Genomic mosaicism due to homoeologous exchange generates extensive phenotypic diversity in nascent allopolyploids

Wu, Ying
Lin, Fan
Zhou, Yao
Wang, Jie
Sun, Shuai
Wang, Bin
Zhang, Zhibin
Li, Guo
Lin, Xiuyun
Wang, Xutong
Sun, Yue
Dong, Qianli
Xu, Chunming
Gong, Lei
Wendel, Jonathan
Zhang, Zhiwu
Liu, Bao
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Allopolyploidy is an important process in plant speciation, yet newly formed allopolyploid species typically suffer from extreme genetic bottlenecks. One escape from this impasse might be homoeologous meiotic pairing, during which homoeologous exchanges (HEs) generate phenotypically variable progeny. However, the immediate genome-wide patterns and resulting phenotypic diversity generated by HEs remain largely unknown. Here, we analyzed the genome composition of 202 phenotyped euploid segmental allopolyploid individuals from the 4th selfed generation following chromosomal doubling of reciprocal F1 hybrids of crosses between rice subspecies, using whole genome sequencing. We describe rampant occurrence of HEs that, by overcoming incompatibility or conferring superiority of hetero-cytonuclear interactions, generate extensive and individualized genomic mosaicism across the analyzed tetraploids. We show that the resulting homoeolog copy number alteration in tetraploids affects known-function genes and their complex genetic interactions, in the process creating extraordinary phenotypic diversity at the population level following a single initial hybridization. Our results illuminate the immediate genomic landscapes possible in a tetraploid genomic environment, and underscore HE as an important mechanism that fuels rapid phenotypic diversification accompanying the initial stages of allopolyploid evolution.


This is a manuscript of an article published as Wu, Y., Lin, F., Zhou, Y., Wang, J., Sun, S., Wang, B., Zhang, Z., Li, G., Lin, X., Wang, X. and Sun, Y., 2020. Genomic mosaicism due to homoeologous exchange generates extensive phenotypic diversity in nascent allopolyploids. National Science Review (2020). doi: 10.1093/nsr/nwaa277.

nascent allopolyploidy, homoeologous recombination, phenotypic diversity, plant evolution, GWAS, dosage effects, epistasis