Identification of photosynthesis-associated C4 candidate genes through comparative leaf gradient transcriptome in multiple lineages of C3 and C4 species

PLoS ONE

Volumn 10, Issue 10, 2015, Pages

  Ding, Zehong ^a,b   Weissmann, Sarit ^c   Wang, Minghui ^b   Du, Baijuan ^d   Huang, Lei ^b   Wang, Lin ^c   Tu, Xiaoyu ^e   Zhong, Silin ^e   Myers, Christopher ^b   Brutnell, Thomas P ^c   Sun, Qi ^b   Li, Pinghua ^d  

^a INSTITUTE OF TROPICAL BIOSCIENCE AND BIOTECHNOLOGY   (China)

^b Cornell University ^*  (United States)

^c DONALD DANFORTH PLANT SCIENCE CENTER   (United States)

^d SHANDONG AGRICULTURAL UNIVERSITY   (China)

^e CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

[No Author keywords available]

Indexed keywords

PLANT RNA; STARCH; SUCROSE; TRANSCRIPTOME; CARBON DIOXIDE; NITROGEN;

ARTICLE; COMPARATIVE STUDY; CONTROLLED STUDY; GENE CONTROL; GENE EXPRESSION; GENE IDENTIFICATION; GENETIC ASSOCIATION; GENETIC TRAIT; GENETIC TRANSCRIPTION; LEAF DEVELOPMENT; MAIZE; METABOLITE; NONHUMAN; PHOTOACTIVATION; PHOTOSYNTHESIS; PLANT GENE; PLANT GENETICS; PLANT LEAF; RICE; SORGHUM; SUCROSE METABOLISM; TRANSCRIPTION REGULATION; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENETICS; LIGHT; METABOLIC ENGINEERING; METABOLISM; ORYZA;

CARBON DIOXIDE; GENE EXPRESSION REGULATION, PLANT; GENE REGULATORY NETWORKS; LIGHT; METABOLIC ENGINEERING; METABOLIC NETWORKS AND PATHWAYS; NITROGEN; ORYZA; PHOTOSYNTHESIS; PLANT LEAVES; SORGHUM; TRANSCRIPTOME; ZEA MAYS;

EID: 84949035143     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0140629     Document Type: Article

References (60)

1. Hibberd JM, Sheehy JE, Langdale JA. Using C4 photosynthesis to increase the yield of rice - rationale and feasibility. Current opinion in plant biology. 2008; 11(2):228-31. doi: 10.1016/j.pbi.2007.11.002 PMID: 18203653
2. Mitchell P, Sheehy J. Supercharging rice photosynthesis to increase yield. New Phytologist. 2006; 171 (4):688-93. PMID: 16918541
3. Zhu X-G, Long SP, Ort DR. Improving photosynthetic efficiency for greater yield. Annual review of plant biology. 2010; 61:235-61. doi: 10.1146/annurev-arplant-042809-112206 PMID: 20192734
4. Sage RF. The evolution of C4 photosynthesis. New phytologist. 2004; 161(2):341-70.
5. Peterhansel C. Best practice procedures for the establishment of a C4 cycle in transgenic C3 plants. Journal of experimental botany. 2011; 62(9):3011-9. doi: 10.1093/jxb/err027 PMID: 21335437
6. Miyao M, Masumoto C, Miyazawa S-I, Fukayama H. Lessons from engineering a single-cell C4 photosynthetic pathway into rice. Journal of experimental botany. 2011; 62(9):3021-9. doi: 10.1093/jxb/err023 PMID: 21459764
7. Kajala K, Covshoff S, Karki S, Woodfield H, Tolley BJ, Dionora MJA, et al. Strategies for engineering a two-celled C4 photosynthetic pathway into rice. Journal of experimental botany. 2011; 62(9):3001-10. doi: 10.1093/jxb/err022 PMID: 21335436
8. Sage RF, Christin P-A, Edwards EJ. The C4 plant lineages of planet Earth. Journal of Experimental Botany. 2011; 62(9):3155-69. doi: 10.1093/jxb/err048 PMID: 21414957
9. Hibberd JM, Covshoff S. The regulation of gene expression required for C4 photosynthesis. Annual review of plant biology. 2010; 61:181-207. doi: 10.1146/annurev-arplant-042809-112238 PMID: 20192753
10. Aubry S, Brown NJ, Hibberd JM. The role of proteins in C3 plants prior to their recruitment into the C4 pathway. Journal of experimental botany. 2011; 62(9):3049-59. doi: 10.1093/jxb/err012 PMID: 21321052
11. Christin P-A, Boxall SF, Gregory R, Edwards EJ, Hartwell J, Osborne CP. Parallel recruitment of multiple genes into C4 photosynthesis. Genome biology and evolution. 2013; 5(11):2174-87. doi: 10.1093/gbe/evt168 PMID: 24179135
12. Schnable PS, Ware D, Fulton RS, Stein JC, Wei F, Pasternak S, et al. The B73 maize genome: complexity, diversity, and dynamics. science. 2009; 326(5956):1112-5. doi: 10.1126/science.1178534 PMID: 19965430
13. Paterson AH, Bowers JE, Bruggmann R, Dubchak I, Grimwood J, Gundlach H, et al. The Sorghum bicolor genome and the diversification of grasses. Nature. 2009; 457(7229):551-6. doi: 10.1038/nature07723 PMID: 19189423
14. Zhang G, Liu X, Quan Z, Cheng S, Xu X, Pan S, et al. Genome sequence of foxtail millet (Setaria italica) provides insights into grass evolution and biofuel potential. Nature biotechnology. 2012; 30(6):549-54. doi: 10.1038/nbt.2195 PMID: 22580950
15. Bennetzen JL, Schmutz J, Wang H, Percifield R, Hawkins J, Pontaroli AC, et al. Reference genome sequence of the model plant Setaria. Nature biotechnology. 2012; 30(6):555-61. doi: 10.1038/nbt.2196 PMID: 22580951
16. Majeran W, Cai Y, Sun Q, van Wijk KJ. Functional differentiation of bundle sheath and mesophyll maize chloroplasts determined by comparative proteomics. The Plant Cell Online. 2005; 17(11):3111-40.
17. Majeran W, Zybailov B, Ytterberg AJ, Dunsmore J, Sun Q, van Wijk KJ. Consequences of C4 differentiation for chloroplast membrane proteomes in maize mesophyll and bundle sheath cells. Molecular & Cellular Proteomics. 2008; 7(9):1609-38.
18. Friso G, Majeran W, Huang M, Sun Q, Van Wijk KJ. Reconstruction of metabolic pathways, protein expression, and homeostasis machineries across maize bundle sheath and mesophyll chloroplasts: large-scale quantitative proteomics using the first maize genome assembly. Plant physiology. 2010; 152(3):1219-50. doi: 10.1104/pp.109.152694 PMID: 20089766
19. Chang Y-M, Liu W-Y, Shih AC-C, Shen M-N, Lu C-H, Lu M-YJ, et al. Characterizing regulatory and functional differentiation between maize mesophyll and bundle sheath cells by transcriptomic analysis. Plant physiology. 2012; 160(1):165-77. doi: 10.1104/pp.112.203810 PMID: 22829318
20. Tausta SL, Li P, Si Y, Gandotra N, Liu P, Sun Q, et al. Developmental dynamics of Kranz cell transcriptional specificity in maize leaf reveals early onset of C4-related processes. Journal of experimental botany. 2014:eru152.
21. Wang P, Kelly S, Fouracre JP, Langdale JA. Genome-wide transcript analysis of early maize leaf development reveals gene cohorts associated with the differentiation of C4 Kranz anatomy. The Plant Journal. 2013; 75(4):656-70. doi: 10.1111/tpj.12229 PMID: 23647263
22. John CR, Smith-Unna RD, Woodfield H, Covshoff S, Hibberd JM. Evolutionary convergence of cellspecific gene expression in independent lineages of C4 grasses. Plant Physiol. 2014; 165(1):62-75. doi: 10.1104/pp.114.238667 PMID: 24676859; PubMed Central PMCID: PMC4012605.
23. Jiao Y, Tausta SL, Gandotra N, Sun N, Liu T, Clay NK, et al. A transcriptome atlas of rice cell types uncovers cellular, functional and developmental hierarchies. Nature genetics. 2009; 41(2):258-63. doi: 10.1038/ng.282 PMID: 19122662
24. Li P, Ponnala L, Gandotra N, Wang L, Si Y, Tausta SL, et al. The developmental dynamics of the maize leaf transcriptome. Nature genetics. 2010; 42(12):1060-7. doi: 10.1038/ng.703 PMID: 21037569
25. Pick TR, Bräutigam A, Schlüter U, Denton AK, Colmsee C, Scholz U, et al. Systems analysis of a maize leaf developmental gradient redefines the current C4 model and provides candidates for regulation. The Plant Cell Online. 2011; 23(12):4208-20.
26. Wang L, Czedik-Eysenberg A, Mertz RA, Si Y, Tohge T, Nunes-Nesi A, et al. Comparative analyses of C4 and C3 photosynthesis in developing leaves of maize and rice. Nature biotechnology. 2014.
27. Bräutigam A, Hoffmann-Benning S, Weber AP. 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 maintaining C4 metabolite fluxes. Plant physiology. 2008; 148(1):568-79. doi: 10.1104/pp.108.121012 PMID: 18599648
28. Bräutigam A, Kajala K, Wullenweber J, Sommer M, Gagneul D, Weber KL, et al. An mRNA blueprint for C4 photosynthesis derived from comparative transcriptomics of closely related C3 and C4 species. Plant Physiology. 2011; 155(1):142-56. doi: 10.1104/pp.110.159442 PMID: 20543093
29. Nelson T. The grass leaf developmental gradient as a platform for a systems understanding of the anatomical specialization of C4 leaves. Journal of experimental botany. 2011; 62(9):3039-48. doi:10. 1093/jxb/err072 PMID: 21414963
30. Sage RF, Zhu X-G. Exploiting the engine of C4 photosynthesis. Journal of Experimental Botany. 2011; 62(9):2989-3000. doi: 10.1093/jxb/err179 PMID: 21652533
31. Usadel B, Obayashi T, Mutwil M, Giorgi FM, Bassel GW, Tanimoto M, et al. Co-expression tools for plant biology: opportunities for hypothesis generation and caveats. Plant, cell & environment. 2009; 32 (12):1633-51.
32. Hansen BO, Vaid N, Musialak-Lange M, Janowski M, Mutwil M. Elucidating gene function and function evolution through comparison of co-expression networks of plants. Frontiers in plant science. 2014; 5.
33. Langfelder P, Horvath S. WGCNA: an R package for weighted correlation network analysis. BMC bioinformatics. 2008; 9(1):559.
34. Han X, Yin L, Xue H. Co-expression Analysis Identifies CRC and AP1 the Regulator of Arabidopsis Fatty Acid Biosynthesis. Journal of integrative plant biology. 2012; 54(7):486-99. doi: 10.1111/j.1744-7909.2012.01132.x PMID: 22676405
35. Persson S, Wei H, Milne J, Page GP, Somerville CR. Identification of genes required for cellulose synthesis by regression analysis of public microarray data sets. Proceedings of the National Academy of Sciences of the United States of America. 2005; 102(24):8633-8. PMID: 15932943
36. Ficklin SP, Luo F, Feltus FA. The association of multiple interacting genes with specific phenotypes in rice using gene coexpression networks. Plant physiology. 2010; 154(1):13-24. doi: 10.1104/pp.110. 159459 PMID: 20668062
37. Ficklin SP, Feltus FA. Gene coexpression network alignment and conservation of gene modules between two grass species: maize and rice. Plant Physiology. 2011; 156(3):1244-56. doi: 10.1104/pp. 111.173047 PMID: 21606319
38. Trapnell C, Pachter L, Salzberg SL. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics. 2009; 25(9):1105-11. doi: 10.1093/bioinformatics/btp120 PMID: 19289445
39. Miller JA, Horvath S, Geschwind DH. Divergence of human and mouse brain transcriptome highlights Alzheimer disease pathways. Proceedings of the National Academy of Sciences. 2010; 107 (28):12698-703.
40. Usadel B, Poree F, Nagel A, Lohse M, CZEDIK-EYSENBERG A, Stitt M. A guide to using MapMan to visualize and compare Omics data in plants: a case study in the crop species, Maize. Plant, cell & environment. 2009; 32(9):1211-29.
41. Schnable JC, Freeling M, Lyons E. Genome-wide analysis of syntenic gene deletion in the grasses. Genome biology and evolution. 2012; 4(3):265-77. doi: 10.1093/gbe/evs009 PMID: 22275519
42. Tesson BM, Breitling R, Jansen RC. DiffCoEx: a simple and sensitive method to find differentially coexpressed gene modules. BMC bioinformatics. 2010; 11(1):497.
43. Aubry S, Kelly S, Kümpers BM, Smith-Unna RD, Hibberd JM. Deep Evolutionary Comparison of Gene Expression Identifies Parallel Recruitment of Trans-Factors in Two Independent Origins of C4 Photosynthesis. PLoS genetics. 2014; 10(6):e1004365. doi: 10.1371/journal.pgen.1004365 PMID: 24901697
44. Majeran W, Friso G, Ponnala L, Connolly B, Huang M, Reidel E, et al. Structural and metabolic transitions of C4 leaf development and differentiation defined by microscopy and quantitative proteomics in maize. The Plant Cell Online. 2010; 22(11):3509-42.
45. Niittylä T, Comparot-Moss S, Lue W-L, Messerli G, Trevisan M, Seymour MD, et al. Similar protein phosphatases control starch metabolism in plants and glycogen metabolism in mammals. Journal of Biological Chemistry. 2006; 281(17):11815-8. PMID: 16513634
46. Smith AM, Zeeman SC, Smith SM. Starch degradation. Annu Rev Plant Biol. 2005; 56:73-98. PMID: 15862090
47. Slewinski TL, Meeley R, Braun DM. Sucrose transporter1 functions in phloem loading in maize leaves. Journal of Experimental Botany. 2009; 60(3):881-92. doi: 10.1093/jxb/ern335 PMID: 19181865
48. Bonke M, Thitamadee S, Mähönen AP, Hauser M-T, Helariutta Y. APL regulates vascular tissue identity in Arabidopsis. Nature. 2003; 426(6963):181-6. PMID: 14614507
49. Monson RK. Gene duplication, neofunctionalization, and the evolution of C4 photosynthesis. International Journal of Plant Sciences. 2003; 164(S3):S43-S54.
50. Wang X, Gowik U, Tang H, Bowers JE, Westhoff P, Paterson AH. Comparative genomic analysis of C4 photosynthetic pathway evolution in grasses. Genome Biol. 2009; 10(6):R68. doi: 10.1186/gb-2009-10-6-r68 PMID: 19549309
51. Garfield DA, Wray GA. The evolution of gene regulatory interactions. BioScience. 2010; 60(1):15-23.
52. Ranz JM, Machado CA. Uncovering evolutionary patterns of gene expression using microarrays. Trends in Ecology & Evolution. 2006; 21(1):29-37.
53. Babu MM, Aravind L. Adaptive evolution by optimizing expression levels in different environments. Trends in microbiology. 2006; 14(1):11-4. PMID: 16356718
54. López-Maury L, Marguerat S, Bähler J. Tuning gene expression to changing environments: from rapid responses to evolutionary adaptation. Nature Reviews Genetics. 2008; 9(8):583-93. doi: 10.1038/nrg2398 PMID: 18591982
55. Yamori W, Hikosaka K, Way DA. Temperature response of photosynthesis in C3, C4, and CAM plants: temperature acclimation and temperature adaptation. Photosynthesis research. 2014; 119(1-2):101-17 doi: 10.1007/s11120-013-9874-6 PMID: 23801171
56. Sheen J. Molecular mechanisms underlying the differential expression of maize pyruvate, orthophosphate dikinase genes. The Plant Cell Online. 1991; 3(3):225-45.
57. Studer AJ, Gandin A, Kolbe AR, Wang L, Cousins AB, Brutnell TP. A limited role for carbonic anhydrase in C4 photosynthesis as revealed by a ca1ca2 double mutant in maize. Plant physiology. 2014; 165 (2):608-17. PMID: 24706552
58. Wang Y, Bräutigam A, Weber AP, Zhu X-G. Three distinct biochemical subtypes of C4 photosynthesis? A modelling analysis. Journal of experimental botany. 2014:eru058.
59. Majeran W, van Wijk KJ. Cell-type-specific differentiation of chloroplasts in C4 plants. Trends in plant science. 2009; 14(2):100-9. doi: 10.1016/j.tplants.2008.11.006 PMID: 19162526
60. Weber AP, von Caemmerer S. Plastid transport and metabolism of C3 and C4 plants - comparative analysis and possible biotechnological exploitation. Current opinion in plant biology. 2010; 13(3):256-64.