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Nucleotide diversity in the two co-resident genomes of allopolyploid cotton

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Abstract

Genetic diversity within and among populations lies at the heart of evolution. Unraveling the extent to which each intrinsic or extrinsic factor determines levels of diversity among genes, populations, and species is challenging, given the difficulty of isolating any single potentially important variable from all others. Allopolyploid species provide an opportunity to disentangle external and intrinsic factors, as the two (or more) homoeologous genomes co-occur in the same nucleus, often exhibiting high collinearity along homoeologous chromosomes. Here we evaluate the pace of molecular evolution and intraspecific, intragenomic diversity in two species of allopolyploid Gossypium, G. hirsutum and G. barbadense, using several hundred genes sequenced from multiple accessions of each species. Genic diversity in both species is low, having been influenced both by the polyploid bottleneck and a domestication bottleneck (for cultivated accessions), but with a directional bias in homoeolog diversity favoring the same genome in both allopolyploids. Total diversity is remarkably similar for the two homoeologous genomes overall, but the two copies of many gene pairs have accumulated statistically different diversity levels, and in a biased fashion with respect to genome. Domesticated accessions show reduced diversity in both genomes, as expected, but with a much greater reduction in one of the two homoeologous genomes. Furthermore, this biased reduction affects opposite homoeologous genomes in the two species. Interspecific introgression has played a role in shaping diversity within each species. Introgression was only detected for certain accessions, and only from G. barbadense into G. hirsutum in one of the two co-resident genomes.

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Acknowledgements

We thank Guanjing Hu and Mark A. Arick for technical assistance; Daniel Ilut, John Nason, and Matthew Hufford for analytical advice; and Richard Percy for assistance in selecting the G. barbadense accessions. The authors are supported by the USDA-ARS and grants from the National Science Foundation, Supima, and Cotton Incorporated. J. P. Gallagher is supported by National Science Foundation Graduate Research Fellowship DGE1247194.

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Authors and Affiliations

  1. Iowa State University, Ames, IA, 50011, USA

    Corrinne E. Grover, Joseph P. Gallagher & Jonathan F. Wendel

  2. INRA UR1052 GAFL, Avignon, France

    Emmanuel P. Szadkowski

  3. Brigham Young University, Provo, UT, 84602, USA

    Justin T. Page & Joshua A. Udall

  4. Plant Breeding and Genetics Section, School of Integrative Plant Science, Cornell University, Ithaca, NY, 14853, USA

    Michael A. Gore

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Correspondence to Corrinne E. Grover.

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Handling editor: Ales Kovarik.

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Online Resource 1. Accessions used for sequence capture, including G. hirsutum and G. barbadense, as well as relevant outgroup species. When available, Germplasm Resources Information Network (GRIN) numbers, cultivated status, and country of origin are given.

Online Resource 2. Identification of genes recovered via sequence capture for both Illumina and Roche sequencing, given as G. raimondii (Paterson et al. 2012) homologs. Arabidopsis thaliana homologs and descriptions are also listed.

Online Resource 3. Assembled sequence capture genes associated with the Gossypium hirsutum and G. barbadense data sets.

Online Resource 4. The number of reads mapped for each accession and used in the present analyses.

Online Resource 5. Polyploid-to-diploid chromosomal equivalency, i.e., homologous chromosomes between diploid progenitor species and polyploid species in cotton.

Online Resource 6. The number of significant comparisons between the diversity (π) of AT and DT homoeologs, partitioned into wild and domesticated accessions.

Online Resource 7. Summary of Patterson’s D statistic for the A and D genome of Gossypium hirsutum.

Online Resource 8. Summary of Patterson’s D statistic for the A and D genome of Gossypium barbadense.

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Grover, C.E., Gallagher, J.P., Szadkowski, E.P. et al. Nucleotide diversity in the two co-resident genomes of allopolyploid cotton. Plant Syst Evol 303, 1021–1042 (2017). https://doi.org/10.1007/s00606-017-1411-1

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