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| Mining of candidate genes for grape berry cracking using a genome-wide association study |
ZHANG Chuan1, 2*, WU Jiu-yun2*, CUI Li-wen3, FANG Jing-gui1
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1 College of Horticulture, Nanjing Agricultural University, Nanjing 210095, P.R.China
2 Turpan Research Institute of Agricultural Sciences, Xinjiang Academy of Agricultural Sciences, Turpan 838000, P.R.China
3 College of Agro-grassland Sciences, Nanjing Agricultural University, Nanjing 210095, P.R.China
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摘要
为了更好地了解葡萄浆果开裂的遗传基础，我们对不同葡萄品种进行了全基因组关联研究（GWAS）。基于混合线性模型（MLM），我们在两年内分别检测到五个和两个与浆果开裂指数和浆果开裂类型相关的单核苷酸多态性（SNP）位点；这些位点主要分布在四条染色体上，即1、2、3和18号染色体。这些相关的SNP位点与10个独特的候选浆果开裂基因相关。基因表达模式表明，易裂果品种的候选基因表达比抗裂果品种丰富。葡萄浆果是一个由多个基因控制的复杂性状，主要涉及包括多聚半乳糖醛酸酶、铜转运蛋白和受体样蛋白相关基因，这些候选浆果开裂基因的高表达可能促进浆果开裂的发生。本研究有助于阐明浆果开裂的遗传机制。
Abstract
Fruit cracking is a common phenomenon during the growth and development of horticultural crops that seriously affects fruit yield and quality. However, there are few studies on the mining of candidate genes related to berry cracking. To better understand the genetic basis of grape berry cracking, we conducted a genome-wide association study (GWAS) of grape varieties. Based on the mixed linear model (MLM), we detected five single nucleotide polymorphism (SNP) loci associated with berry-cracking index and two SNP loci associated with berry-cracking type in two years. These loci were mainly distributed on four chromosomes, namely 1, 2, 3, and 18, and were associated with ten unique candidate berry-cracking genes. The gene expression patterns indicated that the candidate genes in the susceptible berry-cracking variety were more abundant than in the resistant berry-cracking variety. Grape berry-cracking is a complex trait controlled by multiple genes, mainly including genes involved in polygalacturonase, copper transporter, and receptor-like proteins. The high expression of the candidate berry-cracking genes may promote the occurrence of berry cracking, so the present study helps to further elucidate the genetic mechanism of berry cracking.
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Received: 12 May 2021
Accepted: 01 April 2022
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| Fund: The authors are grateful for the National Key Research and Development Program of China (2019YFD1000101), the China Agriculture Research System of MOF and MARA (CARS-29-yc-1); and Crop Resources Protection Program of Ministry of Agriculture and Rural Affairs of China (2130135–34). |
| About author: ZHANG Chuan, E-mail: 2016204005@njau.edu.cn; WU Jiu-yun, E-mail: kobewjy@163.com; Correspondence FANG Jing-gui, Tel/Fax: +86-25-84395217, E-mail: fanggg@njau.edu.cn
* These authors contributed equally to this study. |
Cite this article:
ZHANG Chuan, WU Jiu-yun, CUI Li-wen, FANG Jing-gui.
2022.
Mining of candidate genes for grape berry cracking using a genome-wide association study. Journal of Integrative Agriculture, 21(8): 2291-2304.
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Abbott J D, Peet M M, Willits D H, Sanders D C, Gough R E. 1986. Effects of irrigation frequency and scheduling on fruit production and radial fruit cracking in greenhouse tomatoes in soil beds and in a soil-less medium in bags. Scientia Horticulturae, 28, 209–217.
Alexander D H, Novembre J, Lange K. 2009. Fast model-based estimation of ancestry in unrelated individuals. Genome Research, 19, 1655–1664.
Alkio M, Jonas U, Sprink T, van Nocker S, Knoche M. 2012. Identification of putative candidate genes involved in cuticle formation in Prunus avium (sweet cherry) fruit. Annals of Botany, 110, 101–112.
Avdeev Y I. 1980. Inheritance of resistance to concentric fruit cracking in tomato. Cytology and Genetics, 14, 33–37.
Balbontín C, Ayala H, Bastias R M, Tapia G, Ellena M, Torres C, Yuri J A, Quero-García J, Ríos J C, Silva H. 2013. Cracking in sweet cherries: A comprehensive review from a physiological, molecular, and genomic perspective. Chilean Journal of Agricultural Research, 73, 66–72.
Balbontín C, Ayala H, Rubilar J, Cote J, Figueroa C R. 2014. Transcriptional analysis of cell wall and cuticle related genes during fruit development of two sweet cherry cultivars with contrasting levels of cracking tolerance. Chilean Journal of Agricultural Research, 74, 162–169.
Ban Y, Mitani N, Sato A, Kono A, Hayashi T. 2016. Genetic dissection of quantitative trait loci for berry traits in interspecific hybrid grape (Vitis labruscana×Vitis vinifera). Euphytica, 211, 295–310.
Bargel H, Neinhuis C. 2005. Tomato (Lycopersicon esculentum Mill.) fruit growth and ripening as related to the biomechanical properties of fruit skin and isolated cuticle. Journal of Experimental Botany, 56, 1049–1060.
Bradbury P J, Zhang Z, Kroon D E, Casstevens T M, Ramdoss Y, Buckler E S. 2007. TASSEL software for association mapping of complex traits in diverse samples. Bioinformatics, 23, 2633–2635.
Brummel D A, Harpster M H. 2001. Cell wall metabolism in fruit softening and quality and its manipulation in transgenic plants. Plant Molecular Biology, 47, 311–340.
Brüggenwirth M, Knoche M. 2016. Mechanical properties of skins of sweet cherry fruit of differing susceptibilities to cracking. Journal of the American Society for Horticultural Science, 141, 162–168.
Brüggenwirth M, Knoche M. 2017. Cell wall swelling, fracture mode, and the mechanical properties of cherry fruit skins are closely related. Planta, 245, 765–777.
Christensen J V. 2000. Performance in Denmark of 16 European varieties of sweet cherry. Journal of American Pomological Society, 54, 172–176.
Considine J. 1982. Physical aspects of fruit growth: cuticular fracture and fracture patterns in relation to fruit structure in Vitis vinifera. Journal of Horticultural Science, 57, 79–91.
Considine J A, Kriedemann P E. 2000. Fruit splitting in grapes: Determination of the critical turgor pressure. Australian Journal of Agricultural Research, 23, 17–23.
Correa J, Mamani M, Muñoz-Espinoza C, González-Agüero M, Defilippi B G, Campos-Vargas R, Pinto M, Hinrichsen P. 2016. New stable QTLs for berry firmness in table grapes. American Journal of Enology & Viticulture, 67, 212–217.
Correia S, Schouten R, Silva A P, Gonçalves B. 2018. Sweet cherry fruit cracking mechanisms and prevention strategies: A review. Scientia Horticulturae, 240, 369–377.
Cortés C, Ayuso M C, Palomares G, Cuartero J, Nuez F. 1983. Relationship between radial and concentric cracking of tomato fruit. Scientia Horticulturae, 21, 323–328.
Demirsoy L, Demirsoy H. 2004. The epidermal characteristics of fruit skin of some sweet cherry cultivars in relation to fruit cracking. Pakistan Journal of Botany, 36, 725–731.
Giné-Bordonaba J, Echeverria G, Ubach D, Aguiló-Aguayo I, López M L, Larrigaudière C. 2017. Biochemical and physiological changes during fruit development and ripening of two sweet cherry varieties with different levels of cracking tolerance. Plant Physiology and Biochemistry, 111, 216–225.
Dorais M, Demers D A, Papadopoulos A P, van Ieperen W. 2004. Greenhouse tomato fruit cuticle cracking. Horticultural Reviews, 30, 163–184.
Hardy O J, Vekemans X. 2002. SPAGeDi: A versatile computer program to analyze spatial genetic structure at the individual or population levels. Molecular Ecology Notes, 2, 618–620.
Hofshi R, Arpaia M L. 2002. Avocado fruit abnormalities and defects revisited. California Avocado Society Yearbook, 86, 147–162.
Hou L, Chen W, Zhang Z Y, Pang X M, Li Y Y. 2020. Genome-wide association studies of fruit quality traits in jujube germplasm collections using genotyping-by-sequencing. Plant Genome, 13, e20036.
Huang X M, Huang H B, Wang H C. 2005. Cell walls of loosening skin in post-veraison grape berries lose structural polysaccharides and calcium while accumulate structural proteins. Scientia Horticulturae, 104, 249–263.
Huang X M, Wang H C, Lu X J, Yuan W Q, Lu J M, Li J, Huang H B. 2006. Cell wall modifications in the pericarp of litchi (Litchi chinensis Sonn.) cultivars that differ in their resistance to cracking. The Journal of Horticultural Science and Biotechnology, 81, 231–237.
Hudson L W. 1956. The inheritance of resistance to fruit cracking in the tomato (Lycopersicon esculentum L.). MSc thesis, Oregon State College, Corvallis, OR.
Jiang F L, Lopez A, Jeon S, de Freitas S T, Yu Q, Wu Z, Labavitch M J, Tian S K, Powell A L T, Mitcham E. 2019. Disassembly of the fruit cell wall by the ripening-associated polygalacturonase and expansin influences tomato cracking. Horticulture Research, 6, 17.
Kasai S, Hayama H, Kashimura Y, Kudo S, Osanai Y. 2008. Relationship between fruit cracking and expression of the expansin gene MdEXPA3 in ‘Fuji’ apples (Malus domestica Borkh.). Scientia Horticulturae, 116, 194–198.
Khadivi-Khub A. 2007. Evaluation of genetic diversity in sweet cherry cultivars using morphological and molecular markers. MSc thesis, University of Tehran, Iran.
Khadivi-Khub A. 2011. Evaluation of genetic diversity in Cerasus subgenus using morphological and SSR markers. Ph D thesis, University of Tehran, Iran.
Khadivi-Khub A. 2015. Physiological and genetic factors influencing fruit cracking. Acta Physiologiae Plantarum, 37, 1718.
Knoche M, Peschel S, Hinz M, Bukovac M J. 2001. Studies on water transport through the sweet cherry fruit surface: II. Conductance of the cuticle in relation to fruit development. Planta, 213, 927–936.
Kovács E, Kristof Z, Perlaki R, Szőllősi D. 2008. Cell wall metabolism during ripening and storage of nonclimacteric sour cherry (Prunus cerasus L., cv. Kántorjánosi). Acta Alimentaria, 37, 415–426.
Kozich J J, Westcott S L, Baxter N T, Highlander S K, Schloss P D. 2013. Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the miseq Illumina sequencing platform. Applied & Environmental Microbiology, 79, 5112–5120.
Lancaster D M. 1984. The inheritance of radial fruit cracking in tomato (Lycopersicon Esculentum Mill.). Ph D thesis, University of Arkansas, Fayetteville.
Lang A, Düring H. 1990. Grape berry splitting and some mechanical properties of the skin. Vitis, 29, 61–70.
Li H, Peng Z Y, Yang X H, Wang W D, Fu J J, Wang J H, Han Y J, Chai Y C, Guo T T, Yang N, Liu N, Warburton M L, Cheng Y B, Hao X M, Zhang P, Zhao J Y, Liu Y J, Wang G Y, Li J S, Yan J B. 2013. Genome-wide association study dissects the genetic architecture of oil biosynthesis in maize kernels. Nature Genetics, 45, 43–50.
Li R, Yu C, Li Y, Lam T W, Yiu S M, Kristiansen K. 2009. SOAP2: An improved ultrafast tool for short read alignment. Bioinformatics, 25, 1966–1967.
Li W C, Wu J Y, Zhang H N, Shi S Y, Liu L Q, Shu B, Liang Q Z, Xie J H, Wei Y Z. 2014. De novo assembly and characterization of pericarp transcriptome and identification of candidate genes mediating fruit cracking in Litchi chinensis Sonn. International Journal of Molecular Sciences, 15, 17667–17685.
Lu W, Wang Y, Jiang Y, Li J, Liu H, Duan X, Song L. 2006. Differential expression of litchi XET genes in relation to fruit growth. Plant Physiology & Biochemistry, 44, 707–713.
Matas A J, Cobb E D, Paolillo D J, Niklas K J. 2004. Crack resistance in cherry tomato fruit correlates with cuticular membrane thickness. Hortscience, 39, 1354–1358.
McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, Garimella K, Altshuler D, Gabriel S, Daly M, DePristo M A. 2010. The genome analysis toolkit: a mapreduce framework for analyzing next-generation DNA sequencing data. Genome Research, 20, 1297–1303.
Measham P F, Bound S A, Gracie A J, Wilson S J. 2012. Crop load manipulation and fruit cracking in sweet cherry (Prunus avium L.). Advances in Horticultural Science, 26, 25–31.
Mintz-Oron S, Mandel T, Rogachev I, Feldberg L, Lotan O, Yativ M, Wang Z H, Jetter R, Venger I, Adato A, Aharoni A. 2008. Gene expression and metabolism in tomato fruit surface tissues. Plant Physiology, 147, 823–851.
Moctezuma E, Smith D L, Gross K C. 2003. Antisense suppression of a β-galactosidase gene (TBG6) in tomato increases fruit cracking. Journal of Experimental Botany, 390, 2025–2033.
Peschel S, Knoche M. 2005. Characterization of microcracks in the cuticle of developing sweet cherry fruit. Journal of the American Society for Horticultural Science, 130, 487–495.
Pirrello J, Regad F, Latche A, Pech J C, Bouzayen M. 2009. Regulation of tomato fruit ripening. CAB Reviews, 4, 1–14.
Quero-Garcia J, Campoy J A, Joly J, Tauzin Y, Rosyara U, Iezzoni A, Dirlewanger E. 2012. QTL detection for fruit weight, fruit firmness, and fruit cracking tolerance in sweet cherry. International Plant & Animal Genome XX Conference. San Diego, California, USA. pp.14–18.
Rab A, Haq I U. 2012. Irrigation intervals affect physicochemical quality attributes and skin cracking in litchi fruit. Turkish Journal of Agriculture & Forestry, 36, 553–562.
Riederer M, Schreiber L. 2001. Protecting against water loss: Analysis of the barrier properties of plant cuticles. Journal of Experimental Botany, 52, 2023–2032.
Roser I. 1996. Investigations on cracking susceptibility of sweet cherry cultivars. Acta Horticulturae, 410, 331–337.
Sawada E. 1931. Studies on the cracking of cherries. Agriculture and Horticulture, 6, 864–892.
Sekse L. 2008. Fruit cracking in sweet cherries-some recent advances. Acta Horticulturae, 795, 615–625.
Sherafati A, Hokmabadi H, Abbaspour H. 2012. Early splitting and irregular cracking hull on pistachio cultivars (Pistacia vera L.) in North-East of Iran. Acta Horticulturae, 963, 247–249.
Silva H, Rios J C, Maldonado J, Duchens H, Lang E, Carrasco B. 2012. A functional genomics approach to understand cracking susceptibility in sweet cherries (Prunus avium). Sixth Rosaceous Genomics Conference, San Michele all’Adige, Trento, Italy. 30 September–4 October. Edmund Mach Foundation, Trento, Italy. p. 25.
Simon G. 2006. Review on rain induced fruit cracking of sweet cherries (Prunus avium L.), its causes and the possibilities of prevention. International Journal of Horticultural Science, 12, 27–35.
Simon G, Hrotkó K, Magyar L. 2004. Fruit quality of sweet cherry cultivars grafted on four different rootstocks. Acta Horticulturae, 658, 365–370.
Vicens A, Fournand D, Williams P, Sidhoum L, Moutounet M, Moutounet M. 2009. Changes in polysaccharide and protein composition of cell walls in grape berry skin (cv. Shiraz) during ripening and over-ripening. Journal of Agricultural and Food Chemistry, 57, 2955–2960.
Wo S M, Osman A, Ahmad S H, Saari N. 2005. Peel and pulp splitting disorder in Mas banana (Musa cv Mas (AA)). Journal of Food Agriculture and Environment, 3, 213–217.
Xu J, Ding Z W, Vizcay-Barrena G, Shi J X, Liang W, Yuan Z, Werck-Reichhart D, Schreiber L, Wilson Z A, Zhang D B. 2014. ABORTED MICROSPORES acts as a master regulator of pollen wall formation in Arabidopsis. Plant Cell, 26, 1544–1556
Xu J, Yang C, Yuan Z, Zhang D, Gondwe M Y, Ding Z, Liang W, Zhang D, Wilson Z A. 2010. The ABORTED MICROSPORES regulatory network is required for postmeiotic male reproductive developent in Arabidopsis thaliana. Plant Cell, 22, 91–107.
Yamaguchi M, Sato I, Ishigguro M. 2002. Influences of epidermal cell size and flesh firmness on cracking susceptibility in sweet cherry (Prunus avium L.) cultivars and selections. Journal of the Japanese Society for Horticultural Science, 71, 738–746.
Yang Z N, Wu Z, Zhang C, Hu E M, Zhou R, Jiang F L. 2016. The composition of pericarp, cell aging, and changes in water absorption in two tomato genotypes: mechanism, factors, and potential role in fruit cracking. Acta Physiologiae Plantarum, 38, 215.
Young H W. 1960. Inheritance of radial fruit cracking in a tomato cross. Proceedings of the Florida State Horticultural Society, 72, 207–210.
Wang W, Lu W J, Li J G, Jiang Y M. 2006. Differential expression of two expansin genes in developing fruit of cracking-susceptible and -resistant litchi cultivars. Journal of the American Society for Horticultural Science, 131, 118–121.
Zhang C, Dong S S, Xu J Y, He W M, Yang T L. 2019. PopLDdecay: A fast and effective tool for linkage disequilibrium decay analysis based on variant call format files. Bioinformatics, 35, 1786–1788.
Zhang C, Guan L, Fan X, Zheng T, Dong T, Liu C, Fang J. 2020. Anatomical characteristics associated with different degrees of berry cracking in grapes. Scientia Horticulturae, 261, 108992.
Zhang H, Fan X, Zhang Y, Jiang J, Liu C. 2017. Identification of favorable SNP alleles and candidate genes for seedlessness in Vitis vinifera L. using genome-wide association mapping. Euphytica, 213, 136.
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