|GUO, HUI - University Of Georgia|
|WANG, XIYIN - University Of Georgia|
|GUNDLACH, HEIDRUN - German Research Center For Environmental Health|
|MAYER, KLAUS - German Research Center For Environmental Health|
|PETERSON, DANIEL - Mississippi State University|
|CHEE, PENG - University Of Georgia|
|PATERSON, ANDREW - University Of Georgia|
Submitted to: Genetics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/5/2014
Publication Date: 8/1/2014
Citation: Guo, H., Wang, X., Gundlach, H., Mayer, K.F., Peterson, D.G., Scheffler, B.E., Chee, P.W., Paterson, A.H. 2014. Extensive and biased intergenomic nonreciprocal DNA exchanges shaped a nascent polyploid genome, Gossypium (cotton). Genetics. 197:1153-1163. do1 1 0.1 534/genetics.114.1 66124/-/DC 1.
Interpretive Summary: Allopolyploidy is a widespread evolutionary mechanism whereby gametes from two closely related species hybridize and the zygote undergoes chromosome doubling to produce a nucleus containing both homologous and homeologous chromosomes. Allopolyploids often exhibit traits that eclipse those seen in their progenitors making them truly ‘more than the sum of their parts.’ Commercial cottons are tetraploids derived from hybridization of A and D genome progenitors 1-2 MYA. Comparison of sequences from putative diploid A and D genome progenitor species with the genome of the commercial tetraploid (AtDt) species Gossypium hirsutum revealed that unidirectional DNA exchanges between homeologous chromosome sets (i.e., homeologous gene conversion events or HeGCE) were the predominant mutational type in the newly formed AtDt tetraploid, far outnumbering random mutations. Over time, HeGCE gradually subsided, with HeGCE declining to rates similar to random mutation during radiation of the nascent polyploid into multiple species, and random mutation dominating within-species polymorphism. Despite occurring in a common nucleus, preservation of HeGCE is asymmetric. At to Dt conversion, creating four copies of the Dt allele, is far more abundant than the reciprocal, enriched in heterochromatin, highly correlated with GC content and transposon distribution, and may silence abundant A-genome-derived retrotransposons. Dt to At conversion is abundant in euchromatin and in genes, frequently reversing losses of gene function. The long-standing observation that ‘recruitment’ of alleles from the non-spinnable-fibered D genome contributes to the superior yield and quality of tetraploid cotton fibers1 may be explained by increased allele dosage from the spinnable-fibered A genome by Dt to At HeGCE during domestication and improvement. HeGCE may compensate for the paucity of reciprocal exchanges in heterochromatin, where genes have ~5x greater richness in Dt to At conversion than adjacent intergenic DNA. Spanning exon-to-gene-sized regions, HeGCE provides a natural non-invasive means of gene transfer with the precision of transformation.
Technical Abstract: Cultivated cotton is composed of a tetraploid genome derived from two ancestral genomes that are related but divergent from each other. The “A” genome is derived from a cotton species that is used for low quality spinnable-fiber production in low production areas and has an African origin. The “D” genome contributor produces little or no useable fibers and has a new world origin. What has always been a mystery is why the tetraploid species that is derived from these two ancestors provides superior fiber. This paper provides some significant insight into possible explanations to the superior nature of tetraploid cotton for fiber production. While interchanges between the “A” and “D” genomes within the tetraploid species has been known for a while the extent was unknown. This paper shows that there is a significant number of changes between the two genomes and the location of the changes appears to be strategic. “A” conversions to the “D” genome occur mainly in the non-genic region of the genome and may lend assistance in silencing “A” genome origin retrotransposons, which can cause significant genome instability. “D” to “A” conversions occur mainly in gene rich regions which in the end can result in four copies of an “A” allele in cultivated cotton. However, the long-standing observation that ‘recruitment’ of alleles from the non-spinnable-fibered “D” genome contributes to the superior yield and quality of tetraploid cotton fibers may be instead explained by increased allele dosage from the spinnable-fibered “A” genome by “D” to “A” conversions during domestication and improvement.