Extensive translational regulation of gene expression in an allopolyploid (Glycine dolichocarpa)

Plant Cell

Volumn 26, Issue 1, 2014, Pages 136-150

  Coate, Jeremy E ^a   Bar, Haim ^b   Doyle, Jeff J ^c  

^a REED COLLEGE   (United States)

^b Plant Breeding and Genetics Section in the School of Integrative Plant Science   (United States)

^c Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTOME;

FABACEAE; GENE EXPRESSION REGULATION; GENETICS; POLYPLOIDY; PROTEIN SYNTHESIS;

FABACEAE; GENE EXPRESSION REGULATION, PLANT; POLYPLOIDY; PROTEIN BIOSYNTHESIS; TRANSCRIPTOME;

EID: 84896843137     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.113.119966     Document Type: Article

References (81)

1. Adams, K.L., Cronn, R., Percifield, R., and Wendel, J.F. (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. Adams, K.L., and Wendel, J.F. (2005). Polyploidy and genome evolution in plants. Curr. Opin. Plant Biol. 8: 135-141.
3. Albertin, W., Alix, K., Balliau, T., Brabant, P., Davanture, M., Malosse, C., Valot, B., and Thiellement, H. (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.
4. Albertin, W., Balliau, T., Brabant, P., Chèvre, A.M., Eber, F., Malosse, C., and Thiellement, H. (2006). Numerous and rapid nonstochastic modifications of gene products in newly synthesized Brassica napus allotetraploids. Genetics 173: 1101-1113.
5. Anders, S., and Huber, W. (2010). Differential expression analysis for sequence count data. Genome Biol. 11: R106.
6. Bekaert, M., Edger, P.P., Pires, J.C., and Conant, G.C. (2011). Twophase resolution of polyploidy in the Arabidopsis metabolic network gives rise to relative and absolute dosage constraints. Plant Cell 23: 1719-1728.
7. Birchler, J.A., and Veitia, R.A. (2010). The gene balance hypothesis: Implications for gene regulation, quantitative traits and evolution. New Phytol. 186: 54-62.
8. Birchler, J.A., Yao, H., and Chudalayandi, S. (2007). Biological consequences of dosage dependent gene regulatory systems. Biochim. Biophys. Acta 1769: 422-428.
9. Blanc, G., and Wolfe, K.H. (2004a). Widespread paleopolyploidy in model plant species inferred from age distributions of duplicate genes. Plant Cell 16: 1667-1678.
10. Blanc, G., and Wolfe, K.H. (2004b). Functional divergence of duplicated genes formed by polyploidy during Arabidopsis evolution. Plant Cell 16: 1679-1691.
11. Bowers, J.E., Chapman, B.A., Rong, J.K., and Paterson, A.H. (2003). Unravelling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events. Nature 422: 433-438.
12. Branco-Price, C., Kaiser, K.A., Jang, C.J.H., Larive, C.K., and Bailey-Serres, J. (2008). Selective mRNA translation coordinates energetic and metabolic adjustments to cellular oxygen deprivation and reoxygenation in Arabidopsis thaliana. Plant J. 56: 743-755.
13. Branco-Price, C., Kawaguchi, R., Ferreira, R.B., and Bailey-Serres, J. (2005). Genome-wide analysis of transcript abundance and translation in Arabidopsis seedlings subjected to oxygen deprivation. Ann. Bot. (Lond.) 96: 647-660.
14. Buggs, R.J.A., Chamala, S., Wu, W., Gao, L., May, G.D., Schnable, P.S., Soltis, D.E., Soltis, P.S., and Barbazuk, W.B. (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 (suppl. 1): 132-146.
15. Chang, S., Hartman, G.L., Singh, R.J., Lambert, K.N., Hobbs, H.A., and Domier, L.L. (2013). Identification of high-quality singlenucleotide polymorphisms in Glycine latifolia using a heterologous reference genome sequence. Theor. Appl. Genet. 126: 1627-1638.
16. Coate, J.E., and Doyle, J.J. (2013). Genomics and transcriptomics of photosynthesis in polyploids. In Polyploid and Hybrid Genomics, Z.J. Chen and J.A. Birchler, eds (Hoboken, NJ: Wiley-Blackwell), pp. 153-169.
17. Coate, J.E., and Doyle, J.J. (2010). Quantifying whole transcriptome size, a prerequisite for understanding transcriptome evolution across species: An example from a plant allopolyploid. Genome Biol. Evol. 2: 534-546.
18. Coate, J.E., Luciano, A.K., Seralathan, V., Minchew, K.J., Owens, T.G., and Doyle, J.J. (2012). Anatomical, biochemical, and photosynthetic responses to recent allopolyploidy in Glycine dolichocarpa (Fabaceae). Am. J. Bot. 99: 55-67.
19. Coate, J.E., Powell, A.F., Owens, T.G., and Doyle, J.J. (2013). Transgressive physiological and transcriptomic responses to light stress in allopolyploid Glycine dolichocarpa (Leguminosae). Heredity (Edinb) 110: 160-170.
20. Coate, J.E., Schlueter, J.A., Whaley, A.M., and Doyle, J.J. (2011). Comparative evolution of photosynthetic genes in response to polyploid and nonpolyploid duplication. Plant Physiol. 155: 2081-2095.
21. Conant, G.C., and Wolfe, K.H. (2007). Increased glycolytic flux as an outcome of whole-genome duplication in yeast. Mol. Syst. Biol. 3: 129.
22. Doyle, J.J., Doyle, J.L., Rauscher, J.T., and Brown, A.H.D. (2004). Evolution of the perennial soybean polyploid complex (Glycine subgenus Glycine): A study of contrasts. Biol. J. Linn. Soc. Lond. 82: 583-597.
23. Doyle, J.J., and Egan, A.N. (2010). Dating the origins of polyploidy events. New Phytol. 186: 73-85.
24. Du, J., Tian, Z., Sui, Y., Zhao, M., Song, Q., Cannon, S.B., Cregan, P., and Ma, J. (2012). Pericentromeric effects shape the patterns of divergence, retention, and expression of duplicated genes in the paleopolyploid soybean. Plant Cell 24: 21-32.
25. Du, Z., Zhou, X., Ling, Y., Zhang, Z., and Su, Z. (2010). agriGO: A GO analysis toolkit for the agricultural community. Nucleic Acids Res. 38: W64-W70.
26. Fawcett, J.A., Maere, S., and Van de Peer, Y. (2009). Plants with double genomes might have had a better chance to survive the Cretaceous-Tertiary extinction event. Proc. Natl. Acad. Sci. USA 106: 5737-5742.
27. Flagel, L., Udall, J., Nettleton, D., and Wendel, J. (2008). Duplicate gene expression in allopolyploid Gossypium reveals two temporally distinct phases of expression evolution. BMC Biol. 6: 16.
28. Flagel, L.E., Chen, L., Chaudhary, B., and Wendel, J.F. (2009). Coordinated and fine-scale control of homoeologous gene expression in allotetraploid cotton. J. Hered. 100: 487-490.
29. Freeling, M. (2009). Bias in plant gene content following different sorts of duplication: Tandem, whole-genome, segmental, or by transposition. Annu. Rev. Plant Biol. 60: 433-453.
30. Freeling, M., and Thomas, B.C. (2006). Gene-balanced duplications, like tetraploidy, provide predictable drive to increase morphological complexity. Genome Res. 16: 805-814.
31. Freeling, M., Woodhouse, M.R., Subramaniam, S., Turco, G., Lisch, D., and Schnable, J.C. (2012). Fractionation mutagenesis and similar consequences of mechanisms removing dispensable or less-expressed DNA in plants. Curr. Opin. Plant Biol. 15: 131-139.
32. Grover, C.E., Gallagher, J.P., Szadkowski, E.P., Yoo, M.J., Flagel, L.E., and Wendel, J.F. (2012). Homoeolog expression bias and expression level dominance in allopolyploids. New Phytol. 196: 966-971.
33. Guo, M., Davis, D., and Birchler, J.A. (1996). Dosage effects on gene expression in a maize ploidy series. Genetics 142: 1349-1355.
34. Hegarty, M.J., Barker, G.L., Brennan, A.C., Edwards, K.J., Abbott, R.J., and Hiscock, S.J. (2008). Changes to gene expression associated with hybrid speciation in plants: Further insights from transcriptomic studies in Senecio. Philos. Trans. R. Soc. Lond. B Biol. Sci. 363: 3055-3069.
35. Hsieh, A.C., et al. (2012). The translational landscape of mTOR signalling steers cancer initiation and metastasis. Nature 485: 55-61.
36. Hu, G., Houston, N.L., Pathak, D., Schmidt, L., Thelen, J.J., and Wendel, J.F. (2011). Genomically biased accumulation of seed storage proteins in allopolyploid cotton. Genetics 189: 1103-1115.
37. Hu, G., Koh, J., Yoo, M.J., Grupp, K., Chen, S., and Wendel, J.F. (2013). Proteomic profiling of developing cotton fibers from wild and domesticated Gossypium barbadense. New Phytol. 200: 570-582.
38. Hudson, C.M., Puckett, E.E., Bekaert, M., Pires, J.C., and Conant, G.C. (2011). Selection for higher gene copy number after different types of plant gene duplications. Genome Biol. Evol. 3: 1369-1380.
39. Ilut, D.C., Coate, J.E., Luciano, A.K., Owens, T.G., May, G.D., Farmer, A.D., and Doyle, J.J. (2012). A comparative transcriptomic study of an allotetraploid and its diploid progenitors illustrates the unique advantages and challenges of RNA-seq in plant species. Am. J. Bot. 99: 383-396.
40. Innes, R.W., et al. (2008). Differential accumulation of retroelements and diversification of NB-LRR disease resistance genes in duplicated regions following polyploidy in the ancestor of soybean. Plant Physiol. 148: 1740-1759.
41. Ishihama, Y., Schmidt, T., Rappsilber, J., Mann, M., Hartl, F.U., Kerner, M.J., and Frishman, D. (2008). Protein abundance profiling of the Escherichia coli cytosol. BMC Genomics 9: 102.
42. Jiang, W., Liu, Y., Xia, E., and Gao, L. (2013). Prevalent role of gene features in determining evolutionary fates of whole-genome duplication duplicated genes in flowering plants. Plant Physiol. 161: 1844-1861.
43. Jiao, Y., et al. (2011). Ancestral polyploidy in seed plants and angiosperms. Nature 473: 97-100.
44. Jiao, Y., et al. (2012). A genome triplication associated with early diversification of the core eudicots. Genome Biol. 13: R3.
45. Jiao, Y., and Meyerowitz, E.M. (2010). Cell-type specific analysis of translating RNAs in developing flowers reveals new levels of control. Mol. Syst. Biol. 6: 419.
46. Joshi, A., Van de Peer, Y., and Michoel, T. (2011). Structural and functional organization of RNA regulons in the post-transcriptional regulatory network of yeast. Nucleic Acids Res. 39: 9108-9117.
47. Juntawong, P., and Bailey-Serres, J. (2012). Dynamic light regulation of translation status in Arabidopsis thaliana. Front. Plant Sci. 3: 66.
48. Kawaguchi, R., and Bailey-Serres, J. (2002). Regulation of translational initiation in plants. Curr. Opin. Plant Biol. 5: 460-465.
49. Kawaguchi, R., Girke, T., Bray, E.A., and Bailey-Serres, J. (2004). Differential mRNA translation contributes to gene regulation under non-stress and dehydration stress conditions in Arabidopsis thaliana. Plant J. 38: 823-839.
50. Keene, J.D. (2007). RNA regulons: Coordination of post-transcriptional events. Nat. Rev. Genet. 8: 533-543.
51. Khan, Z., Bloom, J.S., Amini, S., Singh, M., Perlman, D.H., Caudy, A.A., and Kruglyak, L. (2012). Quantitative measurement of allelespecific protein expression in a diploid yeast hybrid by LC-MS. Mol. Syst. Biol. 8: 602.
52. Koh, J., Chen, S., Zhu, N., Yu, F., Soltis, P.S., and Soltis, D.E. (2012). Comparative proteomics of the recently and recurrently formed natural allopolyploid Tragapogon mirus (Asteraceae) and its parents. New Phytol. 196: 292-305.
53. Langmead, B., Trapnell, C., Pop, M., and Salzberg, S.L. (2009). Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10: R25.
54. Levin, D.A. (1983). Poly ploidy and novelty in flowering plants. Am. Nat. 122: 1-25.
55. Lin, J.Y., Stupar, R.M., Hans, C., Hyten, D.L., and Jackson, S.A. (2010). Structural and functional divergence of a 1-Mb duplicated region in the soybean (Glycine max) genome and comparison to an orthologous region from Phaseolus vulgaris. Plant Cell 22: 2545-2561.
56. Lynch, M., and Conery, J.S. (2000). The evolutionary fate and consequences of duplicate genes. Science 290: 1151-1155.
57. Lynch, M., and Conery, J.S. (2003). The evolutionary demography of duplicate genes. J. Struct. Funct. Genomics 3: 35-44.
58. Maere, S., De Bodt, S., Raes, J., Casneuf, T., Van Montagu, M., Kuiper, M., and Van de Peer, Y. (2005). Modeling gene and genome duplications in eukaryotes. Proc. Natl. Acad. Sci. USA 102: 5454-5459.
59. Marguerat, S., Schmidt, A., Codlin, S., Chen, W., Aebersold, R., and Bähler, J. (2012). Quantitative analysis of fission yeast transcriptomes and proteomes in proliferating and quiescent cells. Cell 151: 671-683.
60. Mustroph, A., and Bailey-Serres, J. (2010). The Arabidopsis translatome cell-specific mRNA atlas: Mining suberin and cutin lipid monomer biosynthesis genes as an example for data application. Plant Signal. Behav. 5: 320-324.
61. Mustroph, A., Zanetti, M.E., Jang, C.J.H., Holtan, H.E., Repetti, P.P., Galbraith, D.W., Girke, T., and Bailey-Serres, J. (2009). Profiling translatomes of discrete cell populations resolves altered cellular priorities during hypoxia in Arabidopsis. Proc. Natl. Acad. Sci. USA 106: 18843-18848.
62. Ni, Z., Kim, E.D., Ha, M., Lackey, E., Liu, J., Zhang, Y., Sun, Q., and Chen, Z.J. (2009). Altered circadian rhythms regulate growth vigour in hybrids and allopolyploids. Nature 457: 327-331.
63. Papp, B., Pál, C., and Hurst, L.D. (2003). Dosage sensitivity and the evolution of gene families in yeast. Nature 424: 194-197.
64. Park, S.H., Chung, P.J., Juntawong, P., Bailey-Serres, J., Kim, Y.S., Jung, H., Bang, S.W., Kim, Y.K., Do Choi, Y., and Kim, J.K. (2012). Posttranscriptional control of photosynthetic mRNA decay under stress conditions requires 39 and 59 untranslated regions and correlates with differential polysome association in rice. Plant Physiol. 159: 1111-1124.
65. Paterson, A.H., Chapman, B.A., Kissinger, J.C., Bowers, J.E., Feltus, F.A., and Estill, J.C. (2006). Many gene and domain families have convergent fates following independent whole-genome duplication events in Arabidopsis, Oryza, Saccharomyces and Tetraodon. Trends Genet. 22: 597-602.
66. Pires, J.C., Zhao, J., Schranz, M.E., Leon, E.J., Quijada, P.A., Lukens, L.N., and Osborn, T.C. (2004). Flowering time divergence and genomic rearrangements in resynthesized Brassica polyploids (Brassicaceae). Biol. J. Linn. Soc. Lond. 82: 675-688.
67. Reynoso, M.A., Blanco, F.A., Bailey-Serres, J., Crespi, M., and Zanetti, M.E. (2012). Selective recruitment of mRNAs and miRNAs to polyribosomes in response to rhizobia infection in Medicago truncatula. Plant J. 73: 289-301.
68. Schlueter, J.A., Dixon, P., Granger, C., Grant, D., Clark, L., Doyle, J.J., and Shoemaker, R.C. (2004). Mining EST databases to resolve evolutionary events in major crop species. Genome 47: 868-876.
69. Schmutz, J., et al. (2010). Genome sequence of the palaeopolyploid soybean. Nature 463: 178-183.
70. Schnable, J.C., Springer, N.M., and Freeling, M. (2011). Differentiation of the maize subgenomes by genome dominance and both ancient and ongoing gene loss. Proc. Natl. Acad. Sci. USA 108: 4069-4074.
71. Schwanhäusser, B., Busse, D., Li, N., Dittmar, G., Schuchhardt, J., Wolf, J., Chen, W., and Selbach, M. (2011). Global quantification of mammalian gene expression control. Nature 473: 337-342.
72. Seoighe, C., and Gehring, C. (2004). Genome duplication led to highly selective expansion of the Arabidopsis thaliana proteome. Trends Genet. 20: 461-464.
73. Shoemaker, R.C., Schlueter, J., and Doyle, J.J. (2006). Paleopolyploidy and gene duplication in soybean and other legumes. Curr. Opin. Plant Biol. 9: 104-109.
74. Sonenberg, N., and Hinnebusch, A.G. (2009). Regulation of translation initiation in eukaryotes: Mechanisms and biological targets. Cell 136: 731-745.
75. Tang, H., Wang, X., Bowers, J.E., Ming, R., Alam, M., and Paterson, A.H. (2008). Unraveling ancient hexaploidy through multiply-aligned angiosperm gene maps. Genome Res. 18: 1944-1954.
76. Thomas, B.C., Pedersen, B., and Freeling, M. (2006). Following tetraploidy in an Arabidopsis ancestor, genes were removed preferentially from one homeolog leaving clusters enriched in dosesensitive genes. Genome Res. 16: 934-946.
77. Vogel, C., and Marcotte, E.M. (2012). Insights into the regulation of protein abundance from proteomic and transcriptomic analyses. Nat. Rev. Genet. 13: 227-232.
78. Wang, J., Tian, L., Lee, H.S., Wei, N.E., Jiang, H., Watson, B., Madlung, A., Osborn, T.C., Doerge, R.W., Comai, L., and Chen, Z.J. (2006). Genomewide nonadditive gene regulation in Arabidopsis allotetraploids. Genetics 172: 507-517.
79. Warner, D.A., and Edwards, G.E. (1993). Effects of polyploidy on photosynthesis. Photosynth. Res. 35: 135-147.
80. Wood, T.E., Takebayashi, N., Barker, M.S., Mayrose, I., Greenspoon, P.B., and Rieseberg, L.H. (2009). The frequency of polyploid speciation in vascular plants. Proc. Natl. Acad. Sci. USA 106: 13875-13879.
81. Yao, H., Kato, A., Mooney, B., and Birchler, J.A. (2011). Phenotypic and gene expression analyses of a ploidy series of maize inbred Oh43. Plant Mol. Biol. 75: 237-251.