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11 16, 2021;22 (1): 316.

Resequencing of 388 cassava accessions identifies valuable loci and selection for variation in heterozygosity.

Wei Hu, Changmian Ji, Zhe Liang, Jianqiu Ye, Wenjun Ou, Zehong Ding, Gang Zhou, Weiwei Tie, Yan Yan, Jinghao Yang, Liming Ma, Xiaoying Yang, Yunxie Wei, Zhiqiang Jin, Jianghui Xie, Ming Peng, Wenquan Wang, Anping Guo, Biyu Xu, Jianchun Guo, Songbi Chen, Mingcheng Wang, Yang Zhou, Xiaolong Li, Ruoxi Li, Xinhui Xiao, Zhongqing Wan, Feifei An, Jie Zhang, Qingyun Leng, Yin Li, Haitao Shi, Ray Ming, Kaimian Li
Author Information
  1. Wei Hu: Sanya Research Institute of Chinese Academy of Tropical Agricultural Sciences, Sanya, Hainan, China. huwei2010916@126.com.
  2. Changmian Ji: Sanya Research Institute of Chinese Academy of Tropical Agricultural Sciences, Sanya, Hainan, China.
  3. Zhe Liang: Biotechnology Research Institute, Chinese Academy of Agricultural Sciences, Beijing, China.
  4. Jianqiu Ye: Tropical Crops Genetic Resources Institute, Chinese Academy of Tropical Agricultural Sciences, Haikou, Hainan, China.
  5. Wenjun Ou: Tropical Crops Genetic Resources Institute, Chinese Academy of Tropical Agricultural Sciences, Haikou, Hainan, China.
  6. Zehong Ding: Sanya Research Institute of Chinese Academy of Tropical Agricultural Sciences, Sanya, Hainan, China.
  7. Gang Zhou: Biomarker Technologies Corporation, Beijing, China.
  8. Weiwei Tie: Sanya Research Institute of Chinese Academy of Tropical Agricultural Sciences, Sanya, Hainan, China.
  9. Yan Yan: Sanya Research Institute of Chinese Academy of Tropical Agricultural Sciences, Sanya, Hainan, China.
  10. Jinghao Yang: Hainan Key Laboratory for Biosafety Monitoring and Molecular Breeding in Off-Season Reproduction Regions, Key Laboratory of Biology and Genetic Resources of Tropical Crops, Institute of Tropical Bioscience and Biotechnology, Chinese Academy of Tropical Agricultural Sciences, Haikou, Hainan, China.
  11. Liming Ma: Biomarker Technologies Corporation, Beijing, China.
  12. Xiaoying Yang: College of Food Science and Technology, Qilu University of Technology (Shandong Academy of Sciences), Jinan, China.
  13. Yunxie Wei: Hainan Key Laboratory for Sustainable Utilization of Tropical Bioresources, College of Tropical Crops, Hainan University, Haikou, Hainan, China.
  14. Zhiqiang Jin: Hainan Key Laboratory for Biosafety Monitoring and Molecular Breeding in Off-Season Reproduction Regions, Key Laboratory of Biology and Genetic Resources of Tropical Crops, Institute of Tropical Bioscience and Biotechnology, Chinese Academy of Tropical Agricultural Sciences, Haikou, Hainan, China.
  15. Jianghui Xie: Hainan Key Laboratory for Biosafety Monitoring and Molecular Breeding in Off-Season Reproduction Regions, Key Laboratory of Biology and Genetic Resources of Tropical Crops, Institute of Tropical Bioscience and Biotechnology, Chinese Academy of Tropical Agricultural Sciences, Haikou, Hainan, China.
  16. Ming Peng: Hainan Key Laboratory for Biosafety Monitoring and Molecular Breeding in Off-Season Reproduction Regions, Key Laboratory of Biology and Genetic Resources of Tropical Crops, Institute of Tropical Bioscience and Biotechnology, Chinese Academy of Tropical Agricultural Sciences, Haikou, Hainan, China.
  17. Wenquan Wang: Hainan Key Laboratory for Biosafety Monitoring and Molecular Breeding in Off-Season Reproduction Regions, Key Laboratory of Biology and Genetic Resources of Tropical Crops, Institute of Tropical Bioscience and Biotechnology, Chinese Academy of Tropical Agricultural Sciences, Haikou, Hainan, China.
  18. Anping Guo: Sanya Research Institute of Chinese Academy of Tropical Agricultural Sciences, Sanya, Hainan, China.
  19. Biyu Xu: Hainan Key Laboratory for Biosafety Monitoring and Molecular Breeding in Off-Season Reproduction Regions, Key Laboratory of Biology and Genetic Resources of Tropical Crops, Institute of Tropical Bioscience and Biotechnology, Chinese Academy of Tropical Agricultural Sciences, Haikou, Hainan, China.
  20. Jianchun Guo: Hainan Key Laboratory for Biosafety Monitoring and Molecular Breeding in Off-Season Reproduction Regions, Key Laboratory of Biology and Genetic Resources of Tropical Crops, Institute of Tropical Bioscience and Biotechnology, Chinese Academy of Tropical Agricultural Sciences, Haikou, Hainan, China.
  21. Songbi Chen: Tropical Crops Genetic Resources Institute, Chinese Academy of Tropical Agricultural Sciences, Haikou, Hainan, China.
  22. Mingcheng Wang: Biomarker Technologies Corporation, Beijing, China.
  23. Yang Zhou: Biomarker Technologies Corporation, Beijing, China.
  24. Xiaolong Li: Biomarker Technologies Corporation, Beijing, China.
  25. Ruoxi Li: Fu Foundation School of Engineering and Applied Science, Columbia University, New York, NY, 10027, USA.
  26. Xinhui Xiao: Tropical Crops Genetic Resources Institute, Chinese Academy of Tropical Agricultural Sciences, Haikou, Hainan, China.
  27. Zhongqing Wan: Tropical Crops Genetic Resources Institute, Chinese Academy of Tropical Agricultural Sciences, Haikou, Hainan, China.
  28. Feifei An: Tropical Crops Genetic Resources Institute, Chinese Academy of Tropical Agricultural Sciences, Haikou, Hainan, China.
  29. Jie Zhang: Tropical Crops Genetic Resources Institute, Chinese Academy of Tropical Agricultural Sciences, Haikou, Hainan, China.
  30. Qingyun Leng: Tropical Crops Genetic Resources Institute, Chinese Academy of Tropical Agricultural Sciences, Haikou, Hainan, China.
  31. Yin Li: Waksman Institute of Microbiology, Rutgers, The State University of New Jersey, Piscataway, NJ, USA.
  32. Haitao Shi: Hainan Key Laboratory for Sustainable Utilization of Tropical Bioresources, College of Tropical Crops, Hainan University, Haikou, Hainan, China. haitaoshi@hainanu.edu.cn.
  33. Ray Ming: FAFU and UIUC-SIB Joint Center for Genomics and Biotechnology, Fujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, Key Laboratory of Genetics, Breeding and Multiple Utilization of Crops, Ministry of Education, Fujian Agriculture and Forestry University, Fuzhou, China. rayming@illinois.edu. ORCID
  34. Kaimian Li: Tropical Crops Genetic Resources Institute, Chinese Academy of Tropical Agricultural Sciences, Haikou, Hainan, China. likaimian@sohu.com.
PMID: 34784936 DOI: 10.1186/s13059-021-02524-7

Abstract

BACKGROUND: Heterozygous genomes are widespread in outcrossing and clonally propagated crops. However, the variation in heterozygosity underlying key agronomic traits and crop domestication remains largely unknown. Cassava is a staple crop in Africa and other tropical regions and has a highly heterozygous genome.
RESULTS: We describe a genomic variation map from 388 resequenced genomes of cassava cultivars and wild accessions. We identify 52 loci for 23 agronomic traits through a genome-wide association study. Eighteen allelic variations in heterozygosity for nine candidate genes are significantly associated with seven key agronomic traits. We detect 81 selective sweeps with decreasing heterozygosity and nucleotide diversity, harboring 548 genes, which are enriched in multiple biological processes including growth, development, hormone metabolisms and responses, and immune-related processes. Artificial selection for decreased heterozygosity has contributed to the domestication of the large starchy storage root of cassava. Selection for homozygous GG allele in MeTIR1 during domestication contributes to increased starch content. Selection of homozygous AA allele in MeAHL17 is associated with increased storage root weight and cassava bacterial blight (CBB) susceptibility. We have verified the positive roles of MeTIR1 in increasing starch content and MeAHL17 in resistance to CBB by transient overexpression and silencing analysis. The allelic combinations in MeTIR1 and MeAHL17 may result in high starch content and resistance to CBB.
CONCLUSIONS: This study provides insights into allelic variation in heterozygosity associated with key agronomic traits and cassava domestication. It also offers valuable resources for the improvement of cassava and other highly heterozygous crops.

Keywords

Agronomic traits Cassava Heterozygosity Resequencing Selection

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MeSH Term

Chromosome Mapping
Crops, Agricultural
DNA-Binding Proteins
Domestication
Genetic Variation
Genome, Plant
Genome-Wide Association Study
Manihot
Nuclear Proteins
Phenotype
Phylogeny
Plant Proteins
Sequence Analysis, DNA

Chemicals

DNA-Binding Proteins
Nuclear Proteins
Plant Proteins
Journal Article Research Support, Non-U.S. Gov't
Article has an altmetric score of 21

Word Cloud

Created with Highcharts 10.0.0heterozygositycassavatraitsvariationagronomicdomesticationkeyallelicassociatedSelectionMeTIR1starchcontentMeAHL17CBBgenomescropscropCassavahighlyheterozygous388accessionslocistudygenesprocessesselectionstorageroothomozygousalleleincreasedresistancevaluableResequencingBACKGROUND:HeterozygouswidespreadoutcrossingclonallypropagatedHoweverunderlyingremainslargelyunknownstapleAfricatropicalregionsgenomeRESULTS:describegenomicmapresequencedcultivarswildidentify5223genome-wideassociationEighteenvariationsninecandidatesignificantlysevendetect81selectivesweepsdecreasingnucleotidediversityharboring548enrichedmultiplebiologicalincludinggrowthdevelopmenthormonemetabolismsresponsesimmune-relatedArtificialdecreasedcontributedlargestarchyGGcontributesAAweightbacterialblightsusceptibilityverifiedpositiverolesincreasingtransientoverexpressionsilencinganalysiscombinationsmayresulthighCONCLUSIONS:providesinsightsalsooffersresourcesimprovementidentifiesAgronomicHeterozygosity

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