Advertisement

Theoretical and Applied Genetics

, Volume 132, Issue 8, pp 2295–2308 | Cite as

Extensive changes in gene expression and alternative splicing due to homoeologous exchange in rice segmental allopolyploids

  • Zhibin Zhang
  • Tiansi Fu
  • Zhijian Liu
  • Xutong Wang
  • Hongwei Xun
  • Guo Li
  • Baoxu Ding
  • Yuzhu Dong
  • Xiuyun Lin
  • Karen A. Sanguinet
  • Bao Liu
  • Ying WuEmail author
  • Lei GongEmail author
Original Article

Abstract

Key message

We report rampant homoeologous exchanges in progenies of a newly synthesized rice segmental allotetraploid and demonstrate their consequences to changes of gene expression and alternative splicing.

Abstract

Allopolyploidization is recurrent across the tree of angiosperms and known as a driving evolutionary force in both plants and animals. A salient feature of allopolyploidization is the induction of homoeologous exchange (HE) events between the constituent subgenomes, which may in turn cause changes in gene expression, transcript alternative splicing, and phenotypic novelty. However, this issue has been poorly studied, largely because lack of a system in which the exact parentage donating the subgenomes is known and the HE events are occurring in real time. Here, we employed whole-genome re-sequencing and RNA-seq-based transcriptome profiling in four randomly chosen progeny individuals (at the 10th-selfed generation) of segmental allotetraploids that were constructed by colchicine-mediated whole-genome doubling of F1 hybrids between the two subspecies (japonica and indica) of Asian cultivated Oryza sativa. We show that rampant HE events occurred in these tetraploid individuals, which converted most of the otherwise heterozygous genomic regions into a homogenized state of one parental subgenome. We demonstrate that genes within these homogenized genomic regions in the tetraploids showed high frequencies of altered expression and enhanced alternative splicing relative to their counterparts in the corresponding diploid parents in the embryo tissue. Intriguingly, limited overlaps between the differentially expressed genes and the differential alternative spliced genes were identified, which were partitioned to distinctly enriched gene ontology terms. Together, our results indicate that HE is a major mechanism to rapidly generate novelty in gene expression and transcriptome diversity, which may facilitate phenotypic innovation in nascent allopolyploids and relevant to allopolyploid crop breeding.

Notes

Acknowledgements

This work was supported by the National Natural Science Foundation of China (31500176), the National Key Research and Development Program of China (2016YFD0101004), the Recruitment Program of Global Youth Experts, the Program of Changbai Mountain Scholar and the Program for Introducing Talents to Universities (B07017).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

122_2019_3355_MOESM1_ESM.pdf (1.7 mb)
Supplementary material 1 (PDF 1697 kb)

References

  1. Allen GC, Flores-Vergara MA, Krasynanski S, Kumar S, Thompson WF (2006) A modified protocol for rapid DNA isolation from plant tissues using cetyltrimethylammonium bromide. Nat Protoc 1:2320–2325CrossRefGoogle Scholar
  2. Anders S, Huber W (2010) Differential expression analysis for sequence count data. Genome Biol 11:1–12CrossRefGoogle Scholar
  3. Anders S, Pyl PT, Huber W (2015) HTSeq-a Python framework to work with high-throughput sequencing data. Bioinformatics 31:166–169CrossRefGoogle Scholar
  4. Buggs RJA, 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. Curr Biol 21:551–556CrossRefGoogle Scholar
  5. Chalhoub B, Denoeud F, Liu S, Parkin IA, Tang H, Wang X, Chiquet J, Belcram H, Tong C, Samans B (2014) Plant genetics. Early allopolyploid evolution in the post-Neolithic Brassica napus oilseed genome. Science 345:950–953CrossRefGoogle Scholar
  6. Chang CY, Lin WD, Tu SL (2012) Genome-wide analysis of heat-sensitive alternative splicing in Physcomitrella patens. Plant Physiol 165:826–840CrossRefGoogle Scholar
  7. Chester M, Gallagher JP, Symonds VV, Silva AVCD, Mavrodiev EV, Leitch AR, Soltis PS, Soltis DE (2012) Extensive chromosomal variation in a recently formed natural allopolyploid species, Tragopogon miscellus (Asteraceae). Proc Natl Acad Sci USA 109:1176–1181CrossRefGoogle Scholar
  8. Combes MC, 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 200:251–260CrossRefGoogle Scholar
  9. Doyle JJ, Doyle JL, Rauscher JT, Ahd B (2003) Diploid and polyploid reticulate evolution throughout the history of the perennial soybeans (Glycine subgenus Glycine). New Phytol 161:121–132CrossRefGoogle Scholar
  10. 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 42:443–461CrossRefGoogle Scholar
  11. Feng D, Peng C, Wang Z, Zhang S, Ali S, Xiong L (2014) Genome-wide analysis of alternative splicing of pre-mRNA under salt stress in Arabidopsis. BMC Genom 15:431CrossRefGoogle Scholar
  12. Filichkin SA, Cumbie JS, Dharmawardhana P, Jaiswal P, Chang JH, Palusa SG, Reddy AS, Megraw M, Mockler TC (2015) Environmental stresses modulate abundance and timing of alternatively spliced circadian transcripts in Arabidopsis. Mol Plant 8:207–227CrossRefGoogle Scholar
  13. Flagel LE, Wendel JF, Udall JA (2012) Duplicate gene evolution, homoeologous recombination, and transcriptome characterization in allopolyploid cotton. BMC Genom 13:302CrossRefGoogle Scholar
  14. Foissac S, Sammeth M (2007) ASTALAVISTA: dynamic and flexible analysis of alternative splicing events in custom gene datasets. Nucleic Acids Res 35:297–299CrossRefGoogle Scholar
  15. Gaeta RT, Pires JC (2010) Homoeologous recombination in allopolyploids: the polyploid ratchet. New Phytol 186:18–28CrossRefGoogle Scholar
  16. Grover CE, Gallagher JP, Szadkowski EP, Yoo MJ, Flagel LE, Wendel JF (2012) Homoeolog expression bias and expression level dominance in allopolyploids. New Phytol 196:966–971CrossRefGoogle Scholar
  17. Guo X, Han F (2014) Asymmetric epigenetic modification and elimination of rDNA sequences by polyploidization in wheat. Plant Cell 26:4311–4327CrossRefGoogle Scholar
  18. Haas BJ, Papanicolaou A, Yassour M, Grabherr M, Blood PD, Bowden J, Couger MB, Eccles D, Li B, Lieber M (2013) De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat Protoc 8:1494–1512CrossRefGoogle Scholar
  19. He Z, Wang L, Harper AL, Havlickova L, Pradhan AK, Parkin IAP, Bancroft I (2016) Extensive homoeologous genome exchanges in allopolyploid crops revealed by mRNAseq-based visualization. Plant Biotechnol J 15:594–604CrossRefGoogle Scholar
  20. Henry IM, Tyagi A, Comai L (2014) The BOY NAMED SUE quantitative trait locus confers increased meiotic stability to an adapted natural allopolyploid of Arabidopsis. Plant Cell 26:181–194CrossRefGoogle Scholar
  21. Hurgobin B, Golicz AA, Bayer PE, Chan CK, Tirnaz S, Dolatabadian A, Schiessl SV, Samans B, Montenegro JD, Parkin I (2017) Homoeologous exchange is a major cause of gene presence/absence variation in the amphidiploid Brassica napus. Plant Biotechnol J 16:1265–1274CrossRefGoogle Scholar
  22. Jiao Y, Wickett NJ, Ayyampalayam S, Chanderbali AS, Landherr L, Ralph PE, Tomsho LP, Hu Y, Liang H, Soltis PS (2011) Ancestral polyploidy in seed plants and angiosperms. Nature 473:97–100CrossRefGoogle Scholar
  23. Keren H, Levmaor G, Ast G (2010) Alternative splicing and evolution: diversification, exon definition and function. Nat Rev Genet 11:345–355CrossRefGoogle Scholar
  24. Kornblihtt AR, Schor IE, Alló M, Dujardin G, Petrillo E, Muñoz MJ (2013) Alternative splicing: a pivotal step between eukaryotic transcription and translation. Nat Rev Mol Cell Biol 14:153–165CrossRefGoogle Scholar
  25. Kovarik A, Renny-Byfield S, Grandbastien MA, Leitch A (2012) Evolutionary implications of genome and karyotype Restructuring in Nicotiana tabacum L. In: Soltis P, Soltis D (eds) Polyploidy and genome evolution. Springer, Berlin, HeidelbergGoogle Scholar
  26. Kraitshtein Z, Yaakov B, Khasdan V, Kashkush K (2010) Genetic and epigenetic dynamics of a retrotransposon after allopolyploidization of wheat. Genetics 186:801–812CrossRefGoogle Scholar
  27. Lashermes P, Combes MC, Hueber Y, Severac D, Dereeper A (2014) Genome rearrangements derived from homoeologous recombination following allopolyploidy speciation in coffee. Plant J 78:674–685CrossRefGoogle Scholar
  28. Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 25:1754–1760CrossRefGoogle Scholar
  29. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R (2009) The sequence alignment/map (SAM) format and SAMtools. Transpl Proc 19:1653–1654Google Scholar
  30. Li Q, Xiao G, Zhu YX (2014) Single-nucleotide resolution mapping of the Gossypium raimondii transcriptome reveals a new mechanism for alternative splicing of introns. Mol Plant 7:829–840CrossRefGoogle Scholar
  31. Li F, Fan G, Lu C, Xiao G, Zou C, Kohel RJ, Ma Z, Shang H, Ma X, Wu J (2015) Genome sequence of cultivated Upland cotton (Gossypium hirsutum TM-1) provides insights into genome evolution. Nat Biotechnol 33:524–530CrossRefGoogle Scholar
  32. Li N, Xu CM, Zhang A, Lv RL, Meng XC, Lin XY, Gong L, Wendel JF, Liu B (2019) DNA methylation repatterning accompanying hybridization, whole genome doubling and homoeolog exchange in nascent segmental rice allotetraploids. New Phytologist.  https://doi.org/10.1111/nph.15820 Google Scholar
  33. Lienert F, Wirbelauer C, Som I, Dean A, Mohn F, Schübeler D (2011) Identification of genetic elements that autonomously determine DNA methylation states. Nat Genet 43:1091–1097CrossRefGoogle Scholar
  34. Ling Z, Zhou W, Baldwin IT, Xu S (2015) Insect herbivory elicits genome-wide alternative splicing responses in Nicotiana attenuata. Plant J Cell Mol Biol 84:228–243CrossRefGoogle Scholar
  35. Liu L, Stein A, Wittkop B, Sarvari P, Li J, Yan X, Dreyer F, Frauen M, Friedt W, Snowdon RJ (2012) A knockout mutation in the lignin biosynthesis gene CCR33 explains a major QTL for acid detergent lignin content in Brassica napus seeds. Theor Appl Genet 124:1573–1586CrossRefGoogle Scholar
  36. Liu Z, Qin J, Tian X, Xu S, Wang Y, Li H, Wang X, Peng H, Yao Y, Hu Z (2017) Global profiling of alternative splicing landscape responsive to drought, heat and their combination in wheat (Triticum asetivum L.). Plant Biotechnol J 16:714–726CrossRefGoogle Scholar
  37. Lloyd A, Blary A, Charif D, Charpentier C, Tran J, Balzergue S, Delannoy E, Rigaill G, Jenczewski E (2017) Homoeologous exchanges cause extensive dosage‐dependent gene expression changes in an allopolyploid crop. New Phytologist 217:367–377CrossRefGoogle Scholar
  38. Madlung A, Wendel JF (2013) Genetic and epigenetic aspects of polyploid evolution in plants. Cytogenet Genome Res 140:270–285CrossRefGoogle Scholar
  39. Marquardt S, Raitskin O, Wu Z, Liu F, Sun Q, Dean C (2014) Functional consequences of splicing of the antisense transcript COOLAIR on FLC transcription. Mol Cell 54:156–165CrossRefGoogle Scholar
  40. Pertea M, Kim D, Pertea G, Leek JT, Salzberg SL (2016) Transcript-level expression analysis of RNA-seq experiments with HISAT, StringTie, and Ballgown. Nat Protoc 11:1650–1667CrossRefGoogle Scholar
  41. Quinlan AR, Hall IM (2010) BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26:841–842CrossRefGoogle Scholar
  42. Reddy AS, Marquez Y, Kalyna M, Barta A (2013) Complexity of the alternative splicing landscape in plants. Plant Cell 25:3657–3683CrossRefGoogle Scholar
  43. Renny-Byfield S, Wendel JF (2014) Doubling down on genomes: polyploidy and crop plants. Am J Bot 101:1711–1725CrossRefGoogle Scholar
  44. Rosloski SM, Singh A, Jali SS, Balasubramanian S, Weigel D, Grbic V (2013) Functional analysis of splice variant expression of MADS AFFECTING FLOWERING 2 of Arabidopsis thaliana. Plant Mol Biol 81:57–69CrossRefGoogle Scholar
  45. Salmon A, Flagel L, Ying B, Udall JA, Wendel JF (2010) Homoeologous nonreciprocal recombination in polyploid cotton. New Phytol 186:123–134CrossRefGoogle Scholar
  46. Saminathan T, Nimmakayala P, Manohar S, Malkaram S, Almeida A, Cantrell R, Tomason Y, Abburi L, Rahman MA, Vajja VG (2015) Differential gene expression and alternative splicing between diploid and tetraploid watermelon. J Exp Bot 66:1369–1385CrossRefGoogle Scholar
  47. Schafer S, Miao K, Benson CC, Heinig M, Cook SA, Hubner N (2015) Alternative splicing signatures in RNA-seq data: percent spliced in (PSI). Curr Protoc Hum Genet 24:11–11Google Scholar
  48. Seo PJ, Park MJ, Lim MH, Kim SG, Lee M, Baldwin IT, Park CM (2012) A self-regulatory circuit of CIRCADIAN CLOCK-ASSOCIATED1 underlies the circadian clock regulation of temperature responses in Arabidopsis. Plant Cell 24:2427–2442CrossRefGoogle Scholar
  49. Shi X, Ng DW, Zhang C, Comai L, Ye W, Chen ZJ (2012) Cis- and trans-regulatory divergence between progenitor species determines gene-expression novelty in Arabidopsis allopolyploids. Nat Commun 3:950CrossRefGoogle Scholar
  50. Smith JE, Baker KE (2015) Nonsense-mediated RNA decay: a switch and dial for regulating gene expression. BioEssays 37:612–623CrossRefGoogle Scholar
  51. Soltis PS, Marchant DB, Van de Peer Y, Soltis DE (2015) Polyploidy and genome evolution in plants. Curr Opin Genet Dev 35:119–125CrossRefGoogle Scholar
  52. Soltis DE, Visger CJ, Marchant DB, Soltis PS (2016) Polyploidy: pitfalls and paths to a paradigm. Am J Bot 103:1146–1166CrossRefGoogle Scholar
  53. Song Q, Chen ZJ (2015) Epigenetic and developmental regulation in plant polyploids. Curr Opin Plant Biol 24:101–109CrossRefGoogle Scholar
  54. Stebbins GL (1947) Types of polyploids; their classification and significance. Adv Genet 1:403–429CrossRefGoogle Scholar
  55. Sturgill D, Malone JH, Sun X, Smith HE, Rabinow L, Samson ML, Oliver B (2013) Design of RNA splicing analysis null models for post hoc filtering of Drosophila head RNA-seq data with the splicing analysis kit (Spanki). BMC Bioinform 14:1–18CrossRefGoogle Scholar
  56. Sultan M, Schulz MH, Richard H, Magen A, Klingenhoff A, Scherf M, Seifert M, Borodina T, Soldatov A, Parkhomchuk D (2008) A global view of gene activity and alternative splicing by deep sequencing of the human transcriptome. Science 321:956–960CrossRefGoogle Scholar
  57. Sun Y, Wu Y, Yang C, Sun S, Lin X, Liu L, Xu C, Wendel JF, Gong L, Liu B (2017) Segmental allotetraploidy generates extensive homoeologous expression rewiring and phenotypic diversity at the population level in rice. Mol Ecol 26:5451–5466CrossRefGoogle Scholar
  58. Syed NH, Kalyna M, Marquez Y, Barta A, Brown JW (2012) Alternative splicing in plants–coming of age. Trends Plant Sci 17:616–623CrossRefGoogle Scholar
  59. Szadkowski E, Eber F, Huteau V, Lodé M, Coriton O, Jenczewski E, Chèvre AM (2011) Polyploid formation pathways have an impact on genetic rearrangements in resynthesized Brassica napus. New Phytol 191:884–894CrossRefGoogle Scholar
  60. Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L (2014) Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 7:562–578CrossRefGoogle Scholar
  61. Tsunematsu H, Yoshimura A, Harushima Y, Nagamura Y, Kurata N, Yano M, Sasaki T, Iwata N (1996) RFLP framework map using recombinant inbred lines in rice. Breed Sci 46:279–284Google Scholar
  62. Van de Peer Y, Mizrachi E, Marchal K (2017) The evolutionary significance of polyploidy. Nat Rev Genet 18:411–424CrossRefGoogle Scholar
  63. Vitulo N, Forcato C, Carpinelli EC, Telatin A, Campagna D, D’Angelo M, Zimbello R, Corso M, Vannozzi A, Bonghi C (2014) A deep survey of alternative splicing in grape reveals changes in the splicing machinery related to tissue, stress condition and genotype. BMC Plant Biol 14(2):99CrossRefGoogle Scholar
  64. Wang X, Hu L, Wang X, Li N, Xu C, Gong L, Liu B (2016) DNA methylation affects gene alternative splicing in plants: an example from rice. Mol Plant 9:305–307CrossRefGoogle Scholar
  65. Wang J, Symul L, Yeung J, Gobet C, Sobel J, Lück S, Westermark PO, Molina N, Naef F (2018a) Circadian clock-dependent and -independent posttranscriptional regulation underlies temporal mRNA accumulation in mouse liver. Proc Natl Acad Sci USA 115:E1916–E1925CrossRefGoogle Scholar
  66. Wang M, Wang P, Liang F, Ye Z, Li J, Shen C, Pei L, Wang F, Hu J, Tu L (2018b) A global survey of alternative splicing in allopolyploid cotton: landscape, complexity and regulation. New Phytol 217:163–178CrossRefGoogle Scholar
  67. Wittkopp PJ, Kalay G (2012) Cis-regulatory elements: molecular mechanisms and evolutionary processes underlying divergence. Nat Rev Genet 13:59–69CrossRefGoogle Scholar
  68. Wu Y, Sun Y, Sun S, Li G, Wang J, Wang B, Lin X, Huang M, Gong Z, Sanguinet KA, Zhang Z, Liu B (2018) Aneuploidization under segmental allotetraploidy in rice and its phenotypic manifestation. Theor Appl Genet 131(6):1273–1285CrossRefGoogle Scholar
  69. Xu F, Xu S, Wiermer M, Zhang Y, Li X (2012) The cyclin L homolog MOS12 and the MOS4-associated complex are required for the proper splicing of plant resistance genes. Plant J Cell Mol Biol 70:916–928CrossRefGoogle Scholar
  70. 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. Mol Biol Evol 31:1066–1076CrossRefGoogle Scholar
  71. Yang CC, Kawahara Y, Mizuno H, Wu J, Matsumoto T, Itoh T (2012) Independent domestication of Asian rice followed by gene flow from japonica to indica. Mol Biol Evol 29:1471CrossRefGoogle Scholar
  72. Yu G, Wang LG, Han Y, He QY (2012) clusterProfiler: an R Package for comparing biological themes among gene clusters. Omics J Integr Biol 16:284–287CrossRefGoogle Scholar
  73. Zhang H, Bian Y, Gou X, Zhu B, Xu C, Qi B, Li N, Rustgi S, Zhou H, Han F (2013) Persistent whole-chromosome aneuploidy is generally associated with nascent allohexaploid wheat. Proc Natl Acad Sci USA 110:3447–3452CrossRefGoogle Scholar
  74. Zhao J, Udall JA, Quijada PA, Grau CR, Meng J, Osborn TC (2006) Quantitative trait loci for resistance to Sclerotinia sclerotiorum and its association with a homeologous non-reciprocal transposition in Brassica napus L. Theor Appl Genet 112:509–516CrossRefGoogle Scholar
  75. Zhou R, Moshgabadi N, Adams KL (2011) Extensive changes to alternative splicing patterns following allopolyploidy in natural and resynthesized polyploids. Proc Natl Acad Sci USA 108:16122–16127CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Key Laboratory of Molecular Epigenetics of the Ministry of Education (MOE)Northeast Normal UniversityChangchunChina
  2. 2.Department of AgronomyPurdue UniversityWest LafayetteUSA
  3. 3.Jilin Academy of Agricultural Sciences (JAAS)ChangchunChina
  4. 4.Department of Crop and Soil SciencesWashington State UniversityPullmanUSA

Personalised recommendations