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12 14, 2023;24 (1): 289.

Metabolic GWAS-based dissection of genetic basis underlying nutrient quality variation and domestication of cassava storage root.

Zehong Ding, Lili Fu, Bin Wang, Jianqiu Ye, Wenjun Ou, Yan Yan, Meiying Li, Liwang Zeng, Xuekui Dong, Weiwei Tie, Xiaoxue Ye, Jinghao Yang, Zhengnan Xie, Yu Wang, Jianchun Guo, Songbi Chen, Xinhui Xiao, Zhongqing Wan, Feifei An, Jiaming Zhang, Ming Peng, Jie Luo, Kaimian Li, Wei Hu
Author Information
  1. Zehong Ding: National Key Laboratory for Tropical Crop Breeding, Key Laboratory of Biology and Genetic Resources of Tropical Crops, Institute of Tropical Bioscience and Biotechnology, Sanya Research Institute of Chinese Academy of Tropical Agricultural Sciences, Haikou, China.
  2. Lili Fu: National Key Laboratory for Tropical Crop Breeding, Key Laboratory of Biology and Genetic Resources of Tropical Crops, Institute of Tropical Bioscience and Biotechnology, Sanya Research Institute of Chinese Academy of Tropical Agricultural Sciences, Haikou, China.
  3. Bin Wang: Wuhan Metware Biotechnology Co., Ltd, Wuhan, China.
  4. Jianqiu Ye: Tropical Crops Genetic Resources Institute, Chinese Academy of Tropical Agricultural Sciences, Haikou, China.
  5. Wenjun Ou: Tropical Crops Genetic Resources Institute, Chinese Academy of Tropical Agricultural Sciences, Haikou, China.
  6. Yan Yan: National Key Laboratory for Tropical Crop Breeding, Key Laboratory of Biology and Genetic Resources of Tropical Crops, Institute of Tropical Bioscience and Biotechnology, Sanya Research Institute of Chinese Academy of Tropical Agricultural Sciences, Haikou, China.
  7. Meiying Li: National Key Laboratory for Tropical Crop Breeding, Key Laboratory of Biology and Genetic Resources of Tropical Crops, Institute of Tropical Bioscience and Biotechnology, Sanya Research Institute of Chinese Academy of Tropical Agricultural Sciences, Haikou, China.
  8. Liwang Zeng: Hainan Yazhou Bay Seed Laboratory, Sanya, China.
  9. Xuekui Dong: Wuhan Healthcare Metabolic Biotechnology Co., Ltd, Wuhan, China.
  10. Weiwei Tie: National Key Laboratory for Tropical Crop Breeding, Key Laboratory of Biology and Genetic Resources of Tropical Crops, Institute of Tropical Bioscience and Biotechnology, Sanya Research Institute of Chinese Academy of Tropical Agricultural Sciences, Haikou, China.
  11. Xiaoxue Ye: National Key Laboratory for Tropical Crop Breeding, Key Laboratory of Biology and Genetic Resources of Tropical Crops, Institute of Tropical Bioscience and Biotechnology, Sanya Research Institute of Chinese Academy of Tropical Agricultural Sciences, Haikou, China.
  12. Jinghao Yang: National Key Laboratory for Tropical Crop Breeding, Key Laboratory of Biology and Genetic Resources of Tropical Crops, Institute of Tropical Bioscience and Biotechnology, Sanya Research Institute of Chinese Academy of Tropical Agricultural Sciences, Haikou, China.
  13. Zhengnan Xie: National Key Laboratory for Tropical Crop Breeding, Key Laboratory of Biology and Genetic Resources of Tropical Crops, Institute of Tropical Bioscience and Biotechnology, Sanya Research Institute of Chinese Academy of Tropical Agricultural Sciences, Haikou, China.
  14. Yu Wang: National Key Laboratory for Tropical Crop Breeding, Key Laboratory of Biology and Genetic Resources of Tropical Crops, Institute of Tropical Bioscience and Biotechnology, Sanya Research Institute of Chinese Academy of Tropical Agricultural Sciences, Haikou, China.
  15. Jianchun Guo: National Key Laboratory for Tropical Crop Breeding, Key Laboratory of Biology and Genetic Resources of Tropical Crops, Institute of Tropical Bioscience and Biotechnology, Sanya Research Institute of Chinese Academy of Tropical Agricultural Sciences, Haikou, China.
  16. Songbi Chen: Tropical Crops Genetic Resources Institute, Chinese Academy of Tropical Agricultural Sciences, Haikou, China.
  17. Xinhui Xiao: Tropical Crops Genetic Resources Institute, Chinese Academy of Tropical Agricultural Sciences, Haikou, China.
  18. Zhongqing Wan: Tropical Crops Genetic Resources Institute, Chinese Academy of Tropical Agricultural Sciences, Haikou, China.
  19. Feifei An: Tropical Crops Genetic Resources Institute, Chinese Academy of Tropical Agricultural Sciences, Haikou, China.
  20. Jiaming Zhang: National Key Laboratory for Tropical Crop Breeding, Key Laboratory of Biology and Genetic Resources of Tropical Crops, Institute of Tropical Bioscience and Biotechnology, Sanya Research Institute of Chinese Academy of Tropical Agricultural Sciences, Haikou, China.
  21. Ming Peng: National Key Laboratory for Tropical Crop Breeding, Key Laboratory of Biology and Genetic Resources of Tropical Crops, Institute of Tropical Bioscience and Biotechnology, Sanya Research Institute of Chinese Academy of Tropical Agricultural Sciences, Haikou, China.
  22. Jie Luo: Hainan Yazhou Bay Seed Laboratory, Sanya, China. jie.luo@hainanu.edu.cn. ORCID
  23. Kaimian Li: Tropical Crops Genetic Resources Institute, Chinese Academy of Tropical Agricultural Sciences, Haikou, China. likaimian@sohu.com.
  24. Wei Hu: National Key Laboratory for Tropical Crop Breeding, Key Laboratory of Biology and Genetic Resources of Tropical Crops, Institute of Tropical Bioscience and Biotechnology, Sanya Research Institute of Chinese Academy of Tropical Agricultural Sciences, Haikou, China. huwei2010916@126.com.
PMID: 38098107 DOI: 10.1186/s13059-023-03137-y

Abstract

BACKGROUND: Metabolites play critical roles in regulating nutritional qualities of plants, thereby influencing their consumption and human health. However, the genetic basis underlying the metabolite-based nutrient quality and domestication of root and tuber crops remain largely unknown.
RESULTS: We report a comprehensive study combining metabolic and phenotypic genome-wide association studies to dissect the genetic basis of metabolites in the storage root (SR) of cassava. We quantify 2,980 metabolic features in 299 cultivated cassava accessions. We detect 18,218 significant marker-metabolite associations via metabolic genome-wide association mapping and identify 12 candidate genes responsible for the levels of metabolites that are of potential nutritional importance. Me3GT, MeMYB4, and UGT85K4/UGT85K5, which are involved in flavone, anthocyanin, and cyanogenic glucoside metabolism, respectively, are functionally validated through in vitro enzyme assays and in vivo gene silencing analyses. We identify a cluster of cyanogenic glucoside biosynthesis genes, among which CYP79D1, CYP71E7b, and UGT85K5 are highly co-expressed and their allelic combination contributes to low linamarin content. We find MeMYB4 is responsible for variations in cyanidin 3-O-glucoside and delphinidin 3-O-rutinoside contents, thus controlling SR endothelium color. We find human selection affects quercetin 3-O-glucoside content and SR weight per plant. The candidate gene MeFLS1 is subject to selection during cassava domestication, leading to decreased quercetin 3-O-glucoside content and thus increased SR weight per plant.
CONCLUSIONS: These findings reveal the genetic basis of cassava SR metabolome variation, establish a linkage between metabolites and agronomic traits, and offer useful resources for genetically improving the nutrition of cassava and other root crops.

Keywords

Cassava Domestication Genome-wide association study Metabolic profiling Natural variation Nutrient quality

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Grants

  1. 2019YFD1000500/the National Key Research and Development Program of China
  2. 1630052023010/the Central Public-Interest Scientific Institution Basal Research Fund for Chinese Academy of Tropical Agricultural Sciences
  3. 1630052022017/the Central Public-Interest Scientific Institution Basal Research Fund for Chinese Academy of Tropical Agricultural Sciences
  4. 1630052022008/the Central Public-Interest Scientific Institution Basal Research Fund for Chinese Academy of Tropical Agricultural Sciences
  5. 1630052023004/the Central Public-Interest Scientific Institution Basal Research Fund for Chinese Academy of Tropical Agricultural Sciences
  6. 1630052023016/the Central Public-Interest Scientific Institution Basal Research Fund for Chinese Academy of Tropical Agricultural Sciences
  7. 32260486/the National Natural Science Foundation of China
  8. nycytx-11/the earmarked fund for Modern Agro-industry Technology Research System
  9. ZDYF2022XDNY259/the Key Research and Development Program of Hainan Province
  10. SCKJ-JYRC-2022-03/the Project of Sanya Yazhou Bay Science and Technology City
  11. SCKJ-JYRC-2023-68/the Project of Sanya Yazhou Bay Science and Technology City
  12. ZDKJ2021012/the Major Science and Technology Plan of Hainan Province
  13. NKLTCB202303/the Project of National Key Laboratory for Tropical Crop Breeding

MeSH Term

Humans
Genome-Wide Association Study
Manihot
Domestication
Quercetin
Glucosides
Nutrients

Chemicals

Quercetin
Glucosides
Journal Article Research Support, Non-U.S. Gov't
Article has an altmetric score of 1

Word Cloud

Created with Highcharts 10.0.0cassavaSRgeneticbasisrootqualitydomesticationmetabolicassociationmetabolitescontent3-O-glucosidevariationnutritionalhumanunderlyingnutrientcropsstudygenome-widestorageidentifycandidategenesresponsibleMeMYB4cyanogenicglucosidegenefindthusselectionquercetinweightperplantMetabolicBACKGROUND:MetabolitesplaycriticalrolesregulatingqualitiesplantstherebyinfluencingconsumptionhealthHowevermetabolite-basedtuberremainlargelyunknownRESULTS:reportcomprehensivecombiningphenotypicstudiesdissectquantify2980features299cultivatedaccessionsdetect18218significantmarker-metaboliteassociationsviamapping12levelspotentialimportanceMe3GTUGT85K4/UGT85K5involvedflavoneanthocyaninmetabolismrespectivelyfunctionallyvalidatedvitroenzymeassaysvivosilencinganalysesclusterbiosynthesisamongCYP79D1CYP71E7bUGT85K5highlyco-expressedalleliccombinationcontributeslowlinamarinvariationscyanidindelphinidin3-O-rutinosidecontentscontrollingendotheliumcoloraffectsMeFLS1subjectleadingdecreasedincreasedCONCLUSIONS:findingsrevealmetabolomeestablishlinkageagronomictraitsofferusefulresourcesgeneticallyimprovingnutritionGWAS-baseddissectionCassavaDomesticationGenome-wideprofilingNaturalNutrient

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