). Proceedings of the Royal Society of London Series B 279, 3304-3311.
43. 4 photosynthesis. International Journal of Plant Sciences 164, 959-986.
44. 4 carbon-concentrating mechanisms. International Journal of Plant Sciences 164, S55-S77.
45. 4 dicot, Portulaca oleracea L. Plant Physiology 65, 193-197.
46. 4 dicot, Portulaca oleracea L. under natural environmental conditions. Plant Physiology 69, 757-761.
47. 4 genus Portulaca. International Journal of Plant Sciences 157, 103-109.
48. Langmead B, Salzberg S. 2012. Fast gapped-read alignment with Bowtie 2. Nature Methods 9, 357-359.
49. 4 species. Plant Physiology 142, 673-684.
50. 4 succulent plant, Portulaca oleracea L.: physiological and morphological changes are accompanied by specifc modifcations in phosphoenolpyruvate carboxylase. Photosynthesis Research 77, 241-254.
51. 4 succulent plant, Portulaca oleracea L.: study of enzymes involved in carbon fxation and carbohydrate metabolism. Plant Cell and Environment 45, 618-626.
52. Lepiniec L, Vidal J, Chollet R, Gadal P, Cretin C. 1994. Phosphoenolpyruvate carboxylase: structure, function, regulation and evolution. Plant Science 99, 111-124.
53. Ludwig M. 2011. The molecular evolution of β-carbonic anhydrase in Flaveria. Journal of Experimental Botany 62, 3071-3081.
54. 4 plant Portulaca oleracea. Physiologia Plantarum 98, 111-116.
55. 4 plant Portulaca olearacea. Photosynthetica 38, 385-391.
56. 4 photosynthesis. International Journal of Plant Sciences 164, S43-S54.
57. Nelson EA, Sage TL, Sage RF. 2005. Functional leaf anatomy of plants with crassulacean acid metabolism. Functional Plant Biology 32, 409-419.
58. Nimmo HG. 2003. How to tell the time: the regulation of phosphoenolpyruvate carboxylase in Crassulacean acid metabolism (CAM) plants. Biochemical Society Transactions 31, 728-730.
59. Nyffeler R, Eggli U. 2010. Disintegrating Portulacaceae: a new familial classifcation of the suborder Portulacineae (Caryophyllales) based on molecular and morphological data. Taxon 59, 227-240.
60. Nyffeler R, Eggli U, Ogburn M, Edwards EJ. 2008. Variations on a theme: repeated evolution of succulent life forms in the Portulacineae (Caryophyllales). Haseltonia 14, 26-36.
61. Ocampo G, Columbus JT. 2010. Molecular phylogenetics of suborder Cactineae (Caryophyllales), including insights into photosynthetic diversifcation and historical biogeography. American Journal of Botany 97, 1827-1847.
62. Ocampo G, Columbus JT. 2012. Molecular phylogenetics, historical biogeography, and chromosome number evolution of Portulaca (Portulacaceae). Molecular Phylogenetics and Evolution 63, 97-112.
63. Ocampo G, Koteyeva NK, Voznesenskaya EV, Edwards GE, Sage TL, Sage RF, Columbus JT. 2013. Evolution of leaf anatomy and photosynthetic pathways in Portulacaceae. American Journal of Botany 100, 2388-2402.
64. Ogburn RM, Edwards EJ. 2013. Repeated origin of three-dimensional leaf venation releases constraints on the evolution of succulence in plants. Current Biology 23, 722-726.
65. Osmond CB. 1978. Crassulacean acid metabolism. A curiosity in context. Annual Reviews of Plant Physiology 29, 379-414.
66. Rambaut A, Drummond AJ. 2007. Tracer v1.4, available at http://beadt. bio.ed.ac.uk/Tracer.
67. 4 system of Hydrilla verticillata. Plant Physiology 130, 876-886.
68. 4-signature serine. Plant Science 174, 475-483.
69. Raven JA, Cockell CS, De La Rocha CS. 2008. The evolution of inorganic carbon concentrating mechanisms in photosynthesis. Philosophical Transactions of the Royal Society of London Series B 363, 2641-2650.
70. Rickers J, Cushman JC, Michalowski CB, Schmitt JM, Bohnert HJ. 1989. Expression of the CAM-form of phospho(enol)pyruvate carboxylase and nucleotide sequence of a full length cDNA of Mesembryanthemum crystallinum. Molecular and General Genetics 215, 447-454.
71. Ronquist F, Huelsenbeck JP. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572-1574.
72. 4 photosynthetic syndrome. Plant Biology 3, 202-213.
73. 4 photosynthesis incompatible? Functional Plant Biology 29, 775-785.
74. 4 plant lineages of planet Earth. Journal of Experimental Botany 62, 3155-3169.
75. 4 photosynthesis. Annual Reviews of Plant Biology 63, 19-47.
76. Silvera K, Santiago LS, Winter K. 2005. Distribution of crassulacean acid metabolism in orchids of Panama: evidence of selection for weak and strong modes. Functional Plant Biology 32, 397-407.
77. Soltis DE, Smith SA, Cellinese N et al. 2011. Angiosperm phylogeny: 17 genes, 640 taxa. American Journal of Botany 98, 704-730.
78. 4 phosphoenolpyruvate carboxylase. Archives of Biochemistry and Biophysics 414, 180-188.
79. 4 NADP-dependent malic enzymes are encoded by distinct genes derived from a plastid-localized ancestor. Plant Molecular Biology 50, 635-652.
80. Thompson JD, Higgins DJ, Gibson TJ. 1994. ClustalW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position specifc gap penalties and matrix choice. Nucleic Acids Research 22, 4673-4680.
81. 4 photosynthesis in genus Portulaca L. (Portulacaceae). Journal of Experimental Botany 61, 3647-3662.
82. Yang ZH. 2007. PAML4: phylogenetic analysis by maximum likelihood. Molecular Biology and Evolution 24, 1586-1591.
83. Yang ZH, Nielsen R. 2002. Codon-substitutions models for detecting molecular adaptation at individual sites along specifc lineages. Molecular Biology and Evolution 19, 908-917.