GWAS Characterization of the Genetic Regions Associated with Nine Important Agronomic Traits in Tomato (Solanum lycopersicum L.)

Understanding the genetic background of elite cultivated tomato germplasm resources in crossbreeding and revealing the genetic basis of complex traits are vital for better-targeted germplasm expansion and the creation of strong hybrids. Here, we obtained approximately 21 million single-nucleotide polymorphisms (SNPs) based on the sequencing of 212 cultivated tomato accessions and the population structure of which was revealed. More importantly, we found that target genes distributed on chromosomes 1, 5, 9, and 11 may be actively selected in breeding. In particular, the significant signals related to soluble sugar content (chr1_94170222, chr1_96273188, chr9_4167512, and chr11_55592768), fruit firmness (chr5_4384919 and chr5_5111452) and gray leaf spot resistance (chr11_8935252 and chr11_9707993) were also detected on the corresponding chromosomes, respectively. Overall, we reported 28 significant association signals for nine agronomic traits based on a mixed linear model (MLM), including 114 genes. Among these signals, 21 contained potential novel genes for six fruit traits. These novel candidate genes located in genomic regions without previously known loci or on different chromosomes explained approximately 16% of the phenotypic variance on average in cultivated tomatoes. These findings could accelerate the identification and validation of novel and known candidate genes and QTLs, improving the understanding of the genetic structure of complex quantitative traits. These results also provide a basis for tomato breeding and improvement.

[1]  T. Zhao,et al.  The Sm gene conferring resistance to gray leaf spot disease encodes an NBS-LRR (nucleotide-binding site-leucine-rich repeat) plant resistance protein in tomato , 2022, Theoretical and Applied Genetics.

[2]  Minkyun Kim,et al.  Genome-wide association study identifies QTL for eight fruit traits in cultivated tomato (Solanum lycopersicum L.) , 2021, Horticulture research.

[3]  Z. Fei,et al.  Genome-wide association study reveals the genetic architecture of 27 agronomic traits in tomato. , 2021, Plant physiology.

[4]  Ting Zhao,et al.  Heterosis and Combining Ability Analysis of Fruit Yield, Early Maturity, and Quality in Tomato , 2021 .

[5]  Mingyan Jiang,et al.  Genetic analysis of main flower characteristics in the F1 generation derived from intraspecific hybridization between Plumbago auriculata and Plumbago auriculata f. alba , 2020 .

[6]  F. Carrari,et al.  Validated MAGIC and GWAS populations mapping reveal the link between vitamin E contents and natural variation in chorismate metabolism in tomato. , 2020, The Plant journal : for cell and molecular biology.

[7]  L. Mueller,et al.  Exploiting the diversity of tomato: the development of a phenotypically and genetically detailed germplasm collection , 2020, Horticulture Research.

[8]  J. Arcot,et al.  Co-ingestion of red cabbage with cherry tomato enhances digestive bioaccessibility of anthocyanins but decreases carotenoid bioaccessibility after simulated in vitro gastro-intestinal digestion. , 2019, Food chemistry.

[9]  M. Tester,et al.  Breeding crops to feed 10 billion , 2019, Nature Biotechnology.

[10]  Z. Fei,et al.  Genomic analyses of an extensive collection of wild and cultivated accessions provide new insights into peach breeding history , 2019, Genome Biology.

[11]  Yong-chen Du,et al.  Fine mapping and molecular marker development of the Sm gene conferring resistance to gray leaf spot (Stemphylium spp.) in tomato , 2018, Theoretical and Applied Genetics.

[12]  Xinyuan Hao,et al.  Comprehensive transcriptome analysis reveals common and specific genes and pathways involved in cold acclimation and cold stress in tea plant leaves , 2018, Scientia Horticulturae.

[13]  F. Hochholdinger,et al.  Heterosis in plants , 2018, Current Biology.

[14]  Chuanyou Li,et al.  Current status and prospects on tomato molecular breeding-from gene cloning to cultivar improvement , 2017 .

[15]  Jianbing Yan,et al.  Genome-wide Association Studies in Maize: Praise and Stargaze. , 2017, Molecular plant.

[16]  Xiaojie Xu,et al.  Development of a multiple-hybrid population for genome-wide association studies: theoretical consideration and genetic mapping of flowering traits in maize , 2017, Scientific Reports.

[17]  M. Causse,et al.  Association mapping reveals the genetic architecture of tomato response to water deficit: focus on major fruit quality traits , 2016, Journal of experimental botany.

[18]  Tao Huang,et al.  Genomic architecture of heterosis for yield traits in rice , 2016, Nature.

[19]  Dongyuan Liu,et al.  Subgenome parallel selection is associated with morphotype diversification and convergent crop domestication in Brassica rapa and Brassica oleracea , 2016, Nature Genetics.

[20]  Rachel S. Meyer,et al.  Domestication history and geographical adaptation inferred from a SNP map of African rice , 2016, Nature Genetics.

[21]  Richard B. Gillis,et al.  Genetic improvement of tomato by targeted control of fruit softening , 2016, Nature Biotechnology.

[22]  M. Yamasaki,et al.  Genome-wide association study using whole-genome sequencing rapidly identifies new genes influencing agronomic traits in rice , 2016, Nature Genetics.

[23]  Peter J. Bradbury,et al.  Identification of genetic variants associated with maize flowering time using an extremely large multi-genetic background population. , 2016, The Plant journal : for cell and molecular biology.

[24]  K. Pillen,et al.  Genomic dissection of plant development and its impact on thousand grain weight in barley through nested association mapping , 2016, Journal of experimental botany.

[25]  P. Klein,et al.  Association mapping of germinability and seedling vigor in sorghum under controlled low-temperature conditions. , 2016, Genome.

[26]  Jiantao Zhao,et al.  Genome-Wide Association Mapping for Tomato Volatiles Positively Contributing to Tomato Flavor , 2015, Front. Plant Sci..

[27]  J. Cañizares,et al.  Genomic variation in tomato, from wild ancestors to contemporary breeding accessions , 2015, BMC Genomics.

[28]  Hui Xiang,et al.  Resequencing 302 wild and cultivated accessions identifies genes related to domestication and improvement in soybean , 2015, Nature Biotechnology.

[29]  A. Sacco,et al.  An association mapping approach to identify favourable alleles for tomato fruit quality breeding , 2014, BMC Plant Biology.

[30]  Kui Lin,et al.  Genomic analyses provide insights into the history of tomato breeding , 2014, Nature Genetics.

[31]  A. Fernie,et al.  Genome-Wide Association in Tomato Reveals 44 Candidate Loci for Fruit Metabolic Traits1[W] , 2014, Plant Physiology.

[32]  Xuehui Huang,et al.  Natural variations and genome-wide association studies in crop plants. , 2014, Annual review of plant biology.

[33]  V. Ramanathan,et al.  Determination of heterotic groups for tropical Indica hybrid rice germplasm , 2014, Theoretical and Applied Genetics.

[34]  Ying Li,et al.  A genomic variation map provides insights into the genetic basis of cucumber domestication and diversity , 2013, Nature Genetics.

[35]  Xuehui Huang,et al.  Sequencing-based genome-wide association study in rice. , 2013, Current opinion in plant biology.

[36]  N. Ranc,et al.  Phenotypic diversity and association mapping for fruit quality traits in cultivated tomato and related species , 2013, Theoretical and Applied Genetics.

[37]  Jean-Paul Bouchet,et al.  Genome-Wide Association Mapping in Tomato (Solanum lycopersicum) Is Possible Using Genome Admixture of Solanum lycopersicum var. cerasiforme , 2012, G3: Genes | Genomes | Genetics.

[38]  J. Giovannoni,et al.  Uniform ripening Encodes a Golden 2-like Transcription Factor Regulating Tomato Fruit Chloroplast Development , 2012, Science.

[39]  Xun Xu,et al.  Comparative population genomics of maize domestication and improvement , 2012, Nature Genetics.

[40]  P. Visscher,et al.  Five years of GWAS discovery. , 2012, American journal of human genetics.

[41]  N. Ranc,et al.  Increase in Tomato Locule Number Is Controlled by Two Single-Nucleotide Polymorphisms Located Near WUSCHEL1[C][W] , 2011, Plant Physiology.

[42]  Edward S. Buckler,et al.  Genetic structure and domestication history of the grape , 2011, Proceedings of the National Academy of Sciences.

[43]  Meng Li,et al.  Genome-wide association studies of 14 agronomic traits in rice landraces , 2010, Nature Genetics.

[44]  Richard Durbin,et al.  Fast and accurate long-read alignment with Burrows–Wheeler transform , 2010, Bioinform..

[45]  Gonçalo R. Abecasis,et al.  The Sequence Alignment/Map format and SAMtools , 2009, Bioinform..

[46]  Richard Durbin,et al.  Sequence analysis Fast and accurate short read alignment with Burrows – Wheeler transform , 2009 .

[47]  N. Ranc,et al.  Bmc Plant Biology , 2022 .

[48]  B. Maher.  Personal genomes: The case of the missing heritability , 2008, Nature.

[49]  S. Tanksley,et al.  Regulatory change in YABBY-like transcription factor led to evolution of extreme fruit size during tomato domestication , 2008, Nature Genetics.

[50]  D. Reich,et al.  Population Structure and Eigenanalysis , 2006, PLoS genetics.

[51]  M. Petreikov,et al.  Temporally extended gene expression of the ADP-Glc pyrophosphorylase large subunit (AgpL1) leads to increased enzyme activity in developing tomato fruit , 2006, Planta.

[52]  Marta García-Gusano,et al.  Evaluation of amplified fragment length polymorphism and simple sequence repeats for tomato germplasm fingerprinting: utility for grouping closely related traditional cultivars. , 2006, Genome.

[53]  Mark Daly,et al.  Haploview: analysis and visualization of LD and haplotype maps , 2005, Bioinform..

[54]  M. Stephens,et al.  Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. , 2003, Genetics.

[55]  Edward S. Buckler,et al.  Dwarf8 polymorphisms associate with variation in flowering time , 2001, Nature Genetics.

[56]  P. Donnelly,et al.  Inference of population structure using multilocus genotype data. , 2000, Genetics.

[57]  A. Bennett,et al.  Modification of Expansin Protein Abundance in Tomato Fruit Alters Softening and Cell Wall Polymer Metabolism during Ripening , 1999, Plant Cell.

[58]  M. Ganal,et al.  The SELF-PRUNING gene of tomato regulates vegetative to reproductive switching of sympodial meristems and is the ortholog of CEN and TFL1. , 1998, Development.

[59]  C. R. Bird,et al.  The tomato polygalacturonase gene and ripening-specific expression in transgenic plants , 1988, Plant Molecular Biology.

[60]  N. Saitou,et al.  The neighbor-joining method: a new method for reconstructing phylogenetic trees. , 1987, Molecular biology and evolution.

[61]  R H Moll,et al.  The Relationship of Heterosis and Genetic Divergence in Maize. , 1965, Genetics.

[62]  J. L. Chávez-Servia,et al.  Fruit size QTLs affect in a major proportion the yield in tomato , 2015 .

[63]  S. Kaeppler,et al.  Formation of Heterotic Groups and Understanding Genetic Effects in a Provitamin A Biofortified Maize Breeding Program , 2014 .

[64]  He Lian-shun.  Study on Division of Processing Tomato Heterosis Group and Utilization of Heterosis Models , 2012 .

[65]  S. Tingey,et al.  Whole genome scan detects an allelic variant of fad2 associated with increased oleic acid levels in maize , 2007, Molecular Genetics and Genomics.