Chromosome-level genome sequence assembly and genome-wide association study of Muscadinia rotundifolia reveal the genetics of 12 berry-related traits

Minkyu Park , Daniel Vera , Devaiah Kambrianda , Pranavkumar Gajjar , Lance Cadle-Davidson , Violeta Tsolova , Islam El-Sharkawy

Horticulture Research ›› 2022, Vol. 9 ›› Issue (1) : uhab011

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Horticulture Research ›› 2022, Vol. 9 ›› Issue (1) :uhab011 DOI: 10.1093/hr/uhab011
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Chromosome-level genome sequence assembly and genome-wide association study of Muscadinia rotundifolia reveal the genetics of 12 berry-related traits
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Abstract

Vitis has two subgenera: Euvitis, which includes commercially important Vitis vinifera and interspecific hybrid cultivars, and Muscadinia. Of note, the market for Muscadinia grapes remains small, and only Muscadinia rotundifolia is cultivated as a commercial crop. To establish a basis for the study of Muscadinia species, we generated chromosome-level whole-genome sequences of Muscadinia rotundifolia cv. Noble. A total of 393.8 Mb of sequences were assembled from 20 haploid chromosomes, and 26 394 coding genes were identified from the sequences. Comparative analysis with the genome sequence of V. vinifera revealed a smaller size of the M. rotundifolia genome but highly conserved gene synteny. A genome-wide association study of 12 Muscadinia berry-related traits was performed among 356 individuals from breeding populations of M. rotundifolia. For the transferability of markers between Euvitis and Muscadinia, we used 2000 core genome rhAmpSeq markers developed to allow marker transferability across Euvitis species. A total of 1599 (80%) rhAmpSeq markers returned data in Muscadinia. From the GWAS analyses, we identified a total of 52 quantitative trait nucleotides (QTNs) associated with the 12 berry-related traits. The transferable markers enabled the direct comparison of the QTNs with previously reported results. The whole-genome sequences along with the GWAS results provide a new basis for the extensive study of Muscadinia species.

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Minkyu Park, Daniel Vera, Devaiah Kambrianda, Pranavkumar Gajjar, Lance Cadle-Davidson, Violeta Tsolova, Islam El-Sharkawy. Chromosome-level genome sequence assembly and genome-wide association study of Muscadinia rotundifolia reveal the genetics of 12 berry-related traits. Horticulture Research, 2022, 9 (1) : uhab011 DOI:10.1093/hr/uhab011

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References

[1]

Olien WC . The muscadine grape: botany, viticulture, history, and current industry. HortScience. 1990; 25: 732-9.

[2]

Brizicky GK . The genera of Vitaceae in the southeastern United States. J Arnold Arbor. 1965; 46: 48-67.

[3]

Conner PJ . A century of muscadine grape (Vitis rotundifolia Michx.) breeding at the University of Georgia . Acta Hortic. 2009; 827: 481-4.

[4]

Yi W, Fischer J, Akoh CC . Study of anticancer activities of muscadine grape phenolics in vitro. J Agric Food Chem. 2005; 53: 8804-12.

[5]

Brown JC, Wang J, Kasman L . et al. Activities of muscadine grape skin and quercetin against helicobacter pylori infection in mice . J Appl Microbiol. 2011; 110: 139-46.

[6]

Merdinoglu D, Wiedeman-Merdinoglu S, Coste P. et al. Genetic analysis of downy mildew resistance derived from Muscadinia rotundifolia . Acta Hortic. 2003; 603: 451-6.

[7]

Staudt G . Evaluation of resistance to grapevine powdery mildew (Uncinula necator [SCHW.] Burr., anamorph Oidium tuckeri BERK.) in accessions of Vitis species . Vitis. 1997; 36: 151-4.

[8]

Olmo HP . Vinifera rotundifolia hybrids as wine grapes . Am J Enol Vitic. 1971; 22: 87.

[9]

Firoozabady E, Olmo HP . Resistance to grape phylloxera in Vitis vinifera x V. rodundifolia grape hybrids . Vitis. 1982; 21: 1-4.

[10]

Olmo HP . The potential role of (vinifera x rotundifolia) hybrids in grape variety improvement . Experientia. 1986; 42: 921-6.

[11]

Pauquet J, Bouquet A, This P. et al. Establishment of a local map of AFLP markers around the powdery mildew resistance gene Run1 in grapevine and assessment of their usefulness for marker assisted selection . Theor Appl Genet. 2001; 103: 1201-10.

[12]

Barker CL, Donald T, Pauquet J . et al. Genetic and physical mapping of the grapevine powdery mildew resistance gene, Run1, using a bacterial artificial chromosome library . Theor Appl Genet. 2005; 111: 370-7.

[13]

Feechan A, Anderson C, Torregrosa L. et al. Genetic dissection of a TIR-NB-LRR locus from the wild north American grapevine species Muscadinia rotundifolia identifies paralogous genes conferring resistance to major fungal and oomycete pathogens in cultivated grapevine . Plant J. 2013; 76: 661-74.

[14]

Feechan A, Kocsis M, Riaz S. et al. Strategies for RUN1 deployment using RUN2 and REN2 to manage grapevine powdery mildew informed by studies of race specificity . Phytopathology. 2015; 105: 1104-13.

[15]

Agurto M, Schlechter RO, Armijo G . et al. RUN1 and REN1 pyramiding in grapevine (Vitis vinifera cv. Crimson seedless) displays an improved defense response leading to enhanced resistance to powdery mildew (Erysiphe necator). Front Plant Sci. 2017; 8: 758.

[16]

Stringer SJ, Marshall DA, Perkins-Veazie P . Nutriceutical compound concentrations of muscadine (Vitis rotundifolia michx.) grape cultivars and breeding lines . Acta Hortic. 2009; 841: 553-6.

[17]

Bralley EE, Hargrove JL, Greenspan P . et al. Muscadine skin nutraceutical extract is highly anti-inflammatory in the TPA model of topical inflammation . FASEB J. 2006; 20: A604-5.

[18]

Gourineni V, Shay N, Chung S. et al. Nutraceutical values of muscadine against obesity and metabolic complications in-vivo. FASEB J. 2012; 26: 818.6-6.

[19]

Hudson TS, Hartle DK, Hursting SD . et al. Inhibition of prostate cancer growth by muscadine grape skin extract and resveratrol through distinct mechanisms . Cancer Res. 2007; 67: 8396.

[20]

Mendonca P, Darwish AG, Tsolova V . et al. The anticancer and antioxidant effects of muscadine grape extracts on racially different triple-negative breast cancer cells . Anticancer Res. 2019; 39: 4043.

[21]

Riaz S, Hu R, Walker MA . A framework genetic map of Muscadinia rotundifolia . Theor Appl Genet. 2012; 125: 1195-210.

[22]

Lewter J, Worthington ML, Clark JR . et al. High-density linkage maps and loci for berry color and flower sex in muscadine grape (Vitis rotundifolia) . Theor Appl Genet. 2019; 132: 1571-85.

[23]

Blanc S, Wiedemann-Merdinoglu S, Dumas V . et al. A reference genetic map of Muscadinia rotundifolia and identification of Ren5, a new major locus for resistance to grapevine powdery mildew. Theor Appl Genet. 2012; 125: 1663-75.

[24]

Vezzulli S, Micheletti D, Riaz S. et al. A SNP transferability survey within the genus Vitis . BMC Plant Biol. 2008; 8: 128.

[25]

Zou C, Karn A, Reisch B. et al. Haplotyping the Vitis collinear core genome with rhAmpSeq improves marker transferability in a diverse genus . Nat Commun. 2020; 11: 413.

[26]

Simão FA, Waterhouse RM, Ioannidis P. et al. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics. 2015; 31: 3210-2.

[27]

Cochetel N, Minio A, Massonnet M. et al. Diploid chromosome-scale assembly of the Muscadinia rotundifolia genome supports chromosome fusion and disease resistance gene expansion during Vitis and Muscadinia divergence . G3 (Bethesda). 2021; 11: jkab033.

[28]

Jaillon O, Aury J-M, Noel B. et al. The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature. 2007; 449: 463-7.

[29]

Guo D-L, Zhao H-L, Li Q . et al. Genome-wide association study of berry-related traits in grape [ Vitis vinifera L.] based on genotyping-by-sequencing markers . Hortic Res. 2019; 6: 11.

[30]

Zhang H, Fan X, Zhang Y. et al. Identification of favorable SNP alleles and candidate genes for seedlessness in Vitis vinifera L. using genome-wide association mapping . Euphytica. 2017; 213: 136.

[31]

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.

[32]

Alexander DH, Novembre J, Lange K . Fast model-based estimation of ancestry in unrelated individuals. Genome Res. 2009; 19: 1655-64.

[33]

Zhang Y-M, Jia Z, Dunwell JM . Editorial: the applications of new multi-locus GWAS methodologies in the genetic dissection of complex traits. Front Plant Sci. 2019; 10: 100.

[34]

Zhang Y-W, Tamba CL, Wen Y-J . et al. mrMLM v4.0.2: an R platform for multi-locus genome-wide association studies . Genom Proteom Bioinform. 2020; 18: 481-7.

[35]

Varanasi A. et al. Glutathione S-transferase: a candidate gene for berry color in muscadine grapes (Vitis rotundifolia) . bioRxiv 2020.07.14.202903. 2020.

[36]

Alfenito MR, Souer E, Goodman CD . et al. Functional complementation of anthocyanin sequestration in the vacuole by widely divergent glutathione S-transferases . Plant Cell. 1998; 10: 1135-49.

[37]

Conn S, Curtin C, Bézier A. et al. Purification, molecular cloning, and characterization of glutathione S-transferases (GSTs) from pigmented Vitis vinifera L. cell suspension cultures as putative anthocyanin transport proteins . J Exp Bot. 2008; 59: 3621-34.

[38]

Walker AR, Lee E, Bogs J . et al. White grapes arose through the mutation of two similar and adjacent regulatory genes . Plant J. 2007; 49: 772-85.

[39]

Sun L, Li S, Jiang J . et al. New quantitative trait locus (QTLs) and candidate genes associated with the grape berry color trait identified based on a high-density genetic map . BMC Plant Biol. 2020; 20: 302.

[40]

Hobson GE . The firmness of tomato fruit in relation to polygalacturonase activity. J Hortic Sci. 1965; 40: 66-72.

[41]

Tijskens LMM, Rodis PS, Hertog MLATM . et al. Kinetics of polygalacturonase activity and firmness of peaches during storage . J Food Eng. 1998; 35: 111-26.

[42]

Paniagua C, Ric-Varas P, García-Gago JA . et al. Elucidating the role of polygalacturonase genes in strawberry fruit softening . J Exp Bot. 2020; 71: 7103-17.

[43]

Costa F, Peace CP, Stella S. et al. QTL dynamics for fruit firmness and softening around an ethylene-dependent polygalacturonase gene in apple (malus× domestica Borkh.) . J Exp Bot. 2010; 61: 3029-39.

[44]

Fanizza G, Lamaj F, Costantini L. et al. QTL analysis for fruit yield components in table grapes (Vitis vinifera) . Theor Appl Genet. 2005; 111: 658-64.

[45]

Ranallo-Benavidez TR, Jaron KS, Schatz MC . GenomeScope 2.0 and Smudgeplot for reference-free profiling of polyploid genomes. Nat Commun. 2020; 11: 1432.

[46]

Kokot M, Długosz M, Deorowicz S . KMC 3: counting and manipulating k-mer statistics. Bioinformatics. 2017; 33: 2759-61.

[47]

Hoff KJ, Lange S, Lomsadze A. et al. BRAKER1: unsupervised RNA-seq-based genome annotation with GeneMark-ET and AUGUSTUS. Bioinformatics. 2016; 32: 767-9.

[48]

Alexander DH, Lange K . Enhancements to the ADMIXTURE algorithm for individual ancestry estimation. BMC Bioinformatics. 2011; 12: 246.

[49]

Porras-Hurtado L, Ruiz Y, Santos C. et al. An overview of STRUCTURE: applications, parameter settings, and supporting software. Front Genet. 2013; 4: 98-8.

[50]

Evanno G, Regnaut S, Goudet J . Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol. 2005; 14: 2611-20.

[51]

Campbell J, Sarkhosh A, Habibi F . et al. Evaluation of biochemical juice attributes and color-related traits in muscadine grape population . Foods. 2021; 10: 1101.

[52]

Campbell J, Sarkhosh A, Habibi F . et al. Biometrics assessment of cluster- and berry-related traits of muscadine grape population . Plan Theory. 2021; 10: 1067.

[53]

Campbell J, Gajjar P, Ismail A . et al. Determination of fertility-related traits in muscadine grape population . Plan Theory. 2021; 10: 1175.

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