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08 08, 2023;21 (1): 168.

Genomic insights into biased allele loss and increased gene numbers after genome duplication in autotetraploid Cyclocarya paliurus.

Rui-Min Yu, Ning Zhang, Bo-Wen Zhang, Yu Liang, Xiao-Xu Pang, Lei Cao, Yi-Dan Chen, Wei-Ping Zhang, Yang Yang, Da-Yong Zhang, Er-Li Pang, Wei-Ning Bai
Author Information
  1. Rui-Min Yu: State Key Laboratory of Earth Surface Processes and Resource Ecology, and Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, College of Life Sciences, Beijing Normal University, Beijing, 100875, China.
  2. Ning Zhang: State Key Laboratory of Earth Surface Processes and Resource Ecology, and Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, College of Life Sciences, Beijing Normal University, Beijing, 100875, China.
  3. Bo-Wen Zhang: State Key Laboratory of Earth Surface Processes and Resource Ecology, and Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, College of Life Sciences, Beijing Normal University, Beijing, 100875, China.
  4. Yu Liang: State Key Laboratory of Earth Surface Processes and Resource Ecology, and Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, College of Life Sciences, Beijing Normal University, Beijing, 100875, China.
  5. Xiao-Xu Pang: State Key Laboratory of Earth Surface Processes and Resource Ecology, and Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, College of Life Sciences, Beijing Normal University, Beijing, 100875, China.
  6. Lei Cao: State Key Laboratory of Earth Surface Processes and Resource Ecology, and Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, College of Life Sciences, Beijing Normal University, Beijing, 100875, China.
  7. Yi-Dan Chen: State Key Laboratory of Earth Surface Processes and Resource Ecology, and Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, College of Life Sciences, Beijing Normal University, Beijing, 100875, China.
  8. Wei-Ping Zhang: State Key Laboratory of Earth Surface Processes and Resource Ecology, and Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, College of Life Sciences, Beijing Normal University, Beijing, 100875, China.
  9. Yang Yang: State Key Laboratory of Earth Surface Processes and Resource Ecology, and Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, College of Life Sciences, Beijing Normal University, Beijing, 100875, China.
  10. Da-Yong Zhang: State Key Laboratory of Earth Surface Processes and Resource Ecology, and Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, College of Life Sciences, Beijing Normal University, Beijing, 100875, China. zhangdy@bnu.edu.cn.
  11. Er-Li Pang: State Key Laboratory of Earth Surface Processes and Resource Ecology, and Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, College of Life Sciences, Beijing Normal University, Beijing, 100875, China. pangerli@bnu.edu.cn.
  12. Wei-Ning Bai: State Key Laboratory of Earth Surface Processes and Resource Ecology, and Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, College of Life Sciences, Beijing Normal University, Beijing, 100875, China. baiwn@bnu.edu.cn. ORCID
PMID: 37553642 DOI: 10.1186/s12915-023-01668-1

Abstract

BACKGROUND: Autopolyploidy is a valuable model for studying whole-genome duplication (WGD) without hybridization, yet little is known about the genomic structural and functional changes that occur in autopolyploids after WGD. Cyclocarya paliurus (Juglandaceae) is a natural diploid-autotetraploid species. We generated an allele-aware autotetraploid genome, a chimeric chromosome-level diploid genome, and whole-genome resequencing data for 106 autotetraploid individuals at an average depth of 60 × per individual, along with 12 diploid individuals at an average depth of 90 × per individual.
RESULTS: Autotetraploid C. paliurus had 64 chromosomes clustered into 16 homologous groups, and the majority of homologous chromosomes demonstrated similar chromosome length, gene numbers, and expression. The regions of synteny, structural variation and nonalignment to the diploid genome accounted for 81.3%, 8.8% and 9.9% of the autotetraploid genome, respectively. Our analyses identified 20,626 genes (69.18%) with four alleles and 9191 genes (30.82%) with one, two, or three alleles, suggesting post-polyploid allelic loss. Genes with allelic loss were found to occur more often in proximity to or within structural variations and exhibited a marked overlap with transposable elements. Additionally, such genes showed a reduced tendency to interact with other genes. We also found 102 genes with more than four copies in the autotetraploid genome, and their expression levels were significantly higher than their diploid counterparts. These genes were enriched in enzymes involved in stress response and plant defense, potentially contributing to the evolutionary success of autotetraploids. Our population genomic analyses suggested a single origin of autotetraploids and recent divergence (~ 0.57 Mya) from diploids, with minimal interploidy admixture.
CONCLUSIONS: Our results indicate the potential for genomic and functional reorganization, which may contribute to evolutionary success in autotetraploid C. paliurus.

Keywords

Allele loss Allelic chromosome Autopolyploidy Shallow divergence Tetrasomic inheritance Whole-genome duplication

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MeSH Term

Humans
Alleles
Tetraploidy
Gene Duplication
Polyploidy
Genomics
Journal Article Research Support, Non-U.S. Gov't

Word Cloud

Created with Highcharts 10.0.0autotetraploidgenomegenespaliurusdiploidlossduplicationgenomicstructuralAutopolyploidywhole-genomeWGDfunctionaloccurCyclocaryaindividualsaveragedepthindividualCchromosomeshomologouschromosomegenenumbersexpressionanalysesfourallelesallelicfoundevolutionarysuccessautotetraploidsdivergenceBACKGROUND:valuablemodelstudyingwithouthybridizationyetlittleknownchangesautopolyploidsJuglandaceaenaturaldiploid-autotetraploidspeciesgeneratedallele-awarechimericchromosome-levelresequencingdata10660 × peralong1290 × perRESULTS:Autotetraploid64clustered16groupsmajoritydemonstratedsimilarlengthregionssyntenyvariationnonalignmentaccounted813%88%99%respectivelyidentified206266918%91913082%onetwothreesuggestingpost-polyploidGenesoftenproximitywithinvariationsexhibitedmarkedoverlaptransposableelementsAdditionallyshowedreducedtendencyinteractalso102copieslevelssignificantlyhighercounterpartsenrichedenzymesinvolvedstressresponseplantdefensepotentiallycontributingpopulationsuggestedsingleoriginrecent~ 057MyadiploidsminimalinterploidyadmixtureCONCLUSIONS:resultsindicatepotentialreorganizationmaycontributeGenomicinsightsbiasedalleleincreasedAlleleAllelicShallowTetrasomicinheritanceWhole-genome

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