The legacy of diploid progenitors in allopolyploid gene expression patterns

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 369, Issue 1648, 2014, Pages

  Buggs, Richard J A ^a   Wendel, Jonathan F ^b   Doyle, Jeffrey J ^c   Soltis, Douglas E ^d,e   Soltis, Pamela S ^e   Coate, Jeremy E ^f  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^b IOWA STATE UNIVERSITY   (United States)

^c Department of Obstetrics Gynecology   (United States)

^d UNIVERSITY OF FLORIDA   (United States)

^e UNIVERSITY OF FLORIDA   (United States)

^f REED COLLEGE   (United States)

Author keywords

Hybridization; Polyploidy; Transcriptomes; Whole genome duplication

Indexed keywords

DICOTYLEDON; EVOLUTIONARY BIOLOGY; EVOLUTIONARY THEORY; GENE EXPRESSION; GENOMICS; HYBRIDIZATION; PLOIDY; RESEARCH WORK;

EID: 84902983437     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2013.0354     Document Type: Review

References (104)

1. Gottlieb LD. 1982 Conservation and duplication of isozymes in plants. Science 216, 373-379. (doi:10.1126/Science.216.4544.373)
2. Gottlieb LD. 2003 Plant polyploidy: gene expression and genetic redundancy. Heredity 91, 91-92. (doi:10.1038/Sj.Hdy.6800317)
3. Soltis PS, Liu X, Marchant DB, Visger CJ, Soltis DE. 2014 Polyploidy and novelty: Gottlieb's legacy. Phil. Trans. R. Soc. B 369, 20130351. (doi:10.1098/rstb.2013.0351)
4. Ramsey J, Ramsey TS. 2014 Ecological studies of polyploidy in the 100 years following its discovery. Phil. Trans. R. Soc. B 369, 20130352. (doi:10.1098/ rstb.2013.0352)
5. Vanneste K, Maere S, Van de Peer Y. 2014 Tangled up in two: a burst of genome duplications at the end of the Cretaceous and the consequences for plant evolution. Phil. Trans. R. Soc. B 369, 20130353. (doi:10.1098/ rstb.2013.0353)
6. Jiao Y, Paterson AH. 2014 Polyploidy-associated genome modifications during land plant evolution. Phil. Trans. R. Soc. B 369, 20130355. (doi:10.1098/ rstb.2013.0355)
7. Gottlieb LD. 1971 Gel electrophoresis: new approach to study of evolution. Bioscience 21, 939-944. (doi:10.2307/1296112)
8. Gottlieb LD. 1973 Genetic differentiation, sympatric speciation, and origin of a diploid species of Stephanomeria. Am. J. Bot. 60, 545-553. (doi:10.2307/2441378)
9. Gottlieb LD. 1973 Enzyme differentiation and phylogeny in Clarkia franciscana and Clarkia rubicunda. Genetics 74, S99.
10. Gottlieb LD. 1973 Genetic control of glutamate oxaloacetate transaminase isoenzymes in diploid plant Stephanomeria exigua and its allotetraploid derivative. Biochem. Genet. 9, 97-107. (doi:10.1007/Bf00485595)
11. Roose ML, Gottlieb LD. 1976 Genetic and biochemical consequences of polyploidy in Tragopogon. Evolution 30, 818-830. (doi:10.2307/2407821)
12. Roose ML, Gottlieb LD. 1980 Biochemical properties and level of expression of alcohol dehydrogenases in the allotetraploid plant Tragopogon miscellus and its diploid progenitors. Biochem. Genet. 18, 1065-1085. (doi:10.1007/Bf00484339)
13. Holsinger KE, Gottlieb LD. 1988 Isozyme variability in the tetraploid Clarkia gracilis (Onagraceae) and its diploid relatives. Syst. Bot. 13, 1-6. (doi:10.2307/2419235)
14. Ford VS, Gottlieb LD. 1999 Molecular characterization of PgiC in a tetraploid plant and its diploid relatives. Evolution 53, 1060-1067. (doi:10.2307/2640811)
15. Ford VS, Gottlieb LD. 2002 Single mutations silence PgiC2 genes in two very recent allotetraploid species of Clarkia. Evolution 56, 699-707. (doi:10.1111/j.0014-3820.2002.tb01381.x)
16. Gottlieb LD. 1969 The role of hybridization in the evolution of the annual species of Stephanomeria (Compositae). Ann Arbor, MI: University of Michigan.
17. Smith-Huerta NL. 1986 Isozymic diversity in three allotetraploid Clarkia species and their putative diploid progenitors. J. Hered. 77, 349-354.
18. Stebbins GL. 1971 Chromosomal evolution in higher plants. London, UK: Edward Arnold.
19. Adams KL, Cronn R, Percifield R, Wendel JF. 2003 Genes duplicated by polyploidy show unequal contributions to the transcriptome and organspecific reciprocal silencing. Proc. Natl Acad. Sci. USA 100, 4649-4654. (doi:10.1073/pnas.0630618100)
20. Ownbey M. 1950 Natural hybridization and amphiploidy in the genus Tragopogon. Am. J. Bot. 37, 487-499. (doi:10.2307/2438023)
21. Vallejo-Marin M. 2012 Mimulus peregrinus (Phrymaceae): a new British allopolyploid species. PhytoKeys 14, 1-14. (doi:10.3897/phytokeys.14.3305)
22. Buggs RJA. 2012 Monkeying around with ploidy. Mol. Ecol. 21, 5159-5161. (doi:10.1111/mec.12005)
23. Chelaifa H, Monnier A, Ainouche M. 2010 Transcriptomic changes following recent natural hybridization and allopolyploidy in the salt marsh species Spartina_townsendii and Spartina anglica (Poaceae). New Phytol. 186, 161-174. (doi:10.1111/j.1469-8137.2010.03179.x)
24. Urbanska KM, Hurka H, Landolt E, Neuffer B, Mummenhoff K. 1997 Hybridization and evolution in Cardamine (Brassicaceae) at Urnerboden, Central Switzerland: biosystematic and molecular evidence. Plant Syst. Evol. 204, 233-256. (doi:10.1007/ BF00989208)
25. Mandáková T, Kovaři{dotless}́k A, Zozomová-Lihová J, Shimizu-Inatsugi R, Shimizu KK, Mummenhoff K, Marhold K, Lysak MA. 2013 The more the merrier: recent hybridization and polyploidy in Cardamine. Plant Cell 25, 3280-3295. (doi:10.1105/tpc.113.114405)
26. Hegarty M, Barker G, Wilson I, Abbott RJ, Edwards KJ, Hiscock SJ. 2006 Transcriptome shock after interspecific hybridization in Senecio is ameliorated by genome duplication. Curr. Biol. 16, 1652-1659 (doi:10.1016/j.cub.2006.06.071)
27. Doyle JJ, Egan AN. 2010 Dating the origins of polyploidy events. New Phytol. 186, 73-85. (doi:10.1111/j.1469-8137.2009.03118.x)
28. Tate J, Joshi P, Soltis K, Soltis P, Soltis D. 2009 On the road to diploidization? Homoeolog loss in independently formed populations of the allopolyploid Tragopogon miscellus (Asteraceae). BMC Plant Biol. 9, 80. (doi:10.1186/1471-2229-9-80)
29. Tate JA, Ni ZF, 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. (doi:10.1534/genetics.106.057646)
30. Gaeta RT, Pires JC, Iniguez-Luy F, Leon E, Osborn TC. 2007 Genomic changes in resynthesized Brassica napus and their effect on gene expression and phenotype. Plant Cell 19, 3403-3417. (doi:10.1105/tpc.107.054346)
31. Xu Y, Zhong L, Wu X, Fang X, Wang J. 2009 Rapid alterations of gene expression and cytosine methylation in newly synthesized Brassica napus allopolyploids. Planta 229, 471-483. (doi:10.1007/ s00425-008-0844-8)
32. He P, Friebe BR, Gill BS, Zhou JM. 2003 Allopolyploidy alters gene expression in the highly stable hexaploid wheat. Plant Mol. Biol. 52, 401-414. (doi:10.1023/A:1023965400532)
33. Kashkush K, Feldman M, Levy AA. 2002 Gene loss, silencing and activation in a newly synthesized wheat allotetraploid. Genetics 160, 1651-1659.
34. Madlung A, Masuelli RW, Watson B, Reynolds SH, Davison J, Comai L. 2002 Remodeling of DNA methylation and phenotypic and transcriptional changes in synthetic Arabidopsis allotetraploids. Plant Physiol. 129, 733-746. (doi:10.1104/ pp.003095)
35. Wang J et al. 2006 Genomewide nonadditive gene regulation in Arabidopsis allotetraploids. Genetics 172, 507-517. (doi:10.1534/genetics.105.047894)
36. Udall JA et al. 2007 Spotted cotton oligonucleotide microarrays for gene expression analysis. BMC Genomics 8, 81. (doi:10.1186/1471-2164-8-81)
37. Hovav R, Udall JA, Chaudhary B, Rapp R, Flagel L, Wendel JF. 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. (doi:10.1073/pnas.0711569105)
38. Hegarty MJ et al. 2005 Development of anonymous cDNA microarrays to study changes to the Senecio floral transcriptome during hybrid speciation. Mol. Ecol. 14, 2493-2510. (doi:10.1111/j.1365-294X.2005.02608.x).
39. Gaeta RT, Yoo S-Y, Pires JC, Doerge RW, Chen ZJ, Osborn TC. 2009 Analysis of gene expression in resynthesized Brassica napus allopolyploids using Arabidopsis 70mer oligo microarrays. PLoS ONE 4, e4760. (doi:10.1371/journal.pone.0004760).
40. Chelaifa H et al. 2013 Prevalence of gene expression additivity in genetically stable wheat allohexaploids. New Phytol. 197, 730-736. (doi:10.1111/nph.12108)
41. Chagué V et al. 2010 Genome-wide gene expression changes in genetically stable synthetic and natural wheat allohexaploids. New Phytol. 187, 1181-1194. (doi:10.1111/j.1469-8137.2010.03339.x)
42. Pumphrey MO, Bai J, Laudencia-Chingcuanco D, Anderson O, Gill BS. 2008 Non-additive expression of homoeologous genes is established upon polyploidization in hexaploid wheat. Genetics 181, 1147-1157. (doi:10.1534/genetics.108.096941)
43. Chelaifa H, Mahe F, Ainouche M. 2010 Transcriptome divergence between the hexaploid salt-marsh sister species Spartina maritima and Spartina alterniflora (Poaceae). Mol. Ecol. 19, 2050-2063. (doi:10.1111/j.1365-294X.2010.04637.x)
44. Udall JA, Swanson JM, Nettleton D, Percifield RJ, Wendel JF. 2006 A novel approach for characterizing expression levels of genes duplicated by polyploidy. Genetics 173, 1823-1827. (doi:10.1534/genetics.106.058271)
45. Flagel LE, Udall J, Nettleton D, Wendel J. 2008 Duplicate gene expression in allopolyploid Gossypium reveals two temporally distinct phases of expression evolution. BMC Biol. 6, 16. (doi:10.1186/ 1741-7007-6-16)
46. Buggs RJA et al. 2011 Transcriptomic shock generates evolutionary novelty in a newly formed, natural allopolyploid plant. Curr. Biol. 21, 551-556. (doi:10.1016/j.cub.2011.02.016)
47. Buggs RJA, Chamala S, Wu W, Gao L, May GD, Schnable PS, Soltis DE, Soltis PS, Barbazuk WB. 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. (doi:10.1111/j.1365-294X.2009.04469.x)
48. Chaudhary B, Flagel L, Stupar RM, Udall JA, Verma N, Springer NM, Wendel JF. 2009 Reciprocal silencing, transcriptional bias and functional divergence of homeologs in polyploid cotton (Gossypium). Genetics 182, 503-517. (doi:10.1534/ genetics.109.102608).
49. Shi X, Ng DWK, Zhang C, Comai L, Ye W, Jeffrey CZ. 2012 Cis-and trans-regulatory divergence between progenitor species determines gene-expression novelty in Arabidopsis allopolyploids. Nat. Commun. 3, 950. (doi:10.1038/ncomms1954).
50. Yoo MJ, Szadkowski E, Wendel JF. 2013 Homoeolog expression bias and expression level dominance in allopolyploid cotton. Heredity 110, 171-180. (doi:10.1038/hdy.2012.94)
51. Bombarely A, Edwards K, Sanchez-Tamburrino J, Mueller L. 2012 Deciphering the complex leaf transcriptome of the allotetraploid species Nicotiana tabacum: a phylogenomic perspective. BMC Genomics 13, 406. (doi:10.1186/1471-2164-13-406)
52. Ilut DC, Coate JE, Luciano AK, Owens TG, May GD, Farmer A, Doyle JJ. 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. (doi:10.3732/ajb.1100312).
53. Higgins J, Magusin A, Trick M, Fraser F, Bancroft I. 2012 Use of mRNA-seq to discriminate contributions to the transcriptome from the constituent genomes of the polyploid crop species Brassica napus. BMC Genomics 13, 247. (doi:10.1186/1471-2164-13-247)
54. Jiang J, Shao Y, Du K, Ran L, Fang X, Wang Y. 2013 Use of digital gene expression to discriminate gene expression differences in early generations of resynthesized Brassica napus and its diploid progenitors. BMC Genomics 14, 72. (doi:10.1186/ 1471-2164-14-72)
55. Combes M-C, Dereeper A, Severac D, Bertrand B, Lashermes P. 2013 Contribution of subgenomes to the transcriptome and their intertwined regulation in the allopolyploid Coffea arabica grown at contrasted temperatures. New Phytol. 200, 251-260. (doi:10.1111/nph.12371).
56. Coate JE, Doyle JJ. 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. (doi:10.1093/gbe/evq038)
57. Vogel C, Marcotte EM. 2012 Insights into the regulation of protein abundance from proteomic and transcriptomic analyses. Nat. Rev. Genet. 13, 227-232.
58. Coate JE, Bar H, Doyle JJ. 2014 Extensive translational regulation of gene expression in an allopolyploid (Glycine dolichocarpa). Plant Cell 26, 136-150. (doi:10.1105/tpc.113.119966)
59. Kong F, Mao S, Jiang J, Wang J, Fang X, Wang Y. 2011 Proteomic changes in newly synthesized Brassica napus allotetraploids and their early generations. Plant Mol. Biol. Rep. 29, 927-935. (doi:10.1007/s11105-011-0301-x)
60. Gancel A-L, Grimplet JRM, Sauvage FO-X, Ollitrault P, Brillouet J-M. 2006 Predominant expression of diploid mandarin leaf proteome in two citrus mandarin-derived somatic allotetraploid hybrids. J. Agric. Food Chem. 54, 6212-6218. (doi:10.1021/ jf060657p).
61. Carpentier SC, Panis B, Renaut J, Samyn B, Vertommen A, Vanhove A-C, Swennen R, Sergeant K. 2011 The use of 2D-electrophoresis and de novo sequencing to characterize inter-and intra-cultivar protein polymorphisms in an allopolyploid crop. Phytochemistry 72, 1243-1250. (doi:10.1016/j. phytochem.2010.10.016)
62. Ng DWK, Zhang C, Miller M, Shen Z, Briggs SP, Chen ZJ. 2012 Proteomic divergence in Arabidopsis autopolyploids and allopolyploids and their progenitors. Heredity 108, 419-430. (doi:10.1038/ hdy.2011.92)
63. Albertin W, Alix K, Balliau T, Brabant P, Davanture M, Malosse C, Valot B, 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. (doi:10.1186/ 1471-2164-8-56)
64. Albertin W, Balliau T, Brabant P, Chevre AM, Eber F, Malosse C, Thiellement H. 2006 Numerous and rapid nonstochastic modifications of gene products in newly synthesized Brassica napus allotetraploids. Genetics 173, 1101-1113. (doi:10.1534/genetics.106.057554).
65. Hu G, Houston NL, Pathak D, Schmidt L, Thelen JJ, Wendel JF. 2011 Genomically biased accumulation of seed storage proteins in allopolyploid cotton. Genetics 189, 1103-1115. (doi:10.1534/genetics.111.132407)
66. Bao Y, Hu G, Flagel LE, Salmon A, Bezanilla M, Paterson AH, Wang Z, Wendel JF. 2011 Parallel upregulation of the profilin gene family following independent domestication of diploid and allopolyploid cotton (Gossypium). Proc. Natl Acad. Sci. USA 108, 21 152-21 157. (doi:10.1073/pnas.1115926109)
67. Hu G, Koh J, Yoo M-J, Grupp K, Chen S, Wendel JF. 2013 Proteomic profiling of developing cotton fibers from wild and domesticated Gossypium barbadense. New Phytol. 200, 570-582. (doi:10.1111/nph.12381)
68. 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 Phytol. 196, 292-305. (doi:10.1111/j.1469-8137.2012.04251.x)
69. Flagel LE, Wendel JF. 2010 Evolutionary rate variation, genomic dominance and duplicate gene expression evolution during allotetraploid cotton speciation. New Phytol. 186, 184-193. (doi:10.1111/j.1469-8137.2009.03107.x)
70. Schnable JC, Springer NM, 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. (doi:10.1073/pnas.1101368108)
71. Rapp RA, Udall JA, Wendel JF. 2009 Genomic expression dominance in allopolyploids. BMC Biol. 7, 18. (doi:10.1186/1741-7007-7-18)
72. Buggs RJA. 2013 Unravelling gene expression of complex crop genomes. Heredity 110, 97-98. (doi:10.1038/hdy.2012.61)
73. Grover CE, Gallagher JP, Szadkowski EP, Yoo MJ, Flagel LE, Wendel JF. 2012 Homoeolog expression bias and expression level dominance in allopolyploids. New Phytol. 196, 966-971. (doi:10.1111/j.1469-8137.2012.04365.x)
74. Wang JL, Tian L, Lee HS, Chen ZJ. 2006 Nonadditive regulation of FRI and FLC loci mediates floweringtime variation in Arabidopsis allopolyploids. Genetics 173, 965-974. (doi:10.1534/genetics.106.056580)
75. Gianinetti A. 2013 A criticism of the value of midparent in polyploidization. J. Exp. Bot. 64, 4119-4129. (doi:10.1093/jxb/ert263)
76. Lovén J, Orlando DA, Sigova AA, Lin CY, Rahl PB, Burge CB, Levens DL, Lee TI, Young RA. 2012 Revisiting global gene expression analysis. Cell 151, 476-482. (doi:10.1016/j.cell.2012.10.012)
77. Marguerat S, Schmidt A, Codlin S, Chen W, Aebersold R, Bühler J. 2012 Quantitative analysis of fission yeast transcriptomes and proteomes in proliferating and quiescent cells. Cell 151, 671-683. (doi:10.1016/j.cell.2012.09.019)
78. Guo M, Davis D, Birchler JA. 1996 Dosage effects on gene expression in a maize ploidy series. Genetics 142, 1349-1355.
79. 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. (doi:10.1146/ annurev.arplant.043008.092122).
80. Birchler JA, Veitia RA. 2012 Gene balance hypothesis: connecting issues of dosage sensitivity across biological disciplines. Proc. Natl Acad. Sci. USA 109, 14 746-14 753. (doi:10.1073/pnas.1207726109)
81. Yao H, Kato A, Mooney B, Birchler J. 2011 Phenotypic and gene expression analyses of a ploidy series of maize inbred Oh43. Plant Mol. Biol. 75, 237-251. (doi:10.1007/s11103-010-9722-4)
82. Buggs RJA, Elliott NM, Zhang LJ, Koh J, Viccini LF, Soltis DE, Soltis PS. 2010 Tissue-specific silencing of homoeologs in natural populations of the recent allopolyploid Tragopogon mirus. New Phytol. 186, 175-183. (doi:10.1111/j.1469-8137.2010.03205.x)
83. Buggs RJA, 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. (doi:10.1038/hdy.2009.24)
84. Buggs RJA, Chamala S, Wu W, Tate JA, Schnable PS, Soltis DE, Soltis PS, Barbazuk WB. 2012 Rapid, repeated and clustered loss of duplicate genes in allopolyploid plant populations of independent origin. Curr. Biol. 22, 248-252. (doi:10.1016/j.cub.2011.12.027)
85. Soltis PS, Plunkett GM, Novak SJ, Soltis DE. 1995 Genetic variation in Tragopogon species: additional origins of the allotetraploids T. mirus and T. miscellus (Compositae). Am. J. Bot. 82, 1329-1341. (doi:10.2307/2446255)
86. Wittkopp PJ, Haerum BK, Clark AG. 2004 Evolutionary changes in cis and trans gene regulation. Nature 430, 85-88. (doi:10.1038/ nature02698)
87. Bell GDM, Kane NC, Rieseberg LH, Adams KL. 2013 RNA-seq analysis of allele-specific expression, hybrid effects, and regulatory divergence in hybrids compared with their parents from natural populations. Genome Biol. Evol. 5, 1309-1323. (doi:10.1093/gbe/evt072)
88. Meiklejohn CD, Coolon JD, Hartl DL, Wittkopp PJ. 2014 The roles of cis-and trans-regulation in the evolution of regulatory incompatibilities and sexually dimorphic gene expression. Genome Res. 24, 84-95. (doi:10.1101/gr.156414.113)
89. Goncalves A, Leigh-Brown S, Thybert D, Stefflova K, Turro E, Flicek P, Brazma A, Odom DT, Marioni JC. 2012 Extensive compensatory cis-trans regulation in the evolution of mouse gene expression. Genome Res. 22, 2376-2384. (doi:10.1101/gr.142281.112)
90. Buggs RJA, Soltis PS, Mavrodiev EV, Symonds VV, Soltis DE. 2008 Does phylogenetic distance between parental genomes govern the success of polyploids? Castanea 73, 74-93. (doi:10.2179/0008-7475 (2008)73[74:DPDBPG]2.0.CO;2)
91. Buggs RJA, Soltis PS, Soltis DE. 2009 Does hybridization between divergent progenitors drive whole-genome duplication? Mol. Ecol. 18, 3334-3339. (doi:10.1111/j.1365-294X.2009.04285.x)
92. Buggs RJA, Soltis PS, Soltis DE. 2011 Biosystematic relationships and the formation of polyploids. Taxon 60, 324-332.
93. Chapman MA, Burke JM. 2007 Genetic divergence and hybrid speciation. Evolution 61, 1773-1780. (doi:10.1111/j.1558-5646.2007.00134.x)
94. Paun O, Forest F, Fay MF, Chase MW. 2009 Hybrid speciation in angiosperms: parental divergence drives ploidy. New Phytol. 182, 507-518. (doi:10.1111/j.1469-8137.2009.02767.x)
95. Paun O, Forest F, Fay MF, Chase MW. 2011 Parental divergence and hybrid speciation in angiosperms revisited. Taxon 60, 1241-1244.
96. Adams KL. 2007 Evolution of duplicate gene expression in polyploid and hybrid plants. J. Hered. 98, 136-141. (doi:10.1093/jhered/esl061)
97. Adams KL, Wendel JF. 2005 Novel patterns of gene expression in polyploid plants. Trends Genet. 21, 539-543. (doi:10.1016/j.tig.2005.07.009)
98. Chen ZJ, Ni Z. 2006 Mechanisms of genomic rearrangements and gene expression changes in plant polyploids. Bioessays 28, 240-252. (doi:10.1002/bies.20374)
99. Hegarty MJ, Hiscock SJ. 2008 Genomic clues to the evolutionary success of polyploid plants. Curr. Biol. 18, R435-R444. (doi:10.1016/j.cub.2008.03.043)
100. 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. (doi:10.1146/annurev.genet.42.110807.091524)
101. Soltis PS, Soltis DE. 2009 The role of hybridization in plant speciation. Annu. Rev. Plant Biol. 60, 561-588. (doi:10.1146/annurev.arplant.043008.092039)
102. Comai L, Madlung A, Josefsson C, Tyagi A. 2003 Do the different parental 'heteromes' cause genomic shock in newly formed allopolyploids? Phil. Trans. R. Soc. Lond. B 358, 1149-1155. (doi:10.1098/rstb.2003.1305)
103. Ha M 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, 17 835-17 840. (doi:10.1073/ pnas.0907003106)
104. 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 Phytol. 192, 760-774. (doi:10.1111/j.1469-8137.2011.03833.x)