Origin of a Subgenome and Genome Evolution of Allotetraploid Cotton Species

Cotton (Gossypium spp.) is one of the most important economic crops in the world and also a major source of natural fiber, oil, and protein. The morphology of cotton species varies from trailing herbaceous perennials to trees <10 m. Like other important crops, modern cotton cultivars are polyploids and have gone through polyploidization, evolution, and domestication. The cotton genus comprises approximately 45 diploid (2n = 2x = 26) and seven tetraploid species (2n = 4x = 52) (Guan et al., 2014Guan X. Song Q. Chen Z.J. Polyploidy and small RNA regulation of cotton fiber development.Trends Plant Sci. 2014; 19: 516-528Abstract Full Text Full Text PDF PubMed Scopus (36) Google Scholar). In addition, global diversification of the genus results in eight different genome groups (namely A–G and K) with respect to diploid species (Wendel et al., 2012Wendel J.F. Flagel L.E. Adams K.L. Jeans, genes, and genomes: cotton as a model for studying polyploidy.in: Soltis P.S. Soltis D.E. Polyploidy and Genome Evolution. Springer, Berlin2012: 181-207Crossref Scopus (46) Google Scholar). Although genomes of diploids differ from each other with up to 2-fold differences in size, A and D genomes display comparable gene order and colinearity. A and D genomes diverged about 5–10 million years ago (MYA), while Gossypium allopolyploid (AD) species emerged in the last 1–2 MYA, resulting from polyploidization (Li et al., 2015Li F. Fan G. Lu C. Xiao G. Zou C. Kohel R.J. Ma Z. Shang H. Ma X. Wu J. et al.Genome sequence of cultivated upland cotton (Gossypium hirsutum TM-1) provides insights into genome evolution.Nat. Biotechnol. 2015; 33: 524-530Crossref PubMed Scopus (595) Google Scholar; Zhang et al., 2015Zhang T. Hu Y. Jiang W. Fang L. Guan X. Chen J. Zhang J. Saski C.A. Scheffler B.E. Stelly D.M. et al.Sequencing of allotetraploid cotton (Gossypium hirsutum L. acc. TM-1) provides a resource for fiber improvement.Nat. Biotechnol. 2015; 33: 531-537Crossref PubMed Scopus (869) Google Scholar). Consistently, among these primary cultivated species, the allopolyploid cotton G. hirsutum, rather than diploid cotton species, is widely cultivated and contributes to more than 90% of global cotton fiber production. Therefore, revealing the evolution and domestication of Gossypium from diploid to tetraploid cotton species commonly cultivated can provide us with a classic paradigm to understand the formation processes of allopolyploidization that universally occurred in most of our cultivated crops during their evolution and domestication period. Allotetraploid G. hirsutum originated from the genomic hybridization between an ancestral African diploid with an A genome and an American diploid species with a D genome (Paterson et al., 2012Paterson A.H. Wendel J.F. Gundlach H. Guo H. Jenkins J. Jin D. Llewellyn D. Showmaker K.C. Shu S. Udall J. et al.Repeated polyploidization of Gossypium genomes and the evolution of spinnable cotton fibres.Nature. 2012; 492: 423-427Crossref PubMed Scopus (736) Google Scholar). As for the two donors of allotetraploid, the diploid A genome species rather than the D genome species are cultivated with spinnable fibers. The genome of allotetraploid species G. hirsutum (AD)1 is composed of two sets of homologous chromosomes (At and Dt subgenomes). The Dt subgenome was considered to be inherited from the donor G. raimondii (D5), since it is much closer to this subgenome than to other diploid D genome species (Hu et al., 2019Hu Y. Chen J. Fang L. Zhang Z. Ma W. Niu Y. Ju L. Deng J. Zhao T. Lian J. et al.Gossypium barbadense and Gossypium hirsutum genomes provide insights into the origin and evolution of allotetraploid cotton.Nat. Genet. 2019; 51: 739-748Crossref PubMed Scopus (173) Google Scholar). Unlike the numerous diploid D genome species, there are only two extant A genome species in the world, namely G. herbaceum (A1) and G. arboreum (A2). Genetic and morphological investigations imply that G. arboreum may be the donor of the At subgenome. However, cytogenetic evidence indicates that G. herbaceum is much closer to the At subgenome than G. arboreum. Although the genome sequences of G. arboreum, G. raimondii, G. hirsutum, and G. barbadense have been revealed, controversy regarding which species is the actual donor of the At subgenome persists. Recently, Huang et al., 2020Huang G. Wu Z. Percy R.G. Bai M. Li Y. Frelichowski J.E. Hu J. Wang K. Yu J.Z. Zhu Y. Genome sequence of Gossypium herbaceum and genome updates of Gossypium arboreum and Gossypium hirsutum provide insights into cotton A-genome evolution.Nat. Genet. 2020; 52: 516-524Crossref PubMed Scopus (50) Google Scholar assembled A1-genome var. africanum, and updated the A2-genome cultivar Shixiya1 and the (AD)1-genome genetic standard line Texas Marker-1 (TM-1), and revealed the origin and evolution of the A genome and At subgenome. They developed a novel method, named Gaussian probability density function, to overcome the pitfall of previous analysis methods and detect new TE burst events in cotton genomes. It showed that the actual donor of the At subgenome was neither A1 nor A2, because the A1-A2 clade and the At subgenome had a sister group relationship, and the distance from D5 to At was much smaller than that from D5 to its previously considered common ancestor (A1 or A2), which is indicated by the fact that about 30.54% of the single nucleotide polymorphisms (SNPs) of the At subgenome were identical to those in the D5 genome, while only 20.52% and 20.04% of SNPs of At were found in A1 and A2 genomes, respectively. Furthermore, both A1 and A2 genomes evolved independently, with no ancestor-progeny relationship and A1 var. africanum is the only living ancestor of A1 accessions. Molecular phylogenetic analysis showed that the allotetraploid formation preceded the divergence of A1 and A2 species. These results suggest that the allotetraploid cotton originated from the hybridization of a common A genome ancestor (A0) with the D5 genome about 1.0–1.6 MYA, and that two A genomes (A1 and A2) branched off from a shared ancestor A0 approximately 0.7 MYA (Figure 1). After interspecific hybridization and genome doubling of the Old World A genome and the New World D genome ancestors, allotetraploid Gossypium species were divided into seven different polyploid lineages separately, including G. hirsutum (AD)1, G. barbadense (AD)2, G. tomentosum (AD)3, G. mustelinum (AD)4, and G. darwinii (AD)5, G. ekmanianum (AD)6 and G. stephensii (AD)7 (Gallagher et al., 2017Gallagher J.P. Grover C.E. Rex K. Moran M. Wendel J.F. A new species of cotton from Wake Atoll, Gossypium stephensii (Malvaceae).Syst. Bot. 2017; 42: 115-123Crossref Scopus (34) Google Scholar). To get an insight into the evolution of polyploid cotton species and their domestication history, high-quality genomes of five allotetraploid cotton species were constructed using complementary whole-genome shotgun strategies (Chen et al., 2020Chen Z.J. Sreedasyam A. Ando A. Song Q. De Santiago L.M. Hulse-Kemp A.M. Ding M. Ye W. Kirkbride R.C. Jenkins J. et al.Genomic diversifications of five Gossypium allopolyploid species and their impact on cotton improvement.Nat. Genet. 2020; 52: 525-533Crossref PubMed Scopus (44) Google Scholar). Whole-genome comparative analyses revealed that five allotetraploid species had a monophyletic origin with a common ancestor, which gradually branched into five species within 0.20–0.63 MYA (Figure 1). The genomes of these species were diversified by the dynamic exchanges of subgenomic transposable elements, which facilitated the genome-size equilibration after the emergence of allopolyploidy. Despite a wide geographic distribution and diversification, gene content and genomic synteny of allotetraploid cotton species were conserved during the hybridization, polyploidization, and domestication processes. G. hirsutum and G. barbadense have been independently domesticated into annualized crops in the last 8000 years. Numerous unique genes associated with fiber development and seed oil were enriched in domesticated species, with different phenotypic traits in terms of fiber length, flower morphology, and many pollination- and reproduction-related genes in wild cottons. Fiber length and quality of G. hirsutum, characterized by wide adaptability and high yield potential, and G. barbadense, which has high-quality and extra-long fibers for the production of specialty cotton textiles, vary significantly. These distinct domestication traits were caused by the specific expression and divergent subfunctionalization of homologous genes after the domestication process of allotetraploid cotton species. Interestingly, interspecific hybridization of wild and cultivated cotton species was able to overcome recombination suppression, which provides a practical tactic to break up the bottle neck of traditional crop breeding. Taken together, two recent studies along with previous knowledge revealed the origin, evolution, and domestication of Gossypium, which highlight that the allotetraploid ancestor emerged approximately 1.0–1.6 MYA by the interspecific hybridization between the A0 genome and the D5 genome, and the A0 genome then diverged into two diploid A genomes (A1 and A2) 0.7 MYA. After that, the allotetraploid common ancestor was divided into five polyploid lineages within 0.20–0.63 MYA (Figure 1). Cotton genomic analysis revealed that an abrupt 5- to 6-fold whole-genome duplication plus allopolyploidy led to about 30- to 36-fold gene duplication of ancestral angiosperm genes in allotetraploid cottons (Paterson et al., 2012Paterson A.H. Wendel J.F. Gundlach H. Guo H. Jenkins J. Jin D. Llewellyn D. Showmaker K.C. Shu S. Udall J. et al.Repeated polyploidization of Gossypium genomes and the evolution of spinnable cotton fibres.Nature. 2012; 492: 423-427Crossref PubMed Scopus (736) Google Scholar), which results in the genetic complexity and confers emergent properties, such as the higher fiber productivity and quality of tetraploid cottons compared with diploid cottons. Cotton population studies showed that cotton has narrow genetic diversities perhaps because a large percentage of genetic diversities might have been lost during the domestication processes, which is often a bottle neck for cotton inbreeding practice (Fang et al., 2017Fang L. Wang Q. Hu Y. Jia Y. Chen J. Liu B. Zhang Z. Guan X. Chen S. Zhou B. et al.Genomic analyses in cotton identify signatures of selection and loci associated with fiber quality and yield traits.Nat. Genet. 2017; 49: 1089-1098Crossref PubMed Scopus (152) Google Scholar; Wang et al., 2019Wang K. Wang D. Zheng X. Qin A. Zhou J. Guo B. Chen Y. Wen X. Ye W. Zhou Y. et al.Multi-strategic RNA-seq analysis reveals a high-resolution transcriptional landscape in cotton.Nat. Commun. 2019; 10: 4714Crossref PubMed Scopus (21) Google Scholar). Taking advantage of interspecies hybridization and polyploidization, which relies on the elaborately established evolutionary path of certain crop lineage with its diploid and allotetraploid accessions, would help us bypass the limitation of this traditional breeding to achieve the goal of trait improvement. In future, genome sequencing of the rest of the diploid wild cotton species (i.e., B–G and K) will further complete the jigsaw puzzle of cotton evolution history by adding the missing pieces. Therefore, with the help of genetic manipulation (e.g., CRISPR-Cas9), high-quality genomes of the wild cotton species will provide us with a much more elaborate blueprint to remake and acquire new cultivated cotton species with improved disease resistance and environmental adaptability on the basis of reservation of the fine agronomic traits: higher fiber quality and yield. This work is supported by the Natural Science Basic Research Plan in the Shaanxi Province of China ( 2019JQ-062 and 2020JQ-410 ), Shaanxi Youth Entrusted Talent Program ( 20190205 ), Shaanxi Postdoctoral Project ( 2018BSHYDZZ76 ), Fundamental Research Funds for Central Universities ( GK201903064 , GK202002005 and GK202001004 ), Young Elite Scientists Sponsorship Program by CAST ( 2019-2021QNRC001 ) and State Key Laboratory of Cotton Biology Open Fund ( CB2020A12 ).