Genomically biased accumulation of seed storage proteins in allopolyploid cotton

Genetics

Volumn 189, Issue 3, 2011, Pages 1103-1115

  Hu, Guanjing ^a   Houston, Norma L ^b,c   Pathak, Dharminder ^d   Schmidt, Linnea ^e   Thelen, Jay J ^b   Wendel, Jonathan F ^a  

^a IOWA STATE UNIVERSITY   (United States)

^b University of Missouri   (United States)

^c DUPONT COMPANY   (United States)

^d PUNJAB AGRICULTURAL UNIVERSITY   (India)

^e UNIVERSITY OF COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AVENIN; LEGUMIN A; LEGUMIN B; PROTEOME; SEED STORAGE PROTEIN; UNCLASSIFIED DRUG; VICILIN; VICILIN A; VICILIN B;

ALLOPOLYPLOIDY; AMINO ACID SUBSTITUTION; ARTICLE; COTTON; DIPLOIDY; GENE CONTROL; GENE EXPRESSION; GENE SEQUENCE; GENETIC ANALYSIS; GENETIC VARIABILITY; GOSSYPIUM HERBACEUM; GOSSYPIUM HIRSUTUM; GOSSYPIUM RAIMONDII; MOLECULAR PHYLOGENY; NONHUMAN; NUCLEOTIDE SEQUENCE; PLANT GENOME; PLANT SEED; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN MODIFICATION; PROTEOMICS;

DIPLOIDY; GENOME, PLANT; GOSSYPIUM; POLYPLOIDY; PROTEOMICS; SEED STORAGE PROTEINS; SEEDS;

GOSSYPIUM HIRSUTUM;

EID: 81255175641     PISSN: 00166731     EISSN: 19432631     Source Type: Journal    
DOI: 10.1534/genetics.111.132407     Document Type: Article

References (73)

1. Adams, K. L., R. Cronn, R. Percifield, and J. F. Wendel, 2003 Genes duplicated by polyploidy show unequal contributions to the transcriptome and organ-specific reciprocal silencing. Proc. Natl. Acad. Sci. USA 100: 4649-4654.
2. Albertin, W., P. Brabant, O. Catrice, F. Eber, E. Jenczewski et al., 2005 Autopolyploidy in cabbage (Brassica oleracea L.) does not alter significantly the proteomes of green tissues. Proteomics 5: 2131-2139.
3. Albertin, W., T. Balliau, P. Brabant, A. M. Chevre, F. Eber et al., 2006 Numerous and rapid nonstochastic modifications of gene products in newly synthesized Brassica napus allotetraploids. Genetics 173: 1101-1113.
4. Albertin, W., K. Alix, T. Balliau, P. Brabant, M. Davanture et al., 2007 Differential regulation of gene products in newly synthesized Brassica napus allotetraploids is not related to protein function nor subcellular localization. BMC Genomics 8: 56.
5. Anssour, S., T. Krugel, T. F. Sharbel, H. P. Saluz, G. Bonaventure et al., 2009 Phenotypic, genetic and genomic consequences of natural and synthetic polyploidization of Nicotiana attenuata and Nicotiana obtusifolia. Ann. Bot. (Lond.) 103: 1207-1217.
6. Benjamini, Y., and Y. Hochberg, 1995 Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. B 57: 289-300.
7. Bottley, A., and R. M. Koebner, 2008 Variation for homoeologous gene silencing in hexaploid wheat. Plant J. 56: 297-302.
8. Bottley, A., G. M. Xia, and R. M. Koebner, 2006 Homoeologous gene silencing in hexaploid wheat. Plant J. 47: 897-906.
9. Bottley, A., N. H. Chapman, and R. M. Koebner, 2008 Homoeologous gene silencing in tissue cultured wheat callus. BMC Genet. 9: 65.
10. Bourgeois, M., F. Jacquin, V. Savois, N. Sommerer, V. Labas et al., 2009 Dissecting the proteome of pea mature seeds reveals the phenotypic plasticity of seed protein composition. Proteomics 9: 254-271.
11. Bradford, M. M., 1976 Rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72: 248-254.
12. Bressani, R., L. G. Elias, and E. Baham, 1966 Cottonseed protein in human foods, pp. 75-100 in World Protein Resources, edited by A. M. Altschul. American Chemical Society, Washington, DC.
13. Buggs, R. J., A. N. Doust, J. A. Tate, J. Koh, K. Soltis et al., 2009 Gene loss and silencing in Tragopogon miscellus (Asteraceae): comparison of natural and synthetic allotetraploids. Heredity 103: 73-81.
14. Buggs, R. J., S. Chamala, W. Wu, L. Gao, G. D. May et al., 2010 Characterization of duplicate gene evolution in the recent natural allopolyploid Tragopogon miscellus by next-generation sequencing and Sequenom iPLEX MassARRAY genotyping. Mol. Ecol. 19: 132-146.
15. Chaudhary, B., L. Flagel, R. M. Stupar, J. A. Udall, N. Verma et al., 2009 Reciprocal silencing, transcriptional bias and functional divergence of homeologs in polyploid cotton (Gossypium). Genetics 182: 503-517.
16. Chen, Z. J., and C. S. Pikaard, 1997 Transcriptional analysis of nucleolar dominance in polyploid plants: biased expression/ silencing of progenitor rRNA genes is developmentally regulated in Brassica. Proc. Natl. Acad. Sci. USA 94: 3442-3447.
17. Chlan, C. A., J. B. Pyle, A. B. Legocki, and L. Dure, 1986 Developmental biochemistry of cottonseed embryogenesis and germination. XVIII. cDNA and amino acid sequences of members of the storage protein families. Plant Mol. Biol. 7: 475-489.
18. Chlan, C. A., K. Borroto, J. A. Kamalay, and L. Dure, 1987 Developmental biochemistry of cottonseed embryogenesis and germination. XIX. Sequences and genomic organization of the a globulin (vicilin) genes of cottonseed. Plant Mol. Biol. 9: 533-546.
19. Comai, L., 2005 The advantages and disadvantages of being polyploid. Nat. Rev. Genet. 6: 836-846.
20. Cronn, R. C., R. L. Small, T. Haselkorn, and J. F. Wendel, 2002 Rapid diversification of the cotton genus (Gossypium: Malvaceae) revealed by analysis of sixteen nuclear and chloroplast genes. Am. J. Bot. 89: 707-725.
21. Cui, L., P. K. Wall, J. H. Leebens-Mack, B. G. Lindsay, D. E. Soltis et al., 2006 Widespread genome duplications throughout the history of flowering plants. Genome Res. 16: 738-749.
22. Dure, L., 1989 Characteristics of the storage proteins of cotton. J. Am. Oil Chem. Soc. 66: 356-359.
23. Dure, L., and C. Chlan, 1981 Developmental biochemistry of cottonseed embryogenesis and germination: XII. Purification and properties of principal storage proteins. Plant Physiol. 68: 180-186.
24. Dure, L., and G. A. Galau, 1981 Developmental biochemistry of cottonseed embryogenesis and germination: XIII. Regulation of biosynthesis of principle storage proteins. Plant Physiol. 68: 187-194.
25. Dure, L. III. S. C. Greenway, and G. A. Galau, 1981 Developmental biochemistry of cottonseed embryogenesis and germination: changing messenger ribonucleic acid populations as shown by in vitro and in vivo protein synthesis. Biochemistry 20: 4162-4168.
26. Edgar, R. C., 2004 MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32: 1792-1797.
27. Feldman, M., G. Galili, and A. Levy, 1986 Genetic and evolutionary aspects of allopolyploidy in wheat, pp. 88-100 in The Origin and Domestication of Cultivated Plants, edited by C. Barigozzi. Elsevier, Amsterdam.
28. Flagel, L. E., and J. F. Wendel, 2010 Evolutionary rate variation, genomic dominance and duplicate gene expression evolution during allotetraploid cotton speciation. New Phytol. 186: 184-193.
29. Flagel, L., J. Udall, D. Nettleton, and J. Wendel, 2008 Duplicate gene expression in allopolyploid Gossypium reveals two temporally distinct phases of expression evolution. BMC Biol. 6: 16.
30. Flagel, L. E., L. Chen, B. Chaudhary, and J. F. Wendel, 2009 Coordinated and fine-scale control of homoelogous gene expression in allotetraploid cotton. J. Hered. 100: 487-490.
31. Frampton, V., W. Pons, and T. Kerr, 1958 A comparison of chemical properties of seeds of Gossypium species. Econ. Bot. 14: 197-199.
32. Gaeta, R. T., J. C. Pires, F. Iniguez-Luy, E. Leon, and T. C. Osborn, 2007 Genomic changes in resynthesized Brassica napus and their effect on gene expression and phenotype. Plant Cell 19: 3403-3417.
33. Galau, G. A., C. A. Chlan, and L. Dure, 1983 Developmental biochemistry of cottonseed embryogenesis and germination. Plant Mol. Biol. 2: 189-198.
34. Galau, G. A., H. Y. Wang, and D. W. Hughes, 1991 Sequence of the Gossypium hirsutum D-genome alloallele of legumin A and its mRNA. Plant Physiol. 97: 1268-1270.
35. Galau, G. A., H. Y. Wang, and D. W. Hughes, 1992 Cotton Mat5-A (C164) gene and Mat5-D cDNAs encoding methionine-rich 2S albumin storage proteins. Plant Physiol. 99: 779-782.
36. Galili, G., and M. Feldman, 1983 Diploidization of endosperm protein genes in polyploid wheats, pp. 1119-1123 in 6th International Wheat Genetics Symposium, Kyoto, Japan.
37. Grover, C. E., H. Kim, R. A. Wing, A. H. Paterson, and J. F. Wendel, 2004 Incongruent patterns of local and global genome size evolution in cotton. Genome Res. 14: 1474-1482.
38. Grover, C. E., H. Kim, R. A. Wing, A. H. Paterson, and J. F. Wendel, 2007 Microcolinearity and genome evolution in the AdhA region of diploid and polyploid cotton (Gossypium). Plant J. 50: 995-1006.
39. Ha, M., J. Lu, L. Tian, V. Ramachandran, K. D. Kasschau et al., 2009 Small RNAs serve as a genetic buffer against genomic shock in Arabidopsis interspecific hybrids and allopolyploids. Proc. Natl. Acad. Sci. USA 106: 17835-17840.
40. Hajduch, M., A. Ganapathy, J. W. Stein, and J. J. Thelen, 2005 A systematic proteomic study of seed filling in soybean. Establishment of high-resolution two-dimensional reference maps, expression profiles, and an interactive proteome database. Plant Physiol. 137: 1397-1419.
41. Hajduch, M., J. E. Casteel, K. E. Hurrelmeyer, Z. Song, G. K. Agrawal et al., 2006 Proteomic analysis of seed filling in Brassica napus. Developmental characterization of metabolic isozymes using high-resolution two-dimensional gel electrophoresis. Plant Physiol. 141: 32-46.
42. Hajduch, M., J. E. Casteel, S. Tang, L. B. Hearne, S. Knapp et al., 2007 Proteomic analysis of near-isogenic sunflower varieties differing in seed oil traits. J. Proteome Res. 6: 3232-3241.
43. Hajduch, M., L. B. Hearne, J. A. Miernyk, J. E. Casteel, T. Joshi et al., 2010 Systems analysis of seed filling in Arabidopsis: using general linear modeling to assess concordance of transcript and protein expression. Plant Physiol. 152: 2078-2087.
44. Higashi, Y., M. Y. Hirai, T. Fujiwara, S. Naito, M. Noji et al., 2006 Proteomic and transcriptomic analysis of Arabidopsis seeds: molecular evidence for successive processing of seed proteins and its implication in the stress response to sulfur nutrition. Plant J. 48: 557-571.
45. Houston, N. L., M. Hajduch, and J. J. Thelen, 2009 Quantitative proteomics of seed filling in castor: comparison with soybean and rapeseed reveals differences between photosynthetic and nonphotosynthetic seed metabolism. Plant Physiol. 151: 857-868.
46. Hovav, R., J. A. Udall, B. Chaudhary, R. Rapp, L. Flagel et al., 2008 Partitioned expression of duplicated genes during development and evolution of a single cell in a polyploid plant. Proc. Natl. Acad. Sci. USA 105: 6191-6195.
47. Hughes, D. W., and G. A. Galau, 1989 Temporally modular gene expression during cotyledon development. Genes Dev. 3: 358-369.
48. Islam, N., H. Tsujimoto, and H. Hirano, 2003 Proteome analysis of diploid, tetraploid and hexaploid wheat: Towards understanding genome interaction in protein expression. Proteomics 3: 549-557.
49. Jiao, Y., N. J. Wickett, S. Ayyampalayam, A. S. Chanderbali, L. Landherr et al., 2011 Ancestral polyploidy in seed plants and angiosperms. Nature 473: 97-100.
50. Koh, J., P. S. Soltis, and D. E. Soltis, 2010 Homeolog loss and expression changes in natural populations of the recently and repeatedly formed allotetraploid Tragopogon mirus (Asteraceae). BMC Genomics 11: 97.
51. Larre, C., S. Penninck, B. Bouchet, V. Lollier, O. Tranquet et al., 2010 Brachypodium distachyon grain: identification and subcellular localization of storage proteins. J. Exp. Bot. 61: 1771-1783.
52. Ni, Z., E. D. Kim, M. Ha, E. Lackey, J. Liu et al., 2009 Altered circadian rhythms regulate growth vigour in hybrids and allopolyploids. Nature 457: 327-331.
53. Osborne, T. B., 1924 The Vegetable Proteins. Longmans Green & Co., London.
54. Pandey, S., and N. Thejappa, 1975 Study on relationship between oil, protein, and gossypol in cottonseed kernels. J. Am. Oil Chem. Soc. 52: 312-315.
55. Pires, J. C., J. Zhao, M. E. Schranz, E. J. Leon, P. A. Quijada et al., 2004 Flowering time divergence and genomic rearrangements in resynthesized Brassica polyploids (Brassicaceae). Biol. J. Linn. Soc. Lond. 82: 675-688.
56. Pumphrey, M., J. Bai, D. Laudencia-Chingcuanco, O. Anderson, and B. S. Gill, 2009 Nonadditive expression of homoeologous genes is established upon polyploidization in hexaploid wheat. Genetics 181: 1147-1157.
57. Ramsey, J., 2011 Polyploidy and ecological adaptation in wild yarrow. Proc. Natl. Acad. Sci. USA 108: 7096-7101.
58. Rapp, R. A., J. A. Udall, and J. F. Wendel, 2009 Genomic expression dominance in allopolyploids. BMC Biol. 7: 18.
59. Salmon, A., L. Flagel, B. Ying, J. A. Udall, and J. F. Wendel, 2010 Homoeologous nonreciprocal recombination in polyploid cotton. New Phytol. 186: 123-134.
60. Schnable, J. C., N. M. Springer, and M. Freeling, 2011 Differentiation of the maize subgenomes by genome dominance and both ancient and ongoing gene loss. Proc. Natl. Acad. Sci. USA 108: 4069-4074.
61. Senchina, D. S., I. Alvarez, R. C. Cronn, B. Liu, J. Rong et al., 2003 Rate variation among nuclear genes and the age of polyploidy in Gossypium. Mol. Biol. Evol. 20: 633-643.
62. Shaked, H., K. Kashkush, H. Ozkan, M. Feldman, and A. A. Levy, 2001 Sequence elimination and cytosine methylation are rapid and reproducible responses of the genome to wide hybridization and allopolyploidy in wheat. Plant Cell 13: 1749-1759.
63. Shewry, P. R., J. A. Napier, and A. S. Tatham, 1995 Seed storage proteins: structures and biosynthesis. Plant Cell 7: 945-956.
64. Sunilkumar, G., L. M. Campbell, L. Puckhaber, R. D. Stipanovic, and K. S. Rathore, 2006 Engineering cottonseed for use in human nutrition by tissue-specific reduction of toxic gossypol. Proc. Natl. Acad. Sci. USA 103: 18054-18059.
65. Swofford, D. L., 2001 PAUP* Phylogenetic Analysis Using Parsimony and Other Methods, Version 4. Sinauer Associates, Sunderland, MA.
66. Udall, J. A., J. M. Swanson, K. Haller, R. A. Rapp, M. E. Sparks et al., 2006a A global assembly of cotton ESTs. Genome Res. 16: 441-450.
67. Udall, J. A., J. M. Swanson, D. Nettleton, R. J. Percifield, and J. F. Wendel, 2006b A novel approach for characterizing expression levels of genes duplicated by polyploidy. Genetics 173: 1823-1827.
68. Wang, J., L. Tian, H. S. Lee, N. E. Wei, H. Jiang et al., 2006 Genomewide nonadditive gene regulation in Arabidopsis allotetraploids. Genetics 172: 507-517.
69. Wendel, J. F., 2000 Genome evolution in polyploids. Plant Mol. Biol. 42: 225-249.
70. Wendel, J. F., and R. C. Cronn, 2003 Polyploidy and the evolutionary history of cotton, pp. 139-186 in Advances in Agronomy. Academic Press, New York/London/San Diego.
71. Wendel, J. F., A. Schnabel, and T. Seelanan, 1995 Bidirectional interlocus concerted evolution following allopolyploid speciation in cotton (Gossypium). Proc. Natl. Acad. Sci. USA 92: 280-284.
72. Youle, R. J., and A. H. Huang, 1979 Albumin storage protein and allergens in cottonseeds. J. Agric. Food Chem. 27: 500-503.
73. Youle, R. J., and A. H. C. Huang, 1981 Occurrence of low molecular weight and high cysteine containing albumin storage proteins in oilseeds of diverse species. Am. J. Bot. 68: 5.