Genomic diversifications of five Gossypium allopolyploid species and their impact on cotton improvement.
Journal
Nature genetics
ISSN: 1546-1718
Titre abrégé: Nat Genet
Pays: United States
ID NLM: 9216904
Informations de publication
Date de publication:
05 2020
05 2020
Historique:
received:
03
02
2020
accepted:
16
03
2020
pubmed:
22
4
2020
medline:
4
8
2020
entrez:
22
4
2020
Statut:
ppublish
Résumé
Polyploidy is an evolutionary innovation for many animals and all flowering plants, but its impact on selection and domestication remains elusive. Here we analyze genome evolution and diversification for all five allopolyploid cotton species, including economically important Upland and Pima cottons. Although these polyploid genomes are conserved in gene content and synteny, they have diversified by subgenomic transposon exchanges that equilibrate genome size, evolutionary rate heterogeneities and positive selection between homoeologs within and among lineages. These differential evolutionary trajectories are accompanied by gene-family diversification and homoeolog expression divergence among polyploid lineages. Selection and domestication drive parallel gene expression similarities in fibers of two cultivated cottons, involving coexpression networks and N
Identifiants
pubmed: 32313247
doi: 10.1038/s41588-020-0614-5
pii: 10.1038/s41588-020-0614-5
pmc: PMC7203012
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
525-533Subventions
Organisme : NIGMS NIH HHS
ID : P20 GM103476
Pays : United States
Références
Muller, H. J. Why polyploidy is rarer in animals than in plants. Am. Nat. 59, 346–353 (1925).
Soltis, D. E., Visger, C. J. & Soltis, P. S. The polyploidy revolution then…and now: Stebbins revisited. Am. J. Bot. 101, 1057–1078 (2014).
pubmed: 25049267
Wendel, J. F. The wondrous cycles of polyploidy in plants. Am. J. Bot. 102, 1753–1756 (2015).
pubmed: 26451037
Leitch, A. R. & Leitch, I. J. Genomic plasticity and the diversity of polyploid plants. Science 320, 481–483 (2008).
pubmed: 18436776
Chen, Z. J. Genetic and epigenetic mechanisms for gene expression and phenotypic variation in plant polyploids. Annu. Rev. Plant Biol. 58, 377–406 (2007).
pubmed: 17280525
pmcid: 1949485
Chen, Z. J. et al. Toward sequencing cotton (Gossypium) genomes. Plant Physiol. 145, 1303–1310 (2007).
pubmed: 18056866
pmcid: 2151711
International Wheat Genome Sequencing Consortium et al. Shifting the limits in wheat research and breeding using a fully annotated reference genome. Science 361, eaar7191 (2018).
Chalhoub, B. et al. Early allopolyploid evolution in the post-Neolithic Brassica napus oilseed genome. Science 345, 950–953 (2014).
pubmed: 25146293
Bevan, M. W. et al. Genomic innovation for crop improvement. Nature 543, 346–354 (2017).
pubmed: 28300107
Xiong, Z., Gaeta, R. T. & Pires, J. C. Homoeologous shuffling and chromosome compensation maintain genome balance in resynthesized allopolyploid Brassica napus. Proc. Natl Acad. Sci. USA 108, 7908–7913 (2011).
pubmed: 21512129
Chester, M. et al. Extensive chromosomal variation in a recently formed natural allopolyploid species, Tragopogon miscellus (Asteraceae). Proc. Natl Acad. Sci. USA 109, 1176–1181 (2012).
pubmed: 22228301
Feldman, M. et al. Rapid elimination of low-copy DNA sequences in polyploid wheat: a possible mechanism for differentiation of homoeologous chromosomes. Genetics 147, 1381–1387 (1997).
pubmed: 9383078
pmcid: 1208259
Ding, M. & Chen, Z. J. Epigenetic perspectives on the evolution and domestication of polyploid plants and crops. Curr. Opin. Plant Biol. 42, 37–48 (2018).
pubmed: 29502038
pmcid: 6058195
Wendel, J. F. & Grover, C. E. in Cotton 2nd edn (eds Fang, D. D. & Percey, R. G.), Vol. 57, 25–44 (Agronomy Monograph 57, 2015).
Splitstoser, J. C., Dillehay, T. D., Wouters, J. & Claro, A. Early pre-Hispanic use of indigo blue in Peru. Sci. Adv. 2, e1501623 (2016).
pubmed: 27652337
pmcid: 5023320
Lu, K. et al. Whole-genome resequencing reveals Brassica napus origin and genetic loci involved in its improvement. Nat. Commun. 10, 1154 (2019).
pubmed: 30858362
pmcid: 6411957
Grover, C. E. et al. Re-evaluating the phylogeny of allopolyploid Gossypium L. Mol. Phylogenet. Evol. 92, 45–52 (2015).
pubmed: 26049043
Bailey-Serres, J., Parker, J. E., Ainsworth, E. A., Oldroyd, G. E. D. & Schroeder, J. I. Genetic strategies for improving crop yields. Nature 575, 109–118 (2019).
pubmed: 31695205
pmcid: 7024682
Eshed, Y. & Lippman, Z. B. Revolutions in agriculture chart a course for targeted breeding of old and new crops. Science 366, eaax0025 (2019).
pubmed: 31488704
Paterson, A. H. et al. Repeated polyploidization of Gossypium genomes and the evolution of spinnable cotton fibres. Nature 492, 423–427 (2012).
pubmed: 23257886
Li, F. et al. Genome sequence of the cultivated cotton Gossypium arboreum. Nat. Genet. 46, 567–572 (2014).
pubmed: 24836287
Hu, Y. et al. Gossypium barbadense and Gossypium hirsutum genomes provide insights into the origin and evolution of allotetraploid cotton. Nat. Genet. 51, 739–748 (2019).
pubmed: 30886425
Wang, M. et al. Reference genome sequences of two cultivated allotetraploid cottons, Gossypium hirsutum and Gossypium barbadense. Nat. Genet. 51, 224–229 (2019).
pubmed: 30510239
Li, F. et al. Genome sequence of cultivated Upland cotton (Gossypium hirsutum TM-1) provides insights into genome evolution. Nat. Biotechnol. 33, 524–530 (2015).
pubmed: 25893780
Zhang, T. et al. Sequencing of allotetraploid cotton (Gossypium hirsutum L. acc. TM-1) provides a resource for fiber improvement. Nat. Biotechnol. 33, 531–537 (2015).
pubmed: 25893781
Liu, X. et al. Gossypium barbadense genome sequence provides insight into the evolution of extra-long staple fiber and specialized metabolites. Sci. Rep. 5, 14139 (2015).
pubmed: 26420475
pmcid: 4588572
Paterson, A. H. et al. The Sorghum bicolor genome and the diversification of grasses. Nature 457, 551–556 (2009).
pubmed: 19189423
Gordon, S. P. et al. Extensive gene content variation in the Brachypodium distachyon pan-genome correlates with population structure. Nat. Commun. 8, 2184 (2017).
pubmed: 29259172
pmcid: 5736591
Grover, C. E., Grupp, K. K., Wanzek, R. J. & Wendel, J. F. Assessing the monophyly of polyploid Gossypium species. Plant Syst. Evol. 298, 1177–1183 (2012).
Wendel, J. F., Brubaker, C., Alvarez, I., Cronn, R. & Stewart, J. M. in Genetics and Genomics of Cotton. Plant Genetics and Genomics: Crops and Models Vol. 3 (ed. Paterson, A. H.) 3–22 (Springer, 2009).
Brubaker, C. L., Bourland, F. M. & Wendel, J. F. in Cotton: Origin, History, Technology, and Production (eds Smith, C. W. & Cothren, J. T.) 3–32 (John Wiley & Sons, 1999).
Kulkarni, V. N., Khadi, B. M., Maralappanavar, M. S., Deshapande L. A. & Narayanan, S. S. in Genetics and Genomics of Cotton. Plant Genetics and Genomics: Crops and Models Vol. 3 (ed. Paterson, A. H.) 69–97 (Springer, 2009).
Lynch, M. & Conery, J. S. The evolutionary fate and consequences of duplicate genes. Science 290, 1151–1155 (2000).
pubmed: 11073452
Novikova, P. Y. et al. Genome sequencing reveals the origin of the allotetraploid Arabidopsis suecica. Mol. Biol. Evol. 34, 957–968 (2017).
pubmed: 28087777
pmcid: 5400380
Bertioli, D. J. et al. The genome sequence of segmental allotetraploid peanut Arachis hypogaea. Nat. Genet. 51, 877–884 (2019).
pubmed: 31043755
Zhang, J. et al. Extensive sequence divergence between the reference genomes of two elite indica rice varieties Zhenshan 97 and Minghui 63. Proc. Natl Acad. Sci. USA 113, E5163–E5171 (2016).
pubmed: 27535938
Zhao, X. P. et al. Dispersed repetitive DNA has spread to new genomes since polyploid formation in cotton. Genome Res. 8, 479–492 (1998).
pubmed: 9582192
Ma, Z. et al. Resequencing a core collection of upland cotton identifies genomic variation and loci influencing fiber quality and yield. Nat. Genet. 50, 803–813 (2018).
pubmed: 29736016
Jones, J. D. & Dangl, J. L. The plant immune system. Nature 444, 323–329 (2006).
pubmed: 17108957
Phillips, A. Z. et al. Genomics-enabled analysis of the emergent disease cotton bacterial blight. PLoS Genet. 13, e1007003 (2017).
pubmed: 28910288
pmcid: 5614658
Zheng, D. et al. Histone modifications define expression bias of homoeologous genomes in allotetraploid cotton. Plant Physiol. 172, 1760–1771 (2016).
pubmed: 27637746
pmcid: 5100776
Schroder, R., Atkinson, R. G. & Redgwell, R. J. Re-interpreting the role of endo-beta-mannanases as mannan endotransglycosylase/hydrolases in the plant cell wall. Ann. Bot. 104, 197–204 (2009).
pubmed: 19454593
pmcid: 2710900
Trainin, T., Shmuel, M. & Delmer, D. P. In vitro prenylation of the small GTPase Rac13 of cotton. Plant Physiol. 112, 1491–1497 (1996).
pubmed: 12226460
pmcid: 158081
Tuttle, J. R. et al. Metabolomic and transcriptomic insights into how cotton fiber transitions to secondary wall synthesis, represses lignification, and prolongs elongation. BMC Genomics 16, 477 (2015).
pubmed: 26116072
pmcid: 4482290
Sun, Y. et al. Brassinosteroid regulates fiber development on cultured cotton ovules. Plant Cell Physiol. 46, 1384–1391 (2005).
pubmed: 15958497
Song, Q., Guan, X. & Chen, Z. J. Dynamic roles for small RNAs and DNA methylation during ovule and fiber development in allotetraploid cotton. PLoS Genet. 11, e1005724 (2015).
pubmed: 26710171
pmcid: 4692501
Shen, L., Liang, Z., Wong, C. E. & Yu, H. Messenger RNA modifications in plants. Trends Plant Sci. 24, 328–341 (2019).
pubmed: 30745055
Cifuentes, M. et al. Repeated polyploidy drove different levels of crossover suppression between homoeologous chromosomes in Brassica napus allohaploids. Plant Cell 22, 2265–2276 (2010).
pubmed: 20639447
pmcid: 2929116
Hinze, L. L. et al. Diversity analysis of cotton (Gossypium hirsutum L.) germplasm using the CottonSNP63K Array. BMC Plant Biol. 17, 37 (2017).
pubmed: 28158969
pmcid: 5291959
Purcell, S. et al. PLINK: a tool set for whole-genome association and population-based linkage analyses. Am. J. Hum. Genet. 81, 559–575 (2007).
pubmed: 17701901
pmcid: 1950838
Mirouze, M. et al. Loss of DNA methylation affects the recombination landscape in Arabidopsis. Proc. Natl Acad. Sci. USA 109, 5880–5885 (2012).
pubmed: 22451936
Yelina, N. E. et al. DNA methylation epigenetically silences crossover hot spots and controls chromosomal domains of meiotic recombination in Arabidopsis. Genes Dev. 29, 2183–2202 (2015).
pubmed: 26494791
pmcid: 4617981
Song, Q., Zhang, T., Stelly, D. M. & Chen, Z. J. Epigenomic and functional analyses reveal roles of epialleles in the loss of photoperiod sensitivity during domestication of allotetraploid cottons. Genome Biol. 18, 99 (2017).
pubmed: 28558752
pmcid: 5450403
Yin, D. et al. Comparison of Arachis monticola with diploid and cultivated tetraploid genomes reveals asymmetric subgenome evolution and improvement of peanut. Adv. Sci. 7, 1901672 (2020).
Soltis, D. E. & Soltis, P. S. Polyploidy: recurrent formation and genome evolution. Trends Ecol. Evol. 14, 348–352 (1999).
pubmed: 10441308
Riley, R. & Chapman, V. Genetic control of cytologically diploid behaviour of hexaploid wheat. Nature 182, 713–715 (1958).
Griffiths, S. et al. Molecular characterization of Ph1 as a major chromosome pairing locus in polyploid wheat. Nature 439, 749–752 (2006).
pubmed: 16467840
Saski, C. A. et al. Sub genome anchored physical frameworks of the allotetraploid Upland cotton (Gossypium hirsutum L.) genome, and an approach toward reference-grade assemblies of polyploids. Sci. Rep. 7, 15274 (2017).
pubmed: 29127298
pmcid: 5681701
Xiao, C. L. et al. MECAT: fast mapping, error correction, and de novo assembly for single-molecule sequencing reads. Nat. Methods 14, 1072–1074 (2017).
pubmed: 28945707
Chin, C. S. et al. Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data. Nat. Methods 10, 563–569 (2013).
Durand, N. C. et al. Juicebox provides a visualization system for Hi-C contact maps with unlimited zoom. Cell Syst. 3, 99–101 (2016).
pubmed: 5596920
pmcid: 5596920
Robinson, J. T. et al. Juicebox.js provides a cloud-based visualization system for Hi-C data. Cell Syst. 6, 256–258.E1 (2018).
pubmed: 29428417
pmcid: 6047755
Krumsiek, J., Arnold, R. & Rattei, T. Gepard: a rapid and sensitive tool for creating dotplots on genome scale. Bioinformatics 23, 1026–1028 (2007).
pubmed: 17309896
Li, H. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. Preprint at https://arxiv.org/abs/1303.3997 (2013).
Li, H. Minimap2: pairwise alignment for nucleotide sequences. Bioinformatics 34, 3094–3100 (2018).
pubmed: 29750242
pmcid: 6137996
Goel, M., Sun, H., Jiao, W.-B. & Schneeberger, K. Identification of syntenic and rearranged regions from whole-genome assemblies. Preprint at bioRxiv https://doi.org/10.1101/546622 (2019).
Emms, D. M. & Kelly, S. OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy. Genome Biol. 16, 157 (2015).
pubmed: 26243257
pmcid: 4531804
Cohen, O. & Pupko, T. Inference of gain and loss events from phyletic patterns using stochastic mapping and maximum parsimony–a simulation study. Genome Biol. Evol. 3, 1265–1275 (2011).
pubmed: 21971516
pmcid: 3215202
Edgar, R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792–1797 (2004).
pubmed: 15034147
pmcid: 390337
Wang, D., Zhang, Y., Zhang, Z., Zhu, J. & Yu, J. KaKs_Calculator 2.0: a toolkit incorporating gamma-series methods and sliding window strategies. Genomics Proteomics Bioinformatics 8, 77–80 (2010).
pubmed: 20451164
pmcid: 5054116
Ellinghaus, D., Kurtz, S. & Willhoeft, U. LTRharvest, an efficient and flexible software for de novo detection of LTR retrotransposons. BMC Bioinformatics 9, 18 (2008).
pubmed: 18194517
pmcid: 2253517
Xu, Z. & Wang, H. LTR_FINDER: an efficient tool for the prediction of full-length LTR retrotransposons. Nucleic Acids Res. 35, W265–W268 (2007).
pubmed: 17485477
pmcid: 1933203
Ou, S. & Jiang, N. LTR_retriever: a highly accurate and sensitive program for identification of long terminal repeat retrotransposons. Plant Physiol. 176, 1410–1422 (2018).
pubmed: 29233850
Li, W. & Godzik, A. Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22, 1658–1659 (2006).
pubmed: 16731699
pmcid: 16731699
Chojnacki, S., Cowley, A., Lee, J., Foix, A. & Lopez, R. Programmatic access to bioinformatics tools from EMBL-EBI update: 2017. Nucleic Acids Res. 45, W550–W553 (2017).
pubmed: 28431173
pmcid: 5570243
Eddy, S. R. Accelerated profile HMM searches. PLoS Comput. Biol. 7, e1002195 (2011).
pubmed: 22039361
pmcid: 3197634
Robinson, M. D., McCarthy, D. J. & Smyth, G. K. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26, 139–140 (2010).
pubmed: 19910308
Trapnell, C. et al. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat. Protoc. 7, 562–578 (2012).
pubmed: 22383036
pmcid: 3334321
Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014).
pubmed: 4302049
pmcid: 4302049
Alexa, A. & Rahenfuhrer, J. topGO: Enrichment analysis for Gene Ontology. R package version 2.32.0 (2016).
R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2018).
Dominissini, D., Moshitch-Moshkovitz, S., Salmon-Divon, M., Amariglio, N. & Rechavi, G. Transcriptome-wide mapping of N
pubmed: 23288318
Kim, D. et al. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 14, R36 (2013).
pubmed: 4053844
pmcid: 4053844
Meng, J., Cui, X. D., Rao, M. K., Chen, Y. D. & Huang, Y. F. Exome-based analysis for RNA epigenome sequencing data. Bioinformatics 29, 1565–1567 (2013).
pubmed: 23589649
pmcid: 3673212
Quinlan, A. R. & Hall, I. M. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841–842 (2010).
pubmed: 20110278
pmcid: 20110278
Liu, B. & Davis, T. M. Conservation and loss of ribosomal RNA gene sites in diploid and polyploid Fragaria (Rosaceae). BMC Plant Biol. 11, 157 (2011).
pubmed: 22074487
pmcid: 3261831
Unfried, I. & Gruendler, P. Nucleotide sequence of the 5.8S and 25S rRNA genes and of the internal transcribed spacers from Arabidopsis thaliana. Nucleic Acids Res. 18, 4011 (1990).
pubmed: 2100998
pmcid: 331127
Cox, A. V. et al. Comparison of plant telomere locations using a PCR-generated synthetic probe. Ann. Bot. 72, 239–247 (1993).
Hulse-Kemp, A. M. et al. Development of a 63K SNP array for cotton and high-density mapping of intraspecific and interspecific populations of Gossypium spp. Genes Genomes Genet. 5, 1187–1209 (2015).
Camacho, C. et al. BLAST plus: architecture and applications. BMC Bioinformatics 10, 421 (2009).
pubmed: 20003500
pmcid: 20003500
Ulloa, M., Hulse-Kemp, A. M., De Santiago, L. M., Stelly, D. M. & Burke, J. J. Insights into upland cotton (Gossypium hirsutum L.) genetic recombination based on 3 high-density single-nucleotide polymorphism and a consensus map developed independently with common parents. Genomics Insights 10, 1–15 (2017).
Browning, S. R. & Browning, B. L. Rapid and accurate haplotype phasing and missing-data inference for whole-genome association studies by use of localized haplotype clustering. Am. J. Hum. Genet. 81, 1084–1097 (2007).
pubmed: 17924348
pmcid: 2265661
Korani, W., Clevenger, J. P., Chu, Y. & Ozias-Akins, P. Machine learning as an effective method for identifying true single nucleotide polymorphisms in polyploid plants. Plant Genome 12, 180023 (2019).
Clevenger, J. P., Korani, W., Ozias-Akins, P. & Jackson, S. Haplotype-based genotyping in polyploids. Front. Plant Sci. 9, 564 (2018).
pubmed: 29755500
pmcid: 5932196
Gabriel, S. B. et al. The structure of haplotype blocks in the human genome. Science 296, 2225–2229 (2002).
pubmed: 12029063
Rezvoy, C., Charif, D., Gueguen, L. & Marais, G. A. B. MareyMap: an R-based tool with graphical interface for estimating recombination rates. Bioinformatics 23, 2188–2189 (2007).
pubmed: 17586550
Cleveland, W. S. & Grosse, E. Computational methods for local regression. Stat. Comput. 1, 47–62 (1991).
Wickham, H. ggplot2: Elegant Graphics for Data Analysis (Springer, 2009).
Krueger, F. & Andrews, S. R. Bismark: a flexible aligner and methylation caller for Bisulfite-Seq applications. Bioinformatics 27, 1571–1572 (2011).
pubmed: 21493656
pmcid: 3102221
Akalin, A. et al. methylKit: a comprehensive R package for the analysis of genome-wide DNA methylation profiles. Genome Biol. 13, R87 (2012).
pubmed: 23034086
pmcid: 3491415
Belton, J. M. et al. Hi-C: a comprehensive technique to capture the conformation of genomes. Methods 58, 268–276 (2012).
pubmed: 22652625
Louwers, M., Splinter, E., van Driel, R., de Laat, W. & Stam, M. Studying physical chromatin interactions in plants using chromosome conformation capture (3C). Nat. Protoc. 4, 1216–1229 (2009).
pubmed: 19644461
Servant, N. et al. HiC-Pro: an optimized and flexible pipeline for Hi-C data processing. Genome Biol. 16, 259 (2015).
pubmed: 4665391
pmcid: 4665391