Parallel recruitment of multiple genes into C4 photosynthesis

Genome Biology and Evolution

Volumn 5, Issue 11, 2013, Pages 2174-2187

  Christin, Pascal Antoine ^a   Boxall, Susanna F ^b   Gregory, Richard ^b   Edwards, Erika J ^c   Hartwell, James ^b   Osborne, Colin P ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

^b UNIVERSITY OF LIVERPOOL   (United Kingdom)

^c BROWN UNIVERSITY   (United States)

Author keywords

Co option; Complex traits; Evolutionary novelty; Gene families; Phylogenomics

Indexed keywords

CARBON DIOXIDE; TRANSCRIPTOME; VEGETABLE PROTEIN;

AIR; ARTICLE; CO-OPTION; COMPLEX TRAITS; EVOLUTIONARY NOVELTY; GENE FAMILIES; GENETICS; METABOLISM; MOLECULAR EVOLUTION; PHOTOSYNTHESIS; PHYLOGENOMICS; PLANT GENE; POACEAE;

CO-OPTION; COMPLEX TRAITS; EVOLUTIONARY NOVELTY; GENE FAMILIES; PHYLOGENOMICS;

AIR; CARBON DIOXIDE; EVOLUTION, MOLECULAR; GENES, PLANT; PHOTOSYNTHESIS; PLANT PROTEINS; POACEAE; TRANSCRIPTOME;

EID: 84892657232     PISSN: None     EISSN: 17596653     Source Type: Journal    
DOI: 10.1093/gbe/evt168     Document Type: Article

References (76)

1. 4 species. Photosynth Res. 115:65-80.
2. Arnegard ME, Zwickl DJ, Lu Y, Zakon HH. 2010. Old gene duplication facilitates origins and diversification of an innovative communication system-twice. Proc Natl Acad Sci U S A. 107:22172-22177.
3. 4 pathway. J Exp Bot. 62:3049-3059.
4. Badger MR, Price GD. 1994. The role of carbonic anhydrase in photosynthesis. Annu Rev Plant Physiol Plant Mol Biol. 45:369-392.
5. Bennetzen JL, et al. 2012. Reference genome sequence of the model plant Setaria. Nature Biotech. 30:555-561.
6. Blount ZD, Barrick JE, Davidson CJ, Lenski RE. 2012. Genomic analysis of a key innovation in an experimental Escherichia coli population. Nature 489:513-518.
7. Boxall SF, et al. 2005. Conservation and divergence of circadian clock operation in a stress-inducible crassulacean metabolism species reveals clock compensation against stress. Plant Physiol. 137:969-982.
8. 4 metabolite fluxes. Plant Physiol. 148:568-579.
9. 4 species. Plant Physiol. 155:142-156.
10. 4 photosynthesis. Science 331:1436-1439.
11. Chang YM, et al. 2012. Characterizing regulatory and functional differentiation between maize mesophyll and bundle sheath cells by transcriptomic analysis. Plant Physiol. 160:165-177.
12. Chevreux B, et al. 2004. Using the miraEST assembler for reliable and automated mRNA transcript assembly and SNP detection in sequenced ESTs. Genome Res. 14:1147-1159.
13. 4 photosynthesis evolved in grasses via parallel adaptive genetic changes. Curr Biol. 17:1241-1247.
14. 4 origins and reversals? Trends Ecol Evol. 25:403-409.
15. 4 phosphoenolpyruvate carboxykinase in grasses, from genotype to phenotype. Mol Biol Evol. 26:357-365.
16. 4 photosynthetic subtypes in grasses from genomics and phylogenetics. Genome Biol Evol. 1:221-230.
17. Christin PA, Weinreich D, Besnard G. 2010. Causes and evolutionary significance of genetic convergence. Trends Genet. 26:400-405.
18. 4 photosynthesis in grasses. Curr Biol. 18:37-43.
19. 4 photosynthesis through recurrent lateral gene transfer. Curr Biol. 22:445-449.
20. Edgar RC. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32:1792-1797.
21. Emanuelsson O, Nielsen H, von Heijne G. 1999. ChloroP, a neural network-based method for predicting chloroplast transit peptides and their cleavage sites. Protein Sci. 8:978-984.
22. 4 monocot Urochloa panicoides is encoded by four differentially expressed genes. Plant Physiol. 120:1033-1041.
23. Flagel LE, Wendel JF. 2009. Gene duplication and evolutionary novelty in plants. New Phytol. 183:557-564.
24. 4 acid decarboxylation types? J Exp Bot. 62 3103-3108.
25. Gerstein AC, Lo DS, Otto SP. 2012. Parallel genetic changes and nonparallel gene-environment interactions characterize the evolution of drug resistance in yeast. Genetics 192:241-252.
26. 4? Plant Cell 23:2087-2105.
27. 4 origins. New Phytol. 193:304-312.
28. Guindon S, Gascuel O. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol. 52:696-704.
29. Guo YL. 2013. Gene family evolution in green plants with emphasis on the origination and evolution of Arabidopsis thaliana genes. Plant J. 73:941-951.
30. 4 plants. Planta 119:279-300.
31. 4 photosynthesis: a unique blend of modified biochemistry, anatomy and ultrastructure. Biochim Biophys Acta. 895:81-106.
32. 4 dicarboxylic acid pathway of photosynthesis. Biochem J. 106:141-146.
33. 4 acid decarboxylating systems and ultrastructural features. Aust J Plant Physiol. 2:111-128.
34. 4 photosynthesis. Annu Rev Plant Biol. 61:181-207.
35. Hoffmann FG, Storz JF, Gorr TA, Opazo JC. 2010. Lineage-specific patterns of functional diversification in the a-and/J-globin gene families of tetrapod vertebrates. Mol Biol Evol. 27:1126-1138.
36. 3 photosynthesis. Ann Bot. 103:127-136.
37. 4-dicarboxylic acid pathway of photosynthesis. Biochem J. 119:273-280.
38. 4 photosynthesis. Plant J. 69:47-56.
39. 4 plant biology. San Diego (CA): Academic Press. p. 49-87.
40. 4 dicot. Plant Physiol. 68:1073-1080.
41. Langmead B, Salzberg SL. 2012. Fast gapped-read alignment with Bowtie2. Nat Methods. 9:357-359.
42. Li P, et al. 2010. The developmental dynamics of the maize leaf transcriptome. Nat Genet. 42:1060-1067.
43. Ludwig M. 2011. The molecular evolution of p-carbonic anhydrase in Flaveria. J Exp Bot. 62:3071-3081.
44. Malone S, Bahrami AR, Walker RP, Gray JE, Leegood RC. 2007. Phosphoenolpyruvate carboxykinase in Arabidopsis thaliana: changes in isoforms and location during vegetative and floral development. Plant Cell Physiol. 48:441-450.
45. 3 plant wheat. J Exp Bot. 48:799-811.
46. 4 photosynthesis. Int J Plant Sci. 164:S43-S54.
47. Monteiro A, Podlaha O. 2009. Wings, horns, and butterfly eyespots: how do complex traits evolve? PLoS Biol. 7:e1000037.
48. 4 eudicots. Am J Bot. 94:362-381.
49. Nei M, Rooney AP. 2005. Concerted and birth-and-death evolution of multigene families. Annu Rev Genet. 39:121-152.
50. Parsley K, Hibberd JM. 2006. The Arabidopsis PPDK gene is transcribed from two promoters to produce differentially expressed transcripts responsible for cytosolic and plastidic proteins. Plant Mol Biol. 62:339-349.
51. 4 model and provides candidates for regulation. Plant Cell 23:4208-4220.
52. 4 grasses (Poaceae). Aust J Plant Physiol. 14:403-420.
53. 4 photosynthesis. New Phytol. 161:341-370.
54. 4 plant lineages of planet Earth. J Exp Bot. 62:3155-3169.
55. 4 photosynthesis. Annu Rev Plant Biol. 63:19-47.
56. Sheen J. 1991. Molecular mechanisms underlying the differential expression of maize pyruvate, orthopshosphate dikinase genes. Plant Cell 3:225-245.
57. 4 gene expression. Annu Rev Plant Physiol Plant Mol Biol. 50:187-217.
58. 4 pathway genes in mesophyll and bundle sheath cells of greening maize leaves. J Biol Chem. 262:11726-11730.
59. 4 plant. Plant Physiol. 69:776-780.
60. 4 phosphoenolpyruvate carboxylase. Arch Biochem Biophys. 414:180-188.
61. Storz JF, Opazo JC, Hoffmann FG. 2013. Gene duplication, genome duplication, and the functional diversification of vertebrate genomes. Mol Phylogenet Evol. 66:469-478.
62. Studer RA, Robinson-Rechavi M. 2009. How confident can we be that orthologs are similar, but paralogs differ? Trends Genet. 25 210-216.
63. 4 plant: purification, characterization, and preparation of antibody. Arch Biochem Biophys. 282:427-432.
64. 4 NADP-dependent malic enzymes are encoded by distinct genes derived from a plastid-localized ancestor. Plant Mol Biol. 50:635-652.
65. Thompson JD, Higgins DJ, Gibson TJ. 1994. ClustalW: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position specific gap penalties and matrix choice. Nucleic Acids Res. 22:4673-4680.
66. Ting IP, Osmond CB. 1973. Multiple forms of plant phosphoenolpyruvate carboxylase associated with different metabolic pathways. Plant Physiol. 51:448-453.
67. Tomoyasu Y, Arakane Y, Kramer KJ, Denell RE. 2009. Repeated co-options of exoskeleton formation during wing-to-elytron evolution in beetles. Curr Biol. 19:2057-2065.
68. True JR, Carroll SB. 2002. Gene co-option in physiological and morphological evolution. Annu Rev Cell Dev Biol. 18:53-80.
69. 4 Alloteropsis semialata subspecies. Plant Cell Environ. 29:257-268.
70. 4 photosynthesis. Global Change Biol. 14:2963-2977.
71. 4 photosynthetic pathway evolution in grasses. Genome Biol. 10:R68.
72. Weinreich DM, Delaney NF, DePristo MA, Hartl DL. 2006. Darwinian evolution can follow only very few mutational paths to fitter proteins. Science 312:111-114.
73. Wingler A, Walker RP, Chen ZH, Leegood RC. 1999. Phosphoenolpyruvate carboxykinase is involved in the decarboxylation of aspartate in the bundle sheath of maize. Plant Physiol. 120:539-545.
74. Woods R, Schneider D, Winkworth CL, Riley MA, Lenski RE. 2006. Tests of parallel molecular evolution in a long-term experiment with Escherichia coli. Proc Natl Acad Sci U S A. 103:9107-9112.
75. Xu G, Ma H, Nei M, Kong H. 2009. Evolution of F-box in plants: Different modes of sequence divergence and their relationships with functional diversification. Proc Natl Acad Sci U S A. 106:835-840.
76. Zakon HH, Lu Y, Zwickl DJ, Hillis DM. 2006. Sodium channel genes and the evolution of diversity in communication signals of electric fishes: convergent molecular evolution. Proc Natl Acad Sci U S A. 103:3675-3680.