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Homoeologous exchanges occur through intragenic recombination generating novel transcripts and proteins in wheat and other polyploids.

ABSTRACT: Recombination between homeologous chromosomes, also known as homeologous exchange (HE), plays a significant role in shaping genome structure and gene expression in interspecific hybrids and allopolyploids of several plant species. However, the molecular mechanisms that govern HEs are not well understood. Here, we studied HE events in the progeny of a nascent allotetraploid (genome AADD) derived from two diploid progenitors of hexaploid bread wheat using cytological and whole-genome sequence analyses. In total, 37 HEs were identified and HE junctions were mapped precisely. HEs exhibit typical patterns of homologous recombination hotspots, being biased toward low-copy, subtelomeric regions of chromosome arms and showing association with known recombination hotspot motifs. But, strikingly, while homologous recombination preferentially takes place upstream and downstream of coding regions, HEs are highly enriched within gene bodies, giving rise to novel recombinant transcripts, which in turn are predicted to generate new protein fusion variants. To test whether this is a widespread phenomenon, a dataset of high-resolution HE junctions was analyzed for allopolyploid Brassica, rice, Arabidopsis suecica, banana, and peanut. Intragenic recombination and formation of chimeric genes was detected in HEs of all species and was prominent in most of them. HE thus provides a mechanism for evolutionary novelty in transcript and protein sequences in nascent allopolyploids.

SUBMITTER: Zhang Z

PROVIDER: S-EPMC7321986 | biostudies-literature | 2020 Jun

REPOSITORIES: biostudies-literature

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Homoeologous exchanges occur through intragenic recombination generating novel transcripts and proteins in wheat and other polyploids.

Zhang Zhibin Z Gou Xiaowan X Xun Hongwei H Bian Yao Y Ma Xintong X Li Juzuo J Li Ning N Gong Lei L Feldman Moshe M Liu Bao B Levy Avraham A AA

Proceedings of the National Academy of Sciences of the United States of America 20200609 25

Recombination between homeologous chromosomes, also known as homeologous exchange (HE), plays a significant role in shaping genome structure and gene expression in interspecific hybrids and allopolyploids of several plant species. However, the molecular mechanisms that govern HEs are not well understood. Here, we studied HE events in the progeny of a nascent allotetraploid (genome AADD) derived from two diploid progenitors of hexaploid bread wheat using cytological and whole-genome sequence anal ...[more]

PMID: 32518116

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Project description:IntroductionMeiotic recombination (or crossover, CO) is essential for gamete fertility as well as for alleles and genes reshuffling that is at the heart of plant breeding. However, CO remains a limited event, which strongly hampers the rapid production of original and improved cultivars. RecQ4 is a gene encoding a helicase protein that, when mutated, contributes to improve recombination rate in all species where it has been evaluated so far.MethodsIn this study, we developed wheat (Triticum aestivum L.) triple mutant (TM) for the three homoeologous copies of TaRecQ4 as well as mutants for two copies and heterozygous for the last one (Htz-A, Htz-B, Htz-D).ResultsPhenotypic observation revealed a significant reduction of fertility and pollen viability in TM and Htz-B plants compared to wild type plants suggesting major defects during meiosis. Cytogenetic analyses of these plants showed that complete absence of TaRecQ4 as observed in TM plants, leads to chromosome fragmentation during the pachytene stage, resulting in problems in the segregation of chromosomes during meiosis. Htz-A and Htz-D mutants had an almost normal meiotic progression indicating that both TaRecQ4-A and TaRecQ4-D copies are functional and that there is no dosage effect for TaRecQ4 in bread wheat. On the contrary, the TaRecQ4-B copy seems knocked-out, probably because of a SNP leading to a Threonine>Alanine change at position 539 (T539A) of the protein, that occurs in the crucial helicase ATP bind/DEAD/ResIII domain which unwinds nucleic acids. Occurrence of numerous multivalents in TM plants suggests that TaRecQ4 could also play a role in the control of homoeologous recombination.DiscussionThese findings provide a foundation for further molecular investigations into wheat meiosis regulation to fully understand the underlying mechanisms of how TaRecQ4 affects chiasma formation, as well as to identify ways to mitigate these defects and enhance both homologous and homoeologous recombination efficiency in wheat.

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Homoeologous exchanges occur through intragenic recombination generating novel transcripts and proteins in wheat and other polyploids.

Publications

Homoeologous exchanges occur through intragenic recombination generating novel transcripts and proteins in wheat and other polyploids.

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