Cross species selection scans identify components of C4 photosynthesis in the grasses

Journal of Experimental Botany

Volumn 68, Issue 2, 2017, Pages 127-135

  Huang, Pu ^a   Studer, Anthony J ^b   Schnable, James C ^c   Kellogg, Elizabeth A ^a   Brutnell, Thomas P ^a  

^a DONALD DANFORTH PLANT SCIENCE CENTER   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^c UNIVERSITY OF NEBRASKA LINCOLN   (United States)

Author keywords

Adaptation; C4 photosynthesis; Cross species selection scans; Gene discovery; Grasses; Parallel evolution

Indexed keywords

ADAPTATION; COMPARATIVE STUDY; GENETIC SELECTION; GENETICS; GENOME-WIDE ASSOCIATION STUDY; MOLECULAR EVOLUTION; PHOTOSYNTHESIS; PLANT GENOME; POACEAE;

ADAPTATION, BIOLOGICAL; EVOLUTION, MOLECULAR; GENOME, PLANT; GENOME-WIDE ASSOCIATION STUDY; PHOTOSYNTHESIS; POACEAE; SELECTION, GENETIC;

EID: 85014539619     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/erw256     Document Type: Article

References (52)

1. Aoki N, Ohnishi J, Kanai R. 1992. Two different mechanisms for transport of pyruvate into mesophyll chloroplasts of C4 plants-a comparative study. Plant and cell Physiology 33, 805-809.
2. Bailey KJ, Battistelli A, Dever LV, Lea PJ, Leegood RC. 2000. Control of C4 photosynthesis: effects of reduced activities of phosphoenolpyruvate carboxylase on CO2 assimilation in Amaranthus edulis L. Journal of Experimental Botany 51, 339-346.
3. Bennetzen JL, Schmutz J, Wang H, et al. 2012. Reference genome sequence of the model plant Setaria. Nature Biotechnology 30, 555-561.
4. Brown WV. 1975. Variations in anatomy, associations, and origins of Kranz tissue. American Journal of Botany 62, 395-402.
5. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden TL. 2009. BLAST+: architecture and applications. BMC Bioinformatics 10, 421.
6. Castresana J. 2000. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Biology and Evolution 17, 540-552.
7. Chang Y-M, Liu W-Y, Shih AC-C, et al. 2012. Characterizing regulatory and functional differentiation between maize mesophyll and bundle sheath cells by transcriptomic analysis. Plant Physiology 160, 165-177.
8. Christin P-A, Boxall SF, Gregory R, Edwards EJ, Hartwell J, Osborne CP. 2013. Parallel recruitment of multiple genes into C4 photosynthesis. Genome Biology and Evolution 5, 2174-2187.
9. Christin P-A, Petitpierre B, Salamin N, Buchi L, Besnard G. 2009. Evolution of C4 phosphoenolpyruvate carboxykinase in grasses, from genotype to phenotype. Molecular Biology and Evolution 26, 357-365.
10. Christin P-A, Salamin N, Savolainen V, Duvall MR, Besnard G. 2007. C4 photosynthesis evolved in grasses via parallel adaptive genetic changes. Current Biology 17, 1241-1247.
11. Christin PA, Samaritani E, Petitpierre B, Salamin N, Besnard G. 2010. Evolutionary insights on C4 photosynthetic subtypes in grasses from genomics and phylogenetics. Genome Biology and Evolution 1, 221-230.
12. Christin P-A, Spriggs E, Osborne CP, Stromberg CAE, Salamin N, Edwards EJ. 2014. Molecular dating, evolutionary rates, and the age of the grasses. Systematic Biology 63, 153-165.
13. Cousins AB, Badger MR, von Caemmerer S. 2006. Carbonic anhydrase and its influence on carbon isotope discrimination during C4 photosynthesis. Insights from antisense RNA in Flaveria bidentis. Plant Physiology 141, 232-242.
14. Du Z, Zhou X, Ling Y, Zhang Z, Su Z. 2010. agriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Research 38, W64-W70.
15. Edwards EJ, Smith SA. 2010. Phylogenetic analyses reveal the shady history of C4 grasses. Proceedings of the National Academy of Sciences of the United States of America 107, 2532-2537.
16. Furbank RT. 2011. Evolution of the C4 photosynthetic mechanism: are there really three C4 acid decarboxylation types? Journal of Experimental Botany 62, 3103-3108.
17. Furumoto T, Yamaguchi T, Ohshima-Ichie Y, et al. 2011. A plastidial sodium-dependent pyruvate transporter. Nature 476, 472-475.
18. Giussani LM, Cota-Sánchez JH, Zuloaga FO, Kellogg EA. 2001. A molecular phylogeny of the grass subfamily Panicoideae (Poaceae) shows multiple origins of C4 photosynthesis. American Journal of Botany 88, 1993-2012.
19. Grass Phylogeny Working Group II. 2012. New grass phylogeny resolves deep evolutionary relationships and discovers C4 origins. New Phytologist 193, 304-312.
20. Heckmann D, Schulze S, Denton A, Gowik U, Westhoff P, Weber AP, Lercher MJ. 2013. Predicting C4 photosynthesis evolution: modular, individually adaptive steps on a Mount Fuji fitness landscape. Cell 153, 1579-1588.
21. Huang P, Brutnell TP. 2016. A synthesis of transcriptomic surveys to dissect the genetic basis of C4 photosynthesis. Current Opinion in Plant Biology 31, 91-99.
22. John CR, Smith-Unna RD, Woodfield H, Covshoff S, Hibberd JM. 2014. Evolutionary convergence of cell-specific gene expression in independent lineages of C4 grasses. Plant Physiology 165, 62-75.
23. Kinoshita H, Nagasaki J, Yoshikawa N, Yamamoto A, Takito S, Kawasaki M, Sugiyama T, Miyake H, Weber APM, Taniguchi M. 2011. The chloroplastic 2-oxoglutarate/malate transporter has dual function as the malate valve and in carbon/nitrogen metabolism: OMT in malate valve and C/N interaction. The Plant Journal 65, 15-26.
24. Kumar S, Stecher G, Peterson D, Tamura K. 2012. MEGA-CC: computing core of molecular evolutionary genetics analysis program for automated and iterative data analysis. Bioinformatics 28, 2685-2686.
25. Li P, Ponnala L, Gandotra N, et al. 2010. The developmental dynamics of the maize leaf transcriptome. Nature Genetics 42, 1060-1067.
26. Mailund T, Pedersen CNS. 2004. QDist-quartet distance between evolutionary trees. Bioinformatics 20, 1636-1637.
27. Majeran W, van Wijk KJ. 2009. Cell-type-specific differentiation of chloroplasts in C4 plants. Trends in Plant Science 14, 100-109.
28. Ouyang S, Zhu W, Hamilton J, et al. 2007. The TIGR rice genome annotation resource: improvements and new features. Nucleic Acids Research 35, D883-D887.
29. Paterson AH, Bowers JE, Bruggmann R, et al. 2009. The Sorghum bicolor genome and the diversification of grasses. Nature 457, 551-556.
30. Pick TR, Bräutigam A, Schlüter U, et al. 2011. Systems analysis of a maize leaf developmental gradient redefines the current C4 model and provides candidates for regulation. The Plant Cell 23, 4208-4220.
31. Pyke KA, Leech RM. 1994. A genetic analysis of chloroplast division and expansion in Arabidopsis thaliana. Plant Physiology 104, 201-207.
32. Sage RF. 2004. The evolution of C4 photosynthesis. New Phytologist 161, 341-370.
33. Sage RF, Christin P-A, Edwards EJ. 2011. The C4 plant lineages of planet Earth. Journal of Experimental Botany 62, 3155-3169.
34. Sage RF, Sage TL, Kocacinar F. 2012. Photorespiration and the evolution of C4 photosynthesis. Annual Review of Plant Biology 63, 19-47.
35. Schnable JC, Freeling M, Lyons E. 2012. Genome-wide analysis of syntenic gene deletion in the grasses. Genome Biology and Evolution 4, 265-277.
36. Schnable PS, Ware D, Fulton RS, et al. 2009. The B73 maize genome: complexity, diversity, and dynamics. Science 326, 1112-1115.
37. Sieburth LE. 2006. SCARFACE Encodes an ARF-GAP that is required for normal auxin efflux and vein patterning in Arabidopsis. The Plant Cell 18, 1396-1411.
38. Slewinski TL, Anderson AA, Zhang C, Turgeon R. 2012. Scarecrow plays a role in establishing kranz anatomy in maize leaves. Plant and Cell Physiology 53, 2030-2037.
39. Stamatakis A. 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312-1313.
40. Still CJ, Berry JA, Collatz GJ, DeFries RS. 2003. Global distribution of C3 and C4 vegetation: Carbon cycle implications. Global Biogeochemical Cycles 17, 6-1-6-14.
41. Strimmer K. 2008. fdrtool: a versatile R package for estimating local and tail area-based false discovery rates. Bioinformatics 24, 1461-1462.
42. Studer AJ, Gandin A, Kolbe AR, Wang L, Cousins AB, Brutnell TP. 2014. A limited role for carbonic anhydrase in C4 photosynthesis as revealed by a ca1ca2 double mutant in maize. Plant Physiology 165, 608-617.
43. Szalkowski AM. 2012. Fast and robust multiple sequence alignment with phylogeny-aware gap placement. BMC Bioinformatics 13, 129.
44. Vicentini A, Barber JC, Aliscioni SS, Giussani LM, Kellogg EA. 2008. The age of the grasses and clusters of origins of C4 photosynthesis. Global Change Biology 14, 2963-2977.
45. Vincill ED, Clarin AE, Molenda JN, Spalding EP. 2013. Interacting glutamate receptor-like proteins in phloem regulate lateral root initiation in Arabidopsis. The Plant Cell 25, 1304-1313.
46. Vogel JP, Garvin DF, Mockler TC, et al. 2010. Genome sequencing and analysis of the model grass Brachypodium distachyon. Nature 463, 763-768.
47. Wang L, Czedik-Eysenberg A, Mertz RA, et al. 2014a. Comparative analyses of C4 and C3 photosynthesis in developing leaves of maize and rice. Nature Biotechnology 32, 1158-1165.
48. Wang X, Gowik U, Tang H, Bowers JE, Westhoff P, Paterson AH. 2009. Comparative genomic analysis of C4 photosynthetic pathway evolution in grasses. Genome Biology 10, R68.
49. Wang Y, Long SP, Zhu X-G. 2014b. Elements required for an efficient NADP-malic enzyme type C4 photosynthesis. Plant Physiology 164, 2231-2246.
50. Windhövel A, Hein I, Dabrowa R, Stockhaus J. 2001. Characterization of a novel class of plant homeodomain proteins that bind to the C4 phosphoenolpyruvate carboxylase gene of Flaveria trinervia. Plant Molecular Biology 45, 201-214.
51. Wingler A, Walker RP, Chen Z-H, Leegood RC. 1999. Phosphoenolpyruvate carboxykinase is involved in the decarboxylation of aspartate in the bundle sheath of maize. Plant Physiology 120, 539-546.
52. Yang Z. 2007. PAML 4: phylogenetic analysis by maximum likelihood. Molecular Biology and Evolution 24, 1586-1591.