Abstract
Key message
Using two segregating population, watermelon stripe pattern underlying gene ClSP was delimited to a 611.78 Kb region, consisting of four discrete haploblocks and ongoing recombination suppression.
Abstract
Stripe pattern is an important commodity trait in watermelon, displaying diverse types. In this study, two segregating populations were generated for genetic mapping the single dominant locus ClSP, which was finally delimited to a 611.78 Kb interval with suppression of recombination. According to polymorphism sites detected among genotypes, four discrete haploblocks were characterized in this target region. Based on reference genomes, 81 predicted genes were annotated in the ClSP interval, including seven transcription factors namely as candidate No1-No7. Meanwhile, the ortholog gene of cucumber ist responsible for the irregular stripes was considered as candidate No8. Strikingly, gene structures of No1-No5 completely varied from their reference descriptions and subsequently re-annotated. For instance, the original adjacent distribution candidates No2 and No3 were re-annotated as No2_3, while No4 and No5 were integrated as No4_5. Sequence analysis demonstrated the third polymorphism in CDS of re-annotated No4_5 resulting in truncated proteins in non-stripe plants. Furthermore, only No4_5 was down-regulated in light green stripes relative to dark green stripes. Transcriptome analysis identified 356 DEGs between dark green striped and light green striped peels, with genes involved in photosynthesis and chloroplast development down-regulated in light green stripes but calcium ion binding related genes up-regulated. Additionally, 38 DEGs were annotated as transcription factors, with the majority up-regulated in light green stripes, such as ERFs and WRKYs. This study not only contributes to a better understanding of the molecular mechanisms underlying watermelon stripe development, but also provides new insights into the genomic structure of ClSP locus and valuable candidates.
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References
Danin-Poleg Y, Tadmor Y, Tzuri G, Reis N, Hirschberg J, Katzir N (2002) Construction of a genetic map of melon with molecular markers and horticultural traits, and localization of genes associated with ZYMV resistance. Euphytica 125:373–384
Gama R, Santos C, Dias R, Alves J, Nogueira T (2015) Microsatellite markers linked to the locus of the watermelon fruit stripe pattern. Genet Mol Res 14:269–276
Grumet R, Colle M (2016) Genomic analysis of cucurbit fruit growth. In: Grumet R, Katzir N, Garcia-Mas J (eds) Genetics and genomics of cucurbitaceae. Springer, Cham, pp 321–344
Guo S, Zhang J, Sun H, Salse J, Lucas WJ, Zhang H et al (2013) The draft genome of watermelon (Citrullus lanatus) and resequencing of 20 diverse accessions. Nat Genet 45:51–58
Guo S, Zhao S, Sun H, Wang X, Wu S, Lin T et al (2019) Resequencing of 414 cultivated and wild watermelon accessions identifies selection for fruit quality traits. Nat Genet 51:1616–1623
Gusmini G, Wehner TC (2006) Qualitative inheritance of rind pattern and flesh color in watermelon. J Heredity 97:177–185
Hao N, Du Y, Li H, Wang C, Wang C, Gong S et al (2018) CsMYB36 is involved in the formation of yellow green peel in cucumber (Cucumis sativus L.). Theor Appl Genet 131:1659–1669
HeeBum Y, SungWoo P, GungPyo L, SunCheol K, YongKwon K (2015) Linkage analysis of the three loci determining rind color and stripe pattern in watermelon. Korean J Hortic Sci 33:559–565
Kim H, Han D, Kang J, Choi Y, Levi A, Lee GP, Park Y (2015) Sequence-characterized amplified polymorphism markers for selecting rind stripe pattern in watermelon (Citrullus lanatus L.). Hortic Environ Biote 56:341–349
Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357–359
Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N et al (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25:2078–2079
Liu L, Sun T, Liu X, Guo Y, Huang X, Gao P, Wang X (2019) Genetic analysis and mapping of a striped rind gene (st3) in melon (Cucumis melo L.). Euphytica 215:20
Liu G, Li C, Yu H, Tao P, Yuan L, Ye J et al (2020) GREEN STRIPE, encoding methylated TOMATO AGAMOUS-LIKE 1, regulates chloroplast development and Chl synthesis in fruit. New Phytol 228:302–317
Lou L, Wehner TC (2016) Qualitative inheritance of external fruit traits in watermelon. HortScience 51:487–496
Lv J, Fu Q, Lai Y, Zhou M, Wang H (2018) Inheritance and gene mapping of spotted to non-spotted trait gene CmSp-1 in melon (Cucumis melo L. var. Chinensis Pangalo). Mol Breed 38:105
Meng L, Fan Z, Zhang Q, Wang C, Gao Y, Deng Y et al (2018) BEL1-LIKE HOMEODOMAIN 11 regulates chloroplast development and chlorophyll synthesis in tomato fruit. Plant J 94:1126–1140
Nadakuduti SS, Holdsworth WL, Klein CL, Barry CS (2014) KNOX genes influence a gradient of fruit chloroplast development through regulation of GOLDEN2-LIKE expression in tomato. Plant J 78:1022–1033
Paris HS (2003) Genetic control of irregular striping, a new phenotype in Cucurbita pepo. Euphytica 129:119–126
Paris HS (2009) Genes for “reverse” fruit striping in squash (Cucurbita pepo). J Heredity 100:371–379
Park Y, Cho S (2012) Watermelon production and breeding in South Korea. Isr J Plant Sci 60:415–423
Park S-w, Kim K-T, Kang S-C, Yang H-B (2016) Rapid and practical molecular marker development for rind traits in watermelon. Hortic Environ Biote 57:385–391
Poole C (1944) Genetics of cultivated cucurbits. J Heredity 35:122–128
Qian M, Sun Y, Allan AC, Teng Y, Zhang D (2014) The red sport of ‘Zaosu’ pear and its red-striped pigmentation pattern are associated with demethylation of the PyMYB10 promoter. Phytochemistry 107:16–23
Rhodes B, Zhang X (1995) Gene list for watermelon. Cucurbit Genet Coop
Song M, Zhang M, Cheng F, Wei Q, Wang J, Davoudi M et al (2020) An irregularly striped rind mutant reveals new insight into the function of PG1beta in cucumber (Cucumis sativus L.). Theor Appl Genet 133:371–382
Su W, Tao R, Liu W, Yu C, Yue Z, He S et al (2019) Characterization of four polymorphic genes controlling red leaf colour in lettuce that have undergone disruptive selection since domestication. Plant Biotechnol J 18:479–490
Telias A, Lin-Wang K, Stevenson DE, Cooney JM, Hellens RP, Allan AC et al (2011) Apple skin patterning is associated with differential expression of MYB10. BMC Plant Biol 11:93
Thorvaldsdottir H, Robinson JT, Mesirov JP (2013) Integrative genomics viewer (IGV): high-performance genomics data visualization and exploration. Brief Bioinform 14:178–192
Weetman LM (1937) Inheritance and correlation of shape, size and color in the watermelon, Citrullus vulgaris Schrad. Iowa Agric Home Econ Exp Station Res Bull 20:1
Wehner T, Pitrat M (2008) Overview of the genes of watermelon p. 79–89. In: Pitrat, M. (ed.). Cucurbitaceae 2008. Proceedings IXth EUCARPIA meeting on genetics and breeding of Cucurbitaceae, Il'institut National de la Recherche Agronomique, Avignon, France, 21–24 May 2008
Wei C, Chen X, Wang Z, Liu Q, Li H, Zhang Y et al (2017) Genetic mapping of the LOBED LEAF 1 (ClLL1) gene to a 127.6-kb region in watermelon (Citrullus lanatus L). PloS One 12:e0180741
Wei C, Zhu C, Yang L, Zhao W, Ma R, Li H et al (2019) A point mutation resulting in a 13 bp deletion in the coding sequence of Cldf leads to a GA-deficient dwarf phenotype in watermelon. Hortic Res 6:132
Wu S, Wang X, Reddy U, Sun H, Bao K, Gao L et al (2019) Genome of ‘Charleston Gray’, the principal American watermelon cultivar, and genetic characterization of 1,365 accessions in the U.S. National plant Germplasm system watermelon collection. Plant Biotechnol J 17:2246–2258
Xu W, Dubos C, Lepiniec L (2015) Transcriptional control of flavonoid biosynthesis by MYB-bHLH-WDR complexes. Trends Plant Sci 20:176–185
Yan C, An G, Zhu T, Zhang W, Zhang L, Peng L, Chen J, Kuang H (2019) Independent activation of the BoMYB2 gene leading to purple traits in Brassica oleracea. Theor Appl Genet 132:895–906
Zhai R, Wang Z, Yang C, Lin-Wang K, Espley R, Liu J et al (2019) PbGA2ox8 induces vascular-related anthocyanin accumulation and contributes to red stripe formation on pear fruit. Hortic Res 6:137
Zhang Z, Zhang Y, Sun L, Qiu G, Sun Y, Zhu Z et al (2018) Construction of a genetic map for Citrullus lanatus based on CAPS markers and mapping of three qualitative traits. Sci Hortic 233:532–538
Zhao M, Yang S, Chen CY, Li C, Shan W, Lu W et al (2015) Arabidopsis BREVIPEDICELLUS interacts with the SWI2/SNF2 chromatin remodeling ATPase BRAHMA to regulate KNAT2 and KNAT6 expression in control of inflorescence architecture. PLoS Genet 11:e1005125
Acknowledgements
This work was supported by funding from the National Natural Science Foundation of China [Grant No. 31701939] and the National Natural Science Foundation of Shaanxi Province, China [No. 2019JQ-324].
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CW designed the experiment and wrote the manuscript, with help from XZ. ZY performed the major experiments and analyzed the data. RM, DC, and XY participated in DNA extraction and phenotypic record. YH and CW contributed to gene cloning and sequence analysis. XP and LY participated in RNA extraction. All authors have read and approved the final manuscript.
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Communicated by Sanwen Huang.
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Yue, Z., Ma, R., Cheng, D. et al. Candidate gene analysis of watermelon stripe pattern locus ClSP ongoing recombination suppression. Theor Appl Genet 134, 3263–3277 (2021). https://doi.org/10.1007/s00122-021-03891-2
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DOI: https://doi.org/10.1007/s00122-021-03891-2