Expression quantitative trait loci analysis of two genes encoding Rubisco activase in soybean

Plant Physiology

Volumn 152, Issue 3, 2010, Pages 1625-1637

  Yin, Zhitong ^a,b   Meng, Fanfan ^a   Song, Haina ^a   Wang, Xiaolin ^a   Xu, Xiaoming ^a   Yu, Deyue ^a  

^a NANJING AGRICULTURAL UNIVERSITY   (China)

^b Jiangsu Yanjiang Institute of Agricultural Sciences   (China)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCINE MAX;

EID: 77949507800     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.109.148312     Document Type: Article

References (70)

1. Adams KL, Wendel JF (2005) Polyploidy and genome evolution in plants. Curr Opin Plant Biol 8: 135-141
2. Ayala-Ochoa A, Vargas-Suaez M, Loza-Tavera H, Leon P, Jimenez-Garcia LF, Sanchez-de-Jimenez E (2004) In maize, two distinct ribulose 1,5-bisphosphate carboxylase/oxygenase activase transcripts have different day/night patterns of expression. Biochimie 86: 439-449
3. Blanc G, Wolfe KH (2004) Widespread paleopolyploidy in model plant species inferred from age distributions of duplicate genes. Plant Cell 16: 1667-1678
4. Chen H, Cui S, Fu S, Gai J, Yu D (2008) Identification of quantitative trait loci associated with salt tolerance during seedling growth in soybean (Glycine max L.). Aust J Agric Res 59: 1086-1091
5. Chen K, Rajewsky N (2007) The evolution of gene regulation by transcription factors and microRNAs. Nat Rev Genet 8: 93-103
6. Churchill GA, Doerge RW (1994) Empirical threshold values for quantitative trait mapping. Genetics 138: 963-971
7. Crafts-Brandner SJ, Salvucci ME (2000) Rubisco activase constrains the photosynthetic potential of leaves at high temperature and CO2. Proc Natl Acad Sci USA 97: 13430-13435
8. Cui S, He X, Fu S, Meng Q, Gai J, Yu D (2008) Genetic dissection of the relationship of apparent biological yield and apparent harvest index with seed yield and yield related traits in soybean. Aust J Agric Res 59: 86-93
9. Doyle JJ, Flagel LE, Paterson AH, Rapp RA, Soltis DE, Soltis PS, Wendel JF (2008) Evolutionary genetics of genome merger and doubling in plants. Annu Rev Genet 42: 443-461
10. Eckardt NA, Snyder GW, Portis AR Jr, Ogren WL (1997) Growth and photosynthesis under high and low irradiance of Arabidopsis thaliana antisense mutants with reduced ribulose-1,5-bisphosphate carboxylase/oxygenase activase content. Plant Physiol 113: 575-586
11. Fling SP, Gregerson DS (1986) Peptide and protein molecular weight determination by electrophoresis using a high-molarity Tris buffer system without urea. Anal Biochem 155: 83-88
12. Fu S, Zhan Y, Zhi H, Gai J, Yu D (2006) Mapping of SMV resistance gene Rsc-7 by SSR markers in soybean. Genetica 128: 63-69
13. Hartman FC, Harpel MR (1994) Structure, function, regulation, and assembly of D-ribulose-1,5-bisphosphate carboxylase/oxygenase. Annu Rev Biochem 63: 197-234
14. He Z, von Caemmerer S, Hudson GS, Price GD, Badger MR, Andrews TJ (1997) Ribulose-1,5-bisphosphate carboxylase/oxygenase activase deficiency delays senescence of ribulose-1,5-bisphosphate carboxylase/oxygenase but progressively impairs its catalysis during tobacco leaf development. Plant Physiol 115: 1569-1580
15. Hendrickson L, Sharwood R, Ludwig M, Whitney SM, Badger MR, von Caemmerer S (2008) The effects of Rubisco activase on C4 photosynthesis and metabolism at high temperature. J Exp Bot 59: 1789-1798
16. Jansen RC, Nap JP (2001) Genetical genomics: the added value from segregation. Trends Genet 17: 388-391
17. Kim K, Portis AR Jr (2005) Temperature dependence of photosynthesis in Arabidopsis plants with modifications in Rubisco activase and membrane fluidity. Plant Cell Physiol 46: 522-530
18. Kirst M, Myburg AA, De Leon JPG, Kirst ME, Scott J, Sederoff R (2004) Coordinated genetic regulation of growth and lignin revealed by quantitative trait locus analysis of cDNA microarray data in an interspecific backcross of eucalyptus. Plant Physiol 135: 2368-2378
19. Kumar S, Nei M, Dudley J, Tamura K (2008) MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences. Brief Bioinform 9: 299-306
20. Kurek I, Chang TK, Bertain SM, Madrigal A, Liu L, Lassner MW, Zhu G (2007) Enhanced thermostability of Arabidopsis Rubisco activase improves photosynthesis and growth rates under moderate heat stress. Plant Cell 19: 3230-3241
21. Law RD, Crafts-Brandner SJ (2001) High temperature stress increases the expression of wheat leaf ribulose-1,5-bisphosphate carboxylase/ oxygenase activase protein. Arch Biochem Biophys 386: 261-267
22. Liu Z, Taub CC, McClung CR (1996) Identification of an Arabidopsis thaliana ribulose-1,5-bisphosphate carboxylase/oxygenase activase (RCA) minimal promoter regulated by light and the circadian clock. Plant Physiol 112: 43-51
23. Martino-Catt S, Ort DR (1992) Low temperature interrupts circadian regulation of transcriptional activity in chilling-sensitive plants. Proc Natl Acad Sci USA 89: 3731-3735
24. Mate CJ, Caemmerer S, Evans JR, Hudson GS, Andrews TJ (1996) The relationship between CO2-assimilation rate, Rubisco carbamylation and Rubisco activase content in activase-deficient transgenic tobacco suggests a simple model of activase action. Planta 198: 604-613
25. Mate CJ, Hudson GS, von Caemmerer S, Evans JR, Andrews TJ (1993) Reduction of ribulose bisphosphate carboxylase activase levels in tobacco (Nicotiana tabacum) by antisense RNA reduces ribulose bisphosphate carboxylase carbamylation and impairs photosynthesis. Plant Physiol 102: 1119-1128
26. Mouille G, Witucka-Wall H, Bruyant MP, Loudet O, Pelletier S, Rihouey C, Lerouxel O, Lerouge P, Hofte H, Pauly M (2006) Quantitative trait loci analysis of primary cell wall composition in Arabidopsis. Plant Physiol 141: 1035-1044
27. Pilgrim ML, McClung CR (1993) Differential involvement of the circadian clock in the expression of genes required for ribulose-1,5-bisphosphate carboxylase/oxygenase synthesis, assembly, and activation in Arabidopsis thaliana. Plant Physiol 103: 553-564
28. Pollock SV, Colombo SL, Prout DL Jr, Godfrey AC, Moroney JV (2003) Rubisco activase is required for optimal photosynthesis in the green alga Chlamydomonas reinhardtii in a low-CO2 atmosphere. Plant Physiol 133: 1854-1861
29. Portis A (2003) Rubisco activase: Rubisco's catalytic chaperone. Photosynth Res 75: 11-27
30. Portis AR Jr, Li C, Wang D, Salvucci ME (2008) Regulation of Rubisco activase and its interaction with Rubisco. J Exp Bot 59: 1597-1604
31. Potokina E, Prasad M, Malysheva L, Roder M, Graner A (2006) Expression genetics and haplotype analysis reveal cis regulation of serine carboxypeptidase I (Cxp1), a candidate gene for malting quality in barley (Hordeum vulgare L.). Funct Integr Genomics 6: 25-35
32. Qian J, Rodermel SR (1993) Ribulose-1,5-bisphosphate carboxylase/oxygenase activase cDNAs from Nicotiana tabacum. Plant Physiol 102: 683-684
33. Rundle S, Zielinski R (1991) Organization and expression of two tandemly oriented genes encoding ribulosebisphosphate carboxylase/oxygenase activase in barley. J Biol Chem 266: 4677-4685
34. Salvucci M, Portis A, Ogren W (1985) A soluble chloroplast protein catalyzes ribulosebisphosphate carboxylase/oxygenase activation in vivo. Photosynth Res 7: 193-201
35. Salvucci M, van de Loo F, Stecher D (2003) Two isoforms of Rubisco activase in cotton, the products of separate genes not alternative splicing. Planta 216: 736-744
36. Salvucci ME (2008) Association of Rubisco activase with chaperonin-60b: a possible mechanism for protecting photosynthesis during heat stress. J Exp Bot 59: 1923-1933
37. Salvucci ME, Crafts-Brandner SJ (2004) Relationship between the heat tolerance of photosynthesis and the thermal stability of Rubisco activase in plants from contrasting thermal environments. Plant Physiol 134: 1460-1470
38. Salvucci ME, DeRidder BP, Portis AR Jr (2006) Effect of activase level and isoform on the thermotolerance of photosynthesis in Arabidopsis. J Exp Bot 57: 3793-3799
39. Salvucci ME, Portis AR Jr, Ogren WL (1986) Light and CO2 response of ribulose-1,5-bisphosphate carboxylase/oxygenase activation in Arabidopsis leaves. Plant Physiol 80: 655-659
40. Salvucci ME, Werneke JM, Ogren WL, Portis AR Jr (1987) Purification and species distribution of Rubisco activase. Plant Physiol 84: 930-936
41. Sanchez de Jimenez E, Medrano L, Martinez-Barajas E (1995) Rubisco activase, a possible new member of the molecular chaperone family. Biochemistry 34: 2826-2831
42. Schlueter JA, Dixon P, Granger C, Grant D, Clark L, Doyle JJ, Shoemaker RC (2004) Mining EST databases to resolve evolutionary events in major crop species. Genome 47: 868-876
43. Shen J, Orozco E Jr, Ogren W (1991) Expression of the two isoforms of spinach ribulose 1,5-bisphosphate carboxylase activase and essentiality of the conserved lysine in the consensus nucleotide-binding domain. J Biol Chem 266: 8963-8968
44. Shen JB, Ogren WL (1992) Alteration of spinach ribulose-1,5-bisphosphate carboxylase/oxygenase activase activities by site-directed mutagenesis. Plant Physiol 99: 1201-1207
45. Shoemaker RC, Schlueter J, Doyle JJ (2006) Paleopolyploidy and gene duplication in soybean and other legumes. Curr Opin Plant Biol 9: 104-109
46. Sinclair TR, Purcell LC, Sneller CH (2004) Crop transformation and the challenge to increase yield potential. Trends Plant Sci 9: 70-75
47. Sladek R, Hudson TJ (2006) Elucidating cisand trans-regulatory variation using genetical genomics. Trends Genet 22: 245-250
48. Somerville CR, Portis AR Jr, Ogren WL (1982) A mutant of Arabidopsis thaliana which lacks activation of RuBP carboxylase in vivo. Plant Physiol 70: 381-387
49. Song Q, Marek L, Shoemaker R, Lark K, Concibido V, Delannay X, Specht J, Cregan P (2004) A new integrated genetic linkage map of the soybean. Theor Appl Genet 109: 122-128
50. Spreitzer RJ, Salvucci ME (2002) Rubisco: structure, regulatory interactions, and possibilities for a better enzyme. Annu Rev Plant Biol 53: 449-475
51. Sulpice R, Tschoep H, Korff M, Bussis D, Usadel B, Hohne M, Witucka-Wall IH, Altmann T, Stitt M, Gibon IY (2007) Description and applications of a rapid and sensitive non-radioactive microplate-based assay for maximum and initial activity of D-ribulose-1,5-bisphosphate carboxylase/oxygenase. Plant Cell Environ 30: 1163-1175
52. Thumma BR, Naidu BP, Chandra A, Cameron DF, Bahnisch LM, Liu C (2001) Identification of causal relationships among traits related to drought resistance in Stylosanthes scabra using QTL analysis. J Exp Bot 52: 203-214
53. Tisne S, Reymond M, Vile D, Fabre J, Dauzat M, Koornneef M, Granier C (2008) Combined genetic and modeling approaches reveal that epidermal cell area and number in leaves are controlled by leaf and plant developmental processes in Arabidopsis. Plant Physiol 148: 1117-1127
54. To KY, Suen DF, Chen SCG (1999) Molecular characterization of ribulose-1,5-bisphosphate carboxylase/oxygenase activase in rice leaves. Planta 209: 66-76
55. van de Loo FJ, Salvucci ME (1996) Activation of ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) involves Rubisco activase Trp16. Biochemistry 35: 8143-8148
56. van de Loo FJ, Salvucci ME (1998) Involvement of two aspartate residues of Rubisco activase in coordination of the ATP g-phosphate and subunit cooperativity. Biochemistry 37: 4621-4625
57. von Caemmerer S, Hendrickson L, Quinn V, Vella N, Millgate AG, Furbank RT (2005) Reductions of Rubisco activase by antisense RNA in the C4 plant Flaveria bidentis reduces Rubisco carbamylation and leaf photosynthesis. Plant Physiol 137: 747-755
58. Wang SC, Basten CJ, Zeng ZB (2005) Windows QTL Cartographer v2.5. Department of Statistics, North Carolina State University, Raleigh, NC
59. Watillon B, Kettmann R, Boxus P, Burny A (1993) Developmental and circadian pattern of Rubisco activase mRNA accumulation in apple plants. Plant Mol Biol 23: 501-509
60. Weising K, Atkinson RG, Gardner RC (1995) Genomic fingerprinting by microsatellite-primed PCR: a critical evaluation. PCR Methods Appl 4: 249-255
61. Wendel JF (2000) Genome evolution in polyploids. Plant Mol Biol 42: 225-249
62. Werneke JM, Chatfield JM, Ogren WL (1989) Alternative mRNA splicing generates the two ribulosebisphosphate carboxylase/oxygenase activase polypeptides in spinach and Arabidopsis. Plant Cell 1: 815-825
63. Werneke JM, Zielinski RE, Ogren WL (1988) Structure and expression of spinach leaf cDNA encoding ribulosebisphosphate carboxylase/ oxygenase activase. Proc Natl Acad Sci USA 85: 787-791
64. Weston DJ, Bauerle WL, Swire-Clark GA, Moore BD, Baird WV (2007) Characterization of Rubisco activase from thermally contrasting genotypes of Acer rubrum (Aceraceae). Am J Bot 94: 926-934
65. Wu H, Ding Z, Li L, Jing Y, Kuang T (2006) Expression of the large isoform of ribulose-1,5-bisphosphate carboxylase/oxygenase activase gene driven by rbcS promoter in Oryza sativa enhances the photosynthetic capacity. Photosynthetica 44: 208-214
66. Wu H, Li L, Jing Y, Kuang T (2007) Over-and anti-sense expressions of the large isoform of ribulose-1,5-bisphosphate carboxylase/oxygenase activase gene in Oryza sativa affect the photosynthetic capacity. Photosynthetica 45: 194-201
67. Xu Y (1997) Quantitative trait loci, separating, pyramiding, and cloning. Plant Breed Rev 15: 85-139
68. Zhang N, Kallis RP, Ewy RG, Portis AR (2002) Light modulation of Rubisco in Arabidopsis requires a capacity for redox regulation of the larger Rubisco activase isoform. Proc Natl Acad Sci USA 99: 3330-3334
69. Zhang N, Portis AR (1999) Mechanism of light regulation of Rubisco: a specific role for the larger Rubisco activase isoform involving reductive activation by thioredoxin-f. Proc Natl Acad Sci USA 96: 9438-9443
70. Zhang XC, Wu X, Findley S, Wan J, Libault M, Nguyen HT, Cannon SB, Stacey G (2007) Molecular evolution of lysin motif-type receptor-like kinases in plants. Plant Physiol 144: 623-636