Transcriptome asymmetry in synthetic and natural allotetraploid wheats, revealed by RNA-sequencing

New Phytologist

Volumn 209, Issue 3, 2016, Pages 1264-1277

  Wang, Xutong ^a   Zhang, Huakun ^a   Li, Yaling ^a   Zhang, Zhibin ^a   Li, Linfeng ^a,b   Liu, Bao ^a  

^a NORTHEAST NORMAL UNIVERSITY   (China)

^b WASHINGTON UNIVERSITY   (United States)

Author keywords

Allopolyploidization; Homeolog expression bias; Transcriptome asymmetry; Triticum Aegilops complex; Wheat

Indexed keywords

GENE EXPRESSION; HYBRID; PLOIDY; RNA; WHEAT;

AEGILOPS; AEGILOPS LONGISSIMA; TRITICUM; TRITICUM AESTIVUM; TRITICUM TURGIDUM; TRITICUM URARTU;

MESSENGER RNA; TRANSCRIPTOME;

DIPLOIDY; EVOLUTION; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENETICS; INFLORESCENCE; METABOLISM; PLANT GENE; PLANT LEAF; PLANT SEED; PROCEDURES; SEQUENCE ANALYSIS; TETRAPLOIDY; WHEAT;

BIOLOGICAL EVOLUTION; DIPLOIDY; GENE EXPRESSION REGULATION, PLANT; GENE REGULATORY NETWORKS; GENES, PLANT; INFLORESCENCE; PLANT LEAVES; RNA, MESSENGER; SEEDS; SEQUENCE ANALYSIS, RNA; TETRAPLOIDY; TRANSCRIPTOME; TRITICUM;

EID: 84954121614     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.13678     Document Type: Article

References (100)

1. Abbo S, Gopher A, Peleg Z, Saranga Y, Fahima T, Salamini F, Lev-Yadun S. 2006. The ripples of "The Big (agricultural) Bang": the spread of early wheat cultivation. Genome 49: 861-863.
2. Abbott R, Albach D, Ansell S, Arntzen JW, Baird SJ, Bierne N, Boughman J, Brelsford A, Buerkle CA, Buggs R et al. 2013. Hybridization and speciation. Journal of Evolutionary Biology 26: 229-246.
3. Adams KL, Wendel JF. 2005. Polyploidy and genome evolution in plants. Current Opinion in Plant Biology 8: 135-141.
4. Akhunova AR, Matniyazov RT, Liang H, Akhunov ED. 2010. Homoeolog-specific transcriptional bias in allopolyploid wheat. BMC Genomics 11: 505.
5. Alice B, Small I. 2014. Pentatricopeptide repeat proteins in plants. Annual Review of Plant Biology 65: 415-442.
6. Bardil A, de Almeida JD, Combes MC, Lashermes P, Bertrand B. 2011. Genomic expression dominance in the natural allopolyploid Coffea arabica is massively affected by growth temperature. New Phytologist 192: 760-774.
7. Benjamini Y, Hochberg Y. 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society Series B (Methodological) 57: 289-300.
8. Bentolila S, Alfonso AA, Hanson MR. 2002. A pentatricopeptide repeat-containing gene restores fertility to cytoplasmic male-sterile plants. Proceedings of the National Academy of Sciences, USA 99: 10887-10892.
9. Birchler JA. 2012. Insights from paleogenomic and population studies into the consequences of dosage sensitive gene expression in plants. Current Opinion in Plant Biology 15: 544-548.
10. Buggs RJ, Chamala S, Wu W, Gao L, May GD, Schnable PS, Soltis DE, Soltis PS, Barbazuk WB. 2010a. Characterization of duplicate gene evolution in the recent natural allopolyploid Tragopogon miscellus by next-generation sequencing and Sequenom iPLEX MassARRAY genotyping. Molecular Ecology 19: 132-146.
11. Buggs RJ, Doust AN, Tate JA, Koh J, Soltis K, Feltus FA, Paterson AH, Soltis PS, Soltis DE. 2009. Gene loss and silencing in Tragopogon miscellus (Asteraceae): comparison of natural and synthetic allotetraploids. Heredity 103: 73-81.
12. Buggs RJ, Elliott NM, Zhang L, Koh J, Viccini LF, Soltis DE, Soltis PS. 2010b. Tissue-specific silencing of homoeologs in natural populations of the recent allopolyploid Tragopogon mirus. New Phytologist 186: 175-183.
13. Buggs RJ, Wendel JF, Doyle JJ, Soltis DE, Soltis PS, Coate JE. 2014. The legacy of diploid progenitors in allopolyploid gene expression patterns. Philosophical Transactions of the Royal Society B: Biological 369: 20130354.
14. Buggs RJ, Zhang L, Miles N, Tate JA, Gao L, Wei W, Schnable PS, Barbazuk WB, Soltis PS, Soltis DE. 2011. Transcriptomic shock generates evolutionary novelty in a newly formed, natural allopolyploid plant. Current Biology 21: 551-556.
15. Chague V, Just J, Mestiri I, Balzergue S, Tanguy AM, Huneau C, Huteau V, Belcram H, Coriton O, Jahier J et al. 2010. Genome-wide gene expression changes in genetically stable synthetic and natural wheat allohexaploids. New Phytologist 187: 1181-1194.
16. Chang PL, Dilkes BP, McMahon M, Comai L, Nuzhdin SV. 2010. Homoeolog-specific retention and use in allotetraploid Arabidopsis suecica depends on parent of origin and network partners. Genome Biology 11: R125.
17. Chaudhary B, Hovav R, Rapp R, Verma N, Udall JA, Wendel JF. 2008. Global analysis of gene expression in cotton fibers from wild and domesticated Gossypium barbadense. Evolution & Development 10: 567-582.
18. Chelaifa H, Chague V, Chalabi S, Mestiri I, Arnaud D, Deffains D, Lu Y, Belcram H, Huteau V, Chiquet J et al. 2013. Prevalence of gene expression additivity in genetically stable wheat allohexaploids. New Phytologist 197: 730-736.
19. Chelaifa H, Monnier A, Ainouche M. 2010. Transcriptomic changes following recent natural hybridization and allopolyploidy in the salt marsh species Spartina x townsendii and Spartina anglica (Poaceae). New Phytologist 186: 161-174.
20. Chen ZJ. 2007. Genetic and epigenetic mechanisms for gene expression and phenotypic variation in plant polyploids. Annual Review of Plant Physiology 58: 377-406.
21. Comai L. 2005. The advantages and disadvantages of being polyploid. Nature Reviews Genetics 6: 836-846.
22. Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M, Robles M. 2005. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21: 3674-3676.
23. Cox MP, Dong T, Shen G, Dalvi Y, Scott DB, Ganley AR. 2014. An interspecific fungal hybrid reveals cross-kingdom rules for allopolyploid gene expression patterns. PLoS Genetics 10: e1004180.
24. Dobesova E, Malinska H, Matyasek R, Leitch AR, Soltis DE, Soltis PS, Kovarik A. 2015. Silenced rRNA genes are activated and substitute for partially eliminated active homeologs in the recently formed allotetraploid, Tragopogon mirus (Asteraceae). Heredity 114: 356-365.
25. Dong S, Adams KL. 2011. Differential contributions to the transcriptome of duplicated genes in response to abiotic stresses in natural and synthetic polyploids. New Phytologist 190: 1045-1057.
26. Doyle JJ, Flagel LE, Paterson AH, Rapp RA, Soltis DE, Soltis PS, Wendel JF. 2008. Evolutionary genetics of genome merger and doubling in plants. Annual Review of Genetics 42: 443-461.
27. Dvořák J. 1976. The relationship between the genome of Triticum urartu and the A and B genomes of Triticum aestivum. Canadian Journal of Genetics and Cytology 18: 371-377.
28. Dvorak J, Akhunov ED. 2005. Tempos of gene locus deletions and duplications and their relationship to recombination rate during diploid and polyploid evolution in the Aegilops-Triticum alliance. Genetics 171: 323-332.
29. Eilam T, Anikster Y, Millet E, Manisterski J, Feldman M. 2008. Nuclear DNA amount and genome downsizing in natural and synthetic allopolyploids of the genera Aegilops and Triticum. Genome 51: 616-627.
30. Feldman M, Levy AA. 2005. Allopolyploidy - a shaping force in the evolution of wheat genomes. Cytogenetic and Genome Research 109: 250-258.
31. Feldman M, Levy AA, Fahima T, Korol A. 2012. Genomic asymmetry in allopolyploid plants: wheat as a model. Journal of Experimental Botany 63: 5045-5059.
32. nd edn. London, UK: Longman Scientific, 184-192.
33. Flagel LE, Wendel JF. 2010. Evolutionary rate variation, genomic dominance and duplicate gene expression evolution during allotetraploid cotton speciation. New Phytologist 186: 184-193.
34. Freeling M, Woodhouse MR, Subramaniam S, Turco G, Lisch D, Schnable JC. 2012. Fractionation mutagenesis and similar consequences of mechanisms removing dispensable or less-expressed DNA in plants. Current Opinion in Plant Biology 15: 131-139.
35. Gilad Y, Oshlack A, Rifkin SA. 2006. Natural selection on gene expression. Trends in Genetics 22: 456-461.
36. Gill B, Friebe B. 2002. Cytogenetics, phylogeny and evolution of cultivated wheats. Rajaram S, Curtis BC, Gómez Macpherson H, eds. Bread wheat: improvement and production. FAO Plant production and protection series no. 30. Rome, Italy: Food Agriculture Organization, 71-88.
37. Gordon A, Hannon G. 2012. FASTX-toolkit, FASTQ/A short-reads pre-processing tools. [WWW document] URL http://hannonlab.cshl.edu/fastx_toolkit/ [accessed 2 February 2010]
38. Gornicki P, Zhu H, Wang J, Challa GS, Zhang Z, Gill BS, Li W. 2014. The chloroplast view of the evolution of polyploid wheat. New Phytologist 204: 704-714.
39. Gottlieb L. 2003. Plant polyploidy: gene expression and genetic redundancy. Heredity 91: 91-92.
40. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q et al. 2011. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nature Biotechnology 29: 644-652.
41. Guo X, Han F. 2014. Asymmetric epigenetic modification and elimination of rDNA sequences by polyploidization in wheat. Plant Cell 26: 4311-4327.
42. Hegarty MJ, Barker GL, Wilson ID, Abbott RJ, Edwards KJ, Hiscock SJ. 2006. Transcriptome shock after interspecific hybridization in senecio is ameliorated by genome duplication. Current Biology 16: 1652-1659.
43. Hegarty MJ, Hiscock SJ. 2008. Genomic clues to the evolutionary success of polyploid plants. Current Biology 18: R435-R444.
44. Huang S, Sirikhachornkit A, Su X, Faris J, Gill B, Haselkorn R, Gornicki P. 2002. Genes encoding plastid acetyl-CoA carboxylase and 3-phosphoglycerate kinase of the Triticum/Aegilops complex and the evolutionary history of polyploid wheat. Proceedings of the National Academy of Sciences, USA 99: 8133-8138.
45. Jackson S, Chen ZJ. 2010. Genomic and expression plasticity of polyploidy. Current Opinion in Plant Biology 13: 153-159.
46. Kent WJ. 2002. BLAT-the BLAST-like alignment tool. Genome Research 12: 656-664.
47. Kerber E. 1964. Wheat: reconstitution of the tetraploid component (AABB) of hexaploids. Science 143: 253-255.
48. Kim E-D, Chen ZJ. 2011. Unstable transcripts in Arabidopsis allotetraploids are associated with nonadditive gene expression in response to abiotic and biotic stresses. PLoS ONE 6: e24251.
49. Koh J, Chen S, Zhu N, Yu F, Soltis PS, Soltis DE. 2012. Comparative proteomics of the recently and recurrently formed natural allopolyploid Tragopogon mirus (Asteraceae) and its parents. New Phytologist 196: 292-305.
50. Leach LJ, Belfield EJ, Jiang C, Brown C, Mithani A, Harberd NP. 2014. Patterns of homoeologous gene expression shown by RNA sequencing in hexaploid bread wheat. BMC Genomics 15: 276.
51. Lex A, Gehlenborg N, Strobelt H, Vuillemot R, Pfister H. 2014. UpSet: visualization of intersecting sets. Visualization and Computer Graphics, IEEE Transactions on 20: 1983-1992.
52. Li A, Liu D, Wu J, Zhao X, Hao M, Geng S, Yan J, Jiang X, Zhang L, Wu J et al. 2014. mRNA and small RNA transcriptomes reveal insights into dynamic homoeolog regulation of allopolyploid heterosis in nascent hexaploid wheat. Plant Cell 26: 1878-1900.
53. Li AL, Geng SF, Zhang LQ, Liu DC, Mao L. 2015b. Making the bread: insights from newly synthesized allohexaploid wheat. Molecular Plant 8: 847-859.
54. Li H, Durbin R. 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25: 1754-1760.
55. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, 1000 Genome Project Data Processing Subgroup. 2009. The sequence alignment/map format and SAMtools. Bioinformatics 25: 2078-2079.
56. Li LF, Liu B, Olsen KM, Wendel JF. 2015a. A re-evaluation of the homoploid hybrid origin of Aegilops tauschii, the donor of the wheat D-subgenome. New Phytologist 208: 4-8.
57. Lim KY, Soltis DE, Soltis PS, Tate J, Matyasek R, Srubarova H, Kovarik A, Pires JC, Xiong Z, Leitch AR. 2008. Rapid chromosome evolution in recently formed polyploids in Tragopogon (Asteraceae). PLoS ONE 3: e3353.
58. Liu C, Yang X, Zhang H, Wang X, Zhang Z, Bian Y, Zhu B, Dong Y, Liu B. 2015. Genetic and epigenetic modifications to the BBAA component of common wheat during its evolutionary history at the hexaploid level. Plant Molecular Biology 88: 53-64.
59. Liu Z, Adams KL. 2007. Expression partitioning between genes duplicated by polyploidy under abiotic stress and during organ development. Current Biology 17: 1669-1674.
60. Madlung A. 2013. Polyploidy and its effect on evolutionary success: old questions revisited with new tools. Heredity 110: 99-104.
61. Malinska H, Tate JA, Matyasek R, Leitch AR, Soltis DE, Soltis PS, Kovarik A. 2010. Similar patterns of rDNA evolution in synthetic and recently formed natural populations of Tragopogon (Asteraceae) allotetraploids. BMC Evolutionary Biology 10: 291.
62. Malinska H, Tate JA, Mavrodiev E, Matyasek R, Lim KY, Leitch AR, Soltis DE, Soltis PS, Kovarik A. 2011. Ribosomal RNA genes evolution in Tragopogon: a story of new and old world allotetraploids and the synthetic lines. Taxon 60: 348-354.
63. Marcussen T, Sandve SR, Heier L, Spannagl M, Pfeifer M, Jakobsen KS, Wulff BB, Steuernagel B, Mayer KF, Olsen OA. 2014. Ancient hybridizations among the ancestral genomes of bread wheat. Science 345: 1250092.
64. Matsushita SC, Tyagi AP, Thornton GM, Pires JC, Madlung A. 2012. Allopolyploidization lays the foundation for evolution of distinct populations: evidence from analysis of synthetic Arabidopsis allohexaploids. Genetics 191: 535-547.
65. Otto SP. 2007. The evolutionary consequences of polyploidy. Cell 131: 452-462.
66. Peng J, Ronin Y, Fahima T, Roder MS, Li Y, Nevo E, Korol A. 2003. Domestication quantitative trait loci in Triticum dicoccoides, the progenitor of wheat. Proceedings of the National Academy of Sciences, USA 100: 2489-2494.
67. Pfeifer M, Kugler KG, Sandve SR, Zhan B, Rudi H, Hvidsten TR, International Wheat Genome Sequencing Consortium, Mayer KF, Olsen OA. 2014. Genome interplay in the grain transcriptome of hexaploid bread wheat. Science 345: 1250091.
68. Pont C, Murat F, Confolent C, Balzergue S, Salse J. 2011. RNA-seq in grain unveils fate of neo- and paleopolyploidization events in bread wheat (Triticum aestivum L.). Genome Biology 12: R119.
69. Pont C, Murat F, Guizard S, Flores R, Foucrier S, Bidet Y, Quraishi UM, Alaux M, Dolezel J, Fahima T et al. 2013. Wheat syntenome unveils new evidences of contrasted evolutionary plasticity between paleo- and neoduplicated subgenomes. Plant Journal 76: 1030-1044.
70. Pumphrey M, Bai J, Laudencia-Chingcuanco D, Anderson O, Gill BS. 2009. Nonadditive expression of homoeologous genes is established upon polyploidization in hexaploid wheat. Genetics 181: 1147-1157.
71. Qi B, Huang W, Zhu B, Zhong X, Guo J, Zhao N, Xu C, Zhang H, Pang J, Han F et al. 2012. Global transgenerational gene expression dynamics in two newly synthesized allohexaploid wheat (Triticum aestivum) lines. BMC Biology 10: 3.
72. R Development Core Team. 2014. The R project for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. URL www.R-project.org [accessed 9 June 2015].
73. Renny-Byfield S, Wendel JF. 2014. Doubling down on genomes: polyploidy and crop plants. American Journal of Botany 101: 1711-1725.
74. Rieseberg LH, Willis JH. 2007. Plant speciation. Science 317: 910-914.
75. Romero IG, Ruvinsky I, Gilad Y. 2012. Comparative studies of gene expression and the evolution of gene regulation. Nature Reviews Genetics 13: 505-516.
76. Roose M, Gottlieb L. 1976. Genetic and biochemical consequences of polyploidy in Tragopogon. Evolution 30: 818-830.
77. Roulin A, Auer PL, Libault M, Schlueter J, Farmer A, May G, Stacey G, Doerge RW, Jackson SA. 2012. The fate of duplicated genes in a polyploid plant genome. Plant Journal 73: 143-153.
78. Sehrish T, Symonds VV, Soltis DE, Soltis PS, Tate JA. 2014. Gene silencing via DNA methylation in naturally occurring Tragopogon miscellus (Asteraceae) allopolyploids. BMC Genomics 15: 701.
79. Shaked H, Kashkush K, Ozkan H, Feldman M, Levy AA. 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.
80. Shcherban AB, Badaeva ED, Amosova AV, Adonina IG, Salina EA. 2008. Genetic and epigenetic changes of rDNA in a synthetic allotetraploid. Aegilops sharonensis × Ae. umbellulata. Genome 51: 261-271.
81. Shitsukawa N, Ikari C, Shimada S, Kitagawa S, Sakamoto K, Saito H, Ryuto H, Fukunishi N, Abe T, Takumi S. 2007. The einkorn wheat (Triticum monococcum) mutant, maintained vegetative phase, is caused by a deletion in the VRN1 gene. Genes & Genetic Systems 82: 167-170.
82. Simons KJ, Fellers JP, Trick HN, Zhang Z, Tai Y-S, Gill BS, Faris JD. 2006. Molecular characterization of the major wheat domestication gene Q. Genetics 172: 547-555.
83. Soltis DE, Buggs RJA, Barbazuk WB, Chamala S, Chester M, Gallagher JP, Schnable PS, Soltis PS. 2012. Rapid and repeated evolution in the early stages of polyploidy: genomic and cytogenetic studies of recent polyploidy in Tragopogon. Soltis PS, Soltis DE, eds. Polyploidy and genome evolution. Berlin, Germany: Springer, 271-292.
84. Soltis DE, Albert VA, Leebens-Mack J, Bell CD, Paterson AH, Zheng C, Sankoff D, Depamphilis CW, Wall PK, Soltis PS. 2009. Polyploidy and angiosperm diversification. American Journal of Botany 96: 336-348.
85. Soltis PS, Liu X, Marchant DB, Visger CJ, Soltis DE. 2014. Polyploidy and novelty: Gottlieb's legacy. Philosophical Transactions of the Royal Society B: Biological Sciences 369: 20130351.
86. Soltis DE, Soltis PS, Pires JC, Kovarik A, Tate JA, Mavrodiev E. 2004. Recent and recurrent polyploidy in Tragopogon (Asteraceae): cytogenetic, genomic and genetic comparisons. Biological Journal of the Linnean Society 82: 485-501.
87. Song Q, Chen ZJ. 2015. Epigenetic and developmental regulation in plant polyploids. Current Opinion in Plant Biology 24: 101-109.
88. Tate JA, Joshi P, Soltis KA, Soltis PS, Soltis DE. 2009. On the road to diploidization? Homoeolog loss in independently formed populations of the allopolyploid Tragopogon miscellus (Asteraceae). BMC Plant Biology 9: 80.
89. Tate JA, Ni Z, Scheen AC, Koh J, Gilbert CA, Lefkowitz D, Chen ZJ, Soltis PS, Soltis DE. 2006. Evolution and expression of homeologous loci in Tragopogon miscellus (Asteraceae), a recent and reciprocally formed allopolyploid. Genetics 173: 1599-1611.
90. Wendel JF. 2000. Genome evolution in polyploids. Plant Molecular Biology 42: 225-249.
91. Wickham H. 2009. ggplot2: elegant graphics for data analysis. New York, NY, USA: Springer.
92. Willcox G. 1998. Archaeobotanical evidence for the beginnings of agriculture in Southwest Asia. Damania AB, Valkoun J, Willcox G, Qualset CO, eds. The origins of agriculture and crop domestication. Aleppo, Syria: ICARDA, 25-38.
93. Xu C, Bai Y, Lin X, Zhao N, Hu L, Gong Z, Wendel JF, Liu B. 2014. Genome-wide disruption of gene expression in allopolyploids but not hybrids of rice subspecies. Molecular Biology and Evolution 31: 1066-1076.
94. Yang C, Zhao L, Zhang H, Yang Z, Wang H, Wen S, Zhang C, Rustgi S, von Wettstein D, Liu B. 2014. Evolution of physiological responses to salt stress in hexaploid wheat. Proceedings of the National Academy of Sciences, USA 111: 11882-11887.
95. Yoo MJ, Szadkowski E, Wendel JF. 2013. Homoeolog expression bias and expression level dominance in allopolyploid cotton. Heredity 110: 171-180.
96. Yoo MJ, Wendel JF. 2014. Comparative evolutionary and developmental dynamics of the cotton (Gossypium hirsutum) fiber transcriptome. PLoS Genetics 10: e1004073.
97. Zhang H, Bian Y, Gou X, Dong Y, Rustgi S, Zhang B, Xu C, Li N, Qi B, Han F. 2013. Intrinsic karyotype stability and gene copy number variations may have laid the foundation for tetraploid wheat formation. Proceedings of the National Academy of Sciences, USA 110: 19466-19471.
98. Zhang H, Zhu B, Qi B, Gou X, Dong Y, Xu C, Zhang B, Huang W, Liu C, Wang X, et al. 2014. Evolution of the BBAA component of bread wheat during its history at the allohexaploid level. Plant Cell 26: 2761-2776.
99. Zhang Z, Belcram H, Gornicki P, Charles M, Just J, Huneau C, Magdelenat G, Couloux A, Samain S, Gill BS. 2011. Duplication and partitioning in evolution and function of homoeologous Q loci governing domestication characters in polyploid wheat. Proceedings of the National Academy of Sciences, USA 108: 18737-18742.
100. Zohary D, Feldman M. 1962. Hybridization between amphidiploids and the evolution of polyploids in the wheat (Aegilops-Triticum) group. Evolution 16: 44-61.