Genome-wide association study of eigenvectors provides genetic insights into selective breeding for tomato metabolites

Abstract Background Long-term domestication and intensive breeding of crop plants aim to establish traits desirable for human needs, and characteristics related to yield, disease resistance, and postharvest storage have traditionally received considerable attention. These processes have led also to...

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Main Authors: Junwei Yang, Bin Liang, Yuemei Zhang, Yun Liu, Shengyuan Wang, Qinqin Yang, Xiaolin Geng, Simiao Liu, Yaoyao Wu, Yingfang Zhu, Tao Lin
Format: Article
Language:English
Published: BMC 2022-05-01
Series:BMC Biology
Subjects:
Online Access:https://doi.org/10.1186/s12915-022-01327-x
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author Junwei Yang
Bin Liang
Yuemei Zhang
Yun Liu
Shengyuan Wang
Qinqin Yang
Xiaolin Geng
Simiao Liu
Yaoyao Wu
Yingfang Zhu
Tao Lin
author_facet Junwei Yang
Bin Liang
Yuemei Zhang
Yun Liu
Shengyuan Wang
Qinqin Yang
Xiaolin Geng
Simiao Liu
Yaoyao Wu
Yingfang Zhu
Tao Lin
author_sort Junwei Yang
collection DOAJ
description Abstract Background Long-term domestication and intensive breeding of crop plants aim to establish traits desirable for human needs, and characteristics related to yield, disease resistance, and postharvest storage have traditionally received considerable attention. These processes have led also to negative consequences, as is the case of loss of variants controlling fruit quality, for instance in tomato. Tomato fruit quality is directly associated to metabolite content profiles; however, a full understanding of the genetics affecting metabolite content during tomato domestication and improvement has not been reached due to limitations of the single detection methods previously employed. Here, we aim to reach a broad understanding of changes in metabolite content using a genome-wide association study (GWAS) with eigenvector decomposition (EigenGWAS) on tomato accessions. Results An EigenGWAS was performed on 331 tomato accessions using the first eigenvector generated from the genomic data as a “phenotype” to understand the changes in fruit metabolite content during breeding. Two independent gene sets were identified that affected fruit metabolites during domestication and improvement in consumer-preferred tomatoes. Furthermore, 57 candidate genes related to polyphenol and polyamine biosynthesis were discovered, and a major candidate gene chlorogenate: glucarate caffeoyltransferase (SlCGT) was identified, which affected the quality and diseases resistance of tomato fruit, revealing the domestication mechanism of polyphenols. Conclusions We identified gene sets that contributed to consumer liking during domestication and improvement of tomato. Our study reports novel evidence of selective sweeps and key metabolites controlled by multiple genes, increasing our understanding of the mechanisms of metabolites variation during those processes. It also supports a polygenic selection model for the application of tomato breeding.
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spelling doaj.art-e09736d9ca4f423e995b4857716fed2a2022-12-22T03:21:32ZengBMCBMC Biology1741-70072022-05-0120111610.1186/s12915-022-01327-xGenome-wide association study of eigenvectors provides genetic insights into selective breeding for tomato metabolitesJunwei Yang0Bin Liang1Yuemei Zhang2Yun Liu3Shengyuan Wang4Qinqin Yang5Xiaolin Geng6Simiao Liu7Yaoyao Wu8Yingfang Zhu9Tao Lin10State Key Laborary of Agrobiotechnology, Beijing Key Laboratory of Growth and Developmental Regulation for Protected Vegetable Crops, College of Horticulture, China Agricultural UniversityState Key Laborary of Agrobiotechnology, Beijing Key Laboratory of Growth and Developmental Regulation for Protected Vegetable Crops, College of Horticulture, China Agricultural UniversityState Key Laborary of Agrobiotechnology, Beijing Key Laboratory of Growth and Developmental Regulation for Protected Vegetable Crops, College of Horticulture, China Agricultural UniversityState Key Laborary of Agrobiotechnology, Beijing Key Laboratory of Growth and Developmental Regulation for Protected Vegetable Crops, College of Horticulture, China Agricultural UniversityCollege of Horticulture, China Agricultural UniversityState Key Laborary of Agrobiotechnology, Beijing Key Laboratory of Growth and Developmental Regulation for Protected Vegetable Crops, College of Horticulture, China Agricultural UniversityState Key Laborary of Agrobiotechnology, Beijing Key Laboratory of Growth and Developmental Regulation for Protected Vegetable Crops, College of Horticulture, China Agricultural UniversityState Key Laboratory of Plant Genomics, and National Center for Plant Gene Research, Institute of Genetics and Developmental Biology, Innovation Academy for Seed Design, Chinese Academy of SciencesGenome Analysis Laboratory of the Ministry of Agriculture, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural SciencesInstitute of Plant Stress Biology, State Key Laboratory of Cotton Biology, Department of Biology, Henan UniversityState Key Laborary of Agrobiotechnology, Beijing Key Laboratory of Growth and Developmental Regulation for Protected Vegetable Crops, College of Horticulture, China Agricultural UniversityAbstract Background Long-term domestication and intensive breeding of crop plants aim to establish traits desirable for human needs, and characteristics related to yield, disease resistance, and postharvest storage have traditionally received considerable attention. These processes have led also to negative consequences, as is the case of loss of variants controlling fruit quality, for instance in tomato. Tomato fruit quality is directly associated to metabolite content profiles; however, a full understanding of the genetics affecting metabolite content during tomato domestication and improvement has not been reached due to limitations of the single detection methods previously employed. Here, we aim to reach a broad understanding of changes in metabolite content using a genome-wide association study (GWAS) with eigenvector decomposition (EigenGWAS) on tomato accessions. Results An EigenGWAS was performed on 331 tomato accessions using the first eigenvector generated from the genomic data as a “phenotype” to understand the changes in fruit metabolite content during breeding. Two independent gene sets were identified that affected fruit metabolites during domestication and improvement in consumer-preferred tomatoes. Furthermore, 57 candidate genes related to polyphenol and polyamine biosynthesis were discovered, and a major candidate gene chlorogenate: glucarate caffeoyltransferase (SlCGT) was identified, which affected the quality and diseases resistance of tomato fruit, revealing the domestication mechanism of polyphenols. Conclusions We identified gene sets that contributed to consumer liking during domestication and improvement of tomato. Our study reports novel evidence of selective sweeps and key metabolites controlled by multiple genes, increasing our understanding of the mechanisms of metabolites variation during those processes. It also supports a polygenic selection model for the application of tomato breeding.https://doi.org/10.1186/s12915-022-01327-xTomatoEigenGWASMetabolitesSelectionSlCGT
spellingShingle Junwei Yang
Bin Liang
Yuemei Zhang
Yun Liu
Shengyuan Wang
Qinqin Yang
Xiaolin Geng
Simiao Liu
Yaoyao Wu
Yingfang Zhu
Tao Lin
Genome-wide association study of eigenvectors provides genetic insights into selective breeding for tomato metabolites
BMC Biology
Tomato
EigenGWAS
Metabolites
Selection
SlCGT
title Genome-wide association study of eigenvectors provides genetic insights into selective breeding for tomato metabolites
title_full Genome-wide association study of eigenvectors provides genetic insights into selective breeding for tomato metabolites
title_fullStr Genome-wide association study of eigenvectors provides genetic insights into selective breeding for tomato metabolites
title_full_unstemmed Genome-wide association study of eigenvectors provides genetic insights into selective breeding for tomato metabolites
title_short Genome-wide association study of eigenvectors provides genetic insights into selective breeding for tomato metabolites
title_sort genome wide association study of eigenvectors provides genetic insights into selective breeding for tomato metabolites
topic Tomato
EigenGWAS
Metabolites
Selection
SlCGT
url https://doi.org/10.1186/s12915-022-01327-x
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