Multiple haplotype-based analyses provide genetic and evolutionary insights into tomato fruit weight and composition

Jiantao Zhao , Christopher Sauvage , Frédérique Bitton , Mathilde Causse

Horticulture Research ›› 2022, Vol. 9 ›› Issue (1) : uhab009

PDF (1916KB)
Horticulture Research ›› 2022, Vol. 9 ›› Issue (1) :uhab009 DOI: 10.1093/hr/uhab009
Article
research-article
Multiple haplotype-based analyses provide genetic and evolutionary insights into tomato fruit weight and composition
Author information +
History +
PDF (1916KB)

Abstract

Improving fruit quality traits such as metabolic composition remains a challenge for tomato breeders. To better understand the genetic architecture of these traits and decipher the demographic history of the loci controlling tomato quality traits, we applied an innovative approach using multiple haplotype-based analyses, aiming to test the potentials of haplotype based study in association and genomic prediction studies. We performed and compared haplotype vs SNP-based associations (hapQTL) with multi-locus mixed model (MLMM), focusing on tomato fruit weight and metabolite contents (i.e. sugars, organic acids and amino acids). Using a panel of 163 tomato accessions genotyped with 5995 SNPs, we detected a total of 784 haplotype blocks, with an average size of haplotype blocks ∼58 kb. A total of 108 significant associations for 26 traits were detected thanks to Haplotype/SNP-based Bayes models. Haplotype-based Bayes model (97 associations) outperformed SNP-based Bayes model (50 associations) and MLMM (53 associations) in identifying marker-trait associations as well as in genomic prediction (especially for those traits with moderate to low heritability). To decipher the demographic history, we identified 24 positive selective sweeps using the integrated haplotype score (iHS). Most of the significant associations for tomato quality traits were located within selective sweeps (54.63% and 71.7% in hapQTL and MLMM models, respectively). Promising candidate genes were identified controlling tomato fruit weight and metabolite contents. We thus demonstrated the benefits of using haplotypes for evolutionary and genetic studies, providing novel insights into tomato quality improvement and breeding history.

Cite this article

Download citation ▾
Jiantao Zhao, Christopher Sauvage, Frédérique Bitton, Mathilde Causse. Multiple haplotype-based analyses provide genetic and evolutionary insights into tomato fruit weight and composition. Horticulture Research, 2022, 9 (1) : uhab009 DOI:10.1093/hr/uhab009

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Eichler EE, Flint J, Gibson G. et al. Missing heritability and strategies for finding the underlying causes of complex disease. Nat Rev Genet. 2010; 11: 446-50.

[2]

Belmont JW, Hardenbol P, Willis TD. et al. The international HapMap project. Nature. 2003; 426: 789-96.

[3]

Johnson GCL, Esposito L, Barratt B. et al. Haplotype tagging for the identification of common disease genes. Nat Genet. 2001; 29: 233-7.

[4]

Bader JS . The relative power of SNPs and haplotype as genetic markers for association tests. Pharmacogenomics. 2001; 2: 11-24.

[5]

Xu H, Guan Y . Detecting local haplotype sharing and haplotype association. Genetics. 2014; 197: 823-38.

[6]

Farashi S, Kryza T, Clements J. et al. Post-GWAS in prostate cancer: from genetic association to biological contribution. Nat Rev Cancer. 2019; 19: 46-59.

[7]

Sabeti PC, Reich DE, Higgins JM. et al. Detecting recent positive selection in the human genome from haplotype structure. Nature. 2002; 419: 832-7.

[8]

Khatkar MS, Zenger KR, Hobbs M. et al. A primary assembly of a bovine haplotype block map based on a 15,036-single-nucleotide polymorphism panel genotyped in Holstein-Friesian cattle. Genetics. 2007; 176: 763-72.

[9]

Maldonado C, Mora F, Scapim CA. et al. Genome-wide haplotype-based association analysis of key traits of plant lodging and architecture of maize identifies major determinants for leaf angle: HAPla4 . PLoS One. 2019; 14: e0212925. https://doi.org/10.1371/journal.pone.0212925.

[10]

Daware AV, Srivastava R, Singh AK. et al. Regional association analysis of MetaQTLs delineates candidate grain size genes in Rice. Front Plant Sci. 2017; 8: 807.

[11]

Vitti JJ, Grossman SR, Sabeti PC . Detecting natural selection in genomic data. Annu Rev Genet. 2013; 47: 97-120.

[12]

Gautier M, Klassmann A. Vitalis, R . rehh 2.0: a reimplementation of the R package rehh to detect positive selection from haplotype structure. Mol Ecol Resour. 2017; 17: 78-90.

[13]

Voight BF, Kudaravalli S, Wen X. et al. A map of recent positive selection in the human genome. PLoS Biol. 2006; 4: 0446-58.

[14]

Crossa J, Pérez-Rodríguez P, Cuevas J. et al. Genomic selection in plant breeding: methods, models, and perspectives. Trends Plant Sci. 2017; 22: 961-75.

[15]

Heffner EL, Sorrells ME, Jannink JL . Genomic selection for crop improvement. Crop Sci. 2009; 49: 1-12.

[16]

Hickey LT, Hafeez A, Robinson H. et al. Breeding crops to feed 10 billion. Nat Biotechnol. 2019; 37: 744-54.

[17]

Hickey JM, Chiurugwi T, Mackay I. et al. Genomic prediction unifies animal and plant breeding programs to form platforms for biological discovery. Nat Genet. 2017; 49: 1297-303.

[18]

Calus MPL, Meuwissen THE, Roos APW. et al. Accuracy of genomic selection using different methods to define haplotypes. Genetics. 2008; 178: 553-61.

[19]

Cuyabano BC, Su G, Lund MS . Selection of haplotype variables from a high-density marker map for genomic prediction. Genet Sel Evol. 2015; 47: 61-7.

[20]

Minamikawa MF, Kunihisa M, Noshita K. et al. Tracing founder haplotypes of Japanese apple varieties: application in genomic prediction and genome-wide association study. Hortic Res. 2021; 8: 49.

[21]

Daware A, Parida SK, Tyagi AK . Integrated genomic strategies for cereal genetic enhancement: combining QTL and association mapping. Methods Mol Biol. 2020; 2072: 15-25.

[22]

Yamamoto E, Matsunaga H, Onogi A. et al. A simulation-based breeding design that uses whole-genome prediction in tomato. Sci Rep. 2016; 6: 19454.

[23]

Duangjit J, Causse M, Sauvage C . Efficiency of genomic selection for tomato fruit quality. Mol Breed. 2016; 36: 29.

[24]

Yamamoto E, Matsunaga H, Onogi A. et al. Efficiency of genomic selection for breeding population design and phenotype prediction in tomato. Heredity (Edinb). 2017; 118: 202-9.

[25]

Bauchet G, Causse M . Genetic diversity in tomato (Solanum lycopersicum) and its wild relatives. In: Genetic Diversity in Plants, 2012. IntechOpen, Available from: https://www.intechopen.com/chapters/31476.

[26]

Blanca J, Montero-Pau J, Sauvage C. et al. Genomic variation in tomato, from wild ancestors to contemporary breeding accessions. BMC Genomics. 2015; 16: 257.

[27]

Lin T, Zhu G, Zhang J. et al. Genomic analyses provide insights into the history of tomato breeding. Nat Genet. 2014; 46: 1220-6.

[28]

Klee HJ, Tieman DM . The genetics of fruit flavour preferences. Nat Rev Genet. 2018; 19: 347-56.

[29]

Klee HJ, Tieman DM . Genetic challenges of flavor improvement in tomato. Trends Genet. 2013; 29: 257-62.

[30]

Tieman D, Zhu G, Resende MFR. et al. A chemical genetic roadmap to improved tomato flavor. Science. 2017; 355: 391-4.

[31]

Zhao J, Sauvage C, Zhao J. et al. Meta-analysis of genome-wide association studies provides insights into genetic control of tomato flavor. Nat Commun. 2019; 10: 1534.

[32]

Zhu G, Wang S, Huang Z. et al. Rewiring of the fruit metabolome in tomato breeding. Cell. 2018; 172: 249.e12-61.e12.

[33]

Sauvage C, Segura V, Bauchet G. et al. Genome-wide association in tomato reveals 44 candidate loci for fruit metabolic traits. Plant Physiol. 2014; 165: 1120-32.

[34]

Segura V, Vilhjálmsson BJ, Platt A. et al. An efficient multi-locus mixed-model approach for genome-wide association studies in structured populations. Nat Genet. 2012; 44: 825-30.

[35]

Hendelman A, Zebell S, Rodriguez-leal D. et al. Conserved pleiotropy of an ancient plant homeobox gene uncovered by cis-regulatory dissection. Cell. 2021; 184: 1724-1739.e16.

[36]

Kong D, Hao Y, Cui H . The WUSCHEL related Homeobox protein WOX7 regulates the sugar response of lateral root development in Arabidopsis thaliana . Mol Plant. 2016; 9: 261-70.

[37]

Tam V, Patel N, Turcotte M. et al. Benefits and limitations of genome-wide association studies. Nat Rev Genet. 2019; 20: 467-84.

[38]

Sierra-Orozco E, Shekasteband R, Illa-Berenguer E. et al. Identification and characterization of GLOBE, a major gene controlling fruit shape and impacting fruit size and marketability in tomato. Hortic Res. 2021; 8: 138. https://doi.org/10.1038/s41438-021-00574-3.

[39]

Gutierrez C, Superior C, Cientificas DI . The Arabidopsis cell division cycle. Arab B. 2009; 7: 1-19.

[40]

Bauchet G, Grenier S, Samson N. et al. Identification of major loci and genomic regions controlling acid and volatile content in tomato fruit: implications for flavor improvement. New Phytol. 2017; 215: 624-41.

[41]

Ye J, Wang X, Hu T. et al. An inDel in the promoter of Al-ACTIVATED MALATE TRANSPORTER9 selected during tomato domestication determines fruit malate contents and aluminum tolerance. Plant Cell. 2017; 29: 2249-68.

[42]

Fridman E, Pleban T, Zamir D . A recombination hotspot delimits a wild-species quantitative trait locus for tomato sugar content to 484 bp within an invertase gene. Proc Natl Acad Sci U S A. 2000; 97: 4718-23.

[43]

Chakrabarti M, Zhang N, Sauvage C. et al. A cytochrome P450 regulates a domestication trait in cultivated tomato. Proc Natl Acad Sci U S A. 2013; 110: 17125-30.

[44]

Zhang C, Li X, He Y. et al. Physiological investigation of C4-phosphoenolpyruvate-carboxylase-introduced rice line shows that sucrose metabolism is involved in the improved drought tolerance. Plant Physiol Biochem. 2017; 115: 328-42.

[45]

Durán-Soria S, Pott DM, Osorio S. et al. Sugar signaling during fruit ripening. Front Plant Sci. 2020; 11: 564917, https://doi.org/10.3389/fpls.2020.564917.

[46]

Somssich M, Je BI, Simon R. et al. CLAVATA-WUSCHEL signaling in the shoot meristem. Development. 2016; 143: 3238-48.

[47]

Rodríguez-Leal D, Lemmon ZH, Man J. et al. Engineering quantitative trait variation for crop improvement by genome editing. Cell. 2017; 171: 470, e8- 480.e8.

[48]

Gupta PK, Kulwal PL, Jaiswal V . Association mapping in plants in the post-GWAS genomics era. Adv Genet. 2019; 104: 75-154.

[49]

Hamilton JP, Sim SC, Stoffel K. et al. Single nucleotide polymorphism discovery in cultivated tomato via sequencing by synthesis. The Plant Genome. 2012; 5: 17-29.

[50]

Sim SC, Durstewitz G, Plieske J. et al. Development of a large snp genotyping array and generation of high-density genetic maps in tomato. PLoS One. 2012; 7: e40563. https://doi.org/10.1371/journal.pone.0040563.

[51]

Purcell S, Neale B, Todd-Brown K. et al. PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet. 2007; 81: 559-75.

[52]

Barrett JC, Fry B, Maller J. et al. Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics. 2005; 21: 263-5.

[53]

Delaneau O, Marchini J, Consortium T 1000 GP. et al. Integrating sequence and array data to create an improved 1000 genomes project haplotype reference panel. Nat Commun. 2014; 5: 3934.

[54]

Danecek P, Auton A, Abecasis G. et al. The variant call format and VCFtools. Bioinformatics. 2011; 27: 2156-8.

[55]

Kang HM, Sul JH, Service, S.K. et al. Variance component model to account for sample structure in genome-wide association studies. Nat Genet. 2010; 42: 348-54.

[56]

Li MX, Yeung JMY, Cherny SS. et al. Evaluating the effective numbers of independent tests and significant p-value thresholds in commercial genotyping arrays and public imputation reference datasets. Hum Genet. 2012; 131: 747-56.

[57]

Pritchard JK, Stephens M, Donnelly P . Inference of population structure using multilocus genotype data. Genetics. 2000; 155: 945-59.

[58]

Hardy OJ, Vekemans X . SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes. 2002; 2: 618-20.

[59]

Fernandez-Pozo N, Zheng Y, Snyder SI. et al. The tomato expression atlas. Bioinformatics. 2017; 33: 2397-8.

[60]

Waese J, Fan J, Pasha A. et al. ePlant: visualizing and exploring multiple levels of data for hypothesis generation in plant biology. Plant Cell. 2017; 29: 1806-21.

[61]

Pérez P, de los Campos G, Goddard ME . Genome-wide regression and prediction with the BGLR statistical package. Genetics. 2014; 198: 483-95.

[62]

Covarrubias-Pazaran G. Genome-assisted prediction of quantitative traits using the R package sommer. PLoS One. 2016; 11: e0156744.

PDF (1916KB)

64

Accesses

0

Citation

Detail

Sections
Recommended

/