Abstract
The dwarf watermelon forms, determined by bushiness and semi-bushiness, are of great economic importance, determining the rational use of sown areas owing to the high planting density and the possibility of mechanized processing and harvesting. In this regard, the study of genes that determine the small habitus of watermelon plants is an important task for accelerating the selection. The aim of this work was to analyze the known and search for new dwarf genes of watermelon Citrullus lanatus (Thunb.) Matsum. & Nakai by analyzing the unique VIR collection of melon crops and selection forms of the Kuban experimental station of VIR. As a result, the known mutation in the dw-1 gene (ABC transporter) was revealed in all bush and ultra-bush genotypes, except for two samples from Azerbaijan. The dwarfism of these two samples was not associated with other known genes, dsh (gibberellin-20-oxidase) and df (gibberellin-3β-hydroxylase), or their copies df2 and dsh2 identified in the present study. Thus, the VIR collection of melon crops contains potentially new genes that determine the dwarfism of watermelon.
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REFERENCES
Tekhanovich, G.A., Elatskova, A.G., and Elatskova, Y.A., Genetic sources for breeding bushy and short-vine watermelon cultivars, Proc. Appl. Bot. Genet. Breed., 2019, vol. 180, no. 2, pp. 89—94. https://doi.org/10.30901/2227-8834-2019-2-89-94
Peng, J., Richards, D.E., Hartley, N.M., et al., ‘Green revolution’ genes encode mutant gibberellin response modulators, Nature, 1999, vol. 400, no. 6741, pp. 256—261. https://doi.org/10.1038/22307
Spielmeyer, W., Ellis, M.H., and Chandler, P.M., Semidwarf (sd-1), “green revolution” rice, contains a defective gibberellin 20-oxidase gene, Proc. Natl. Acad. Sci. U.S.A., 2002, vol. 99, no. 13, pp. 9043—9048. https://doi.org/10.1073/pnas.132266399
Multani, D.S., Briggs, S.P., Chamberlin, M.A., et al., Loss of an MDR transporter in compact stalks of maize br2 and sorghum dw3 mutants, Science, 2003, vol. 302, no. 5642, pp. 81—84. https://doi.org/10.1126/science.1086072
Nomura, T., Jager, C.E., Kitasaka, Y., et al., Brassinosteroid deficiency due to truncated steroid 5 α-reductase causes dwarfism in the lk mutant of pea, Plant Physiol., 2004, vol. 135, no. 4, pp. 2220—2229. https://doi.org/10.1104/pp.104.043786
Pearce, S., Saville, R., Vaughan, S.P., et al., Molecular characterization of Rht-1 dwarfing genes in hexaploid wheat, Plant Physiol., 2011, vol. 157, no. 4, pp. 1820—1831. https://doi.org/10.1104/pp.111.183657
Pearce, S., Saville, R., Vaughan, S.P., et al., A cytochrome P450, OsDSS1, is involved in growth and drought stress responses in rice (Oryza sativa L.), Plant Mol. Biol., 2015, vol. 88, nos. 1—2, pp. 85—99. https://doi.org/10.1007/s11103-015-0310-5
Shifriss, O., Developmental reversal of dominance in Cucurbita pepo, Proc. Am. Soc. Hortic. Sci., 1947, vol. 50, pp. 330—346.
Denna, D.W. and Munger, H.M., Morphology of the bush and vine habits and the allelism of the bush genes in Cucurbita maxima and C. pepo squash, Proc. Am. Soc. Hortic. Sci., 1963, vol. 82, pp. 370—377.
Robinson, R.W., Munger, H.M., Whitaker, T.W., and Bohn, G.W., Genes of the Cucurbitaceae, HortScience, 1976, vol. 11, no. 6, pp. 554—568.
Paris, H.S. and Brown, R.N., The genes of pumpkin and squash, HortScience, 2005, vol. 40, no. 6, pp. 1620—1630. https://doi.org/10.21273/hortsci.40.6.1620
Wang, S., Li, H., Zhang, Z., et al., Comparative mapping of the dwarf gene Bu from tropical pumpkin (Cucurbita moschata Duchesne), Hortic. Sin., 2011, vol. 38, no. 1, pp. 95—100.
Zhang, G., Ren, Y., Sun, H., et al., A high-density genetic map for anchoring genome sequences and identifying QTLs associated with dwarf vine in pumpkin (Cucurbita maxima Duch.), BMC Genomics, 2015, vol. 16, no. 1, p. 1101. https://doi.org/10.1186/s12864-015-2312-8
Zhang, G., Ren, Y., Sun, H., et al., Fine genetic mapping of a locus controlling short internode length in melon (Cucumis melo L.), Mol. Breed., 2014, vol. 34, no. 3, pp. 949—961. https://doi.org/10.1007/s11032-014-0088-1
Knavel, D.E., Inheritance of a short-internode mutant of ‘mainstream’ muskmelon, HortScience, 1990, vol. 25, no. 10, pp. 1274—1275. https://doi.org/10.21273/HORTSCI.25.10.1274
Fukino, N., Ohara, T., Sugiyama, M., et al., Mapping of a gene that confers short lateral branching (slb) in melon (Cucumis melo L.), Euphytica, 2012, vol. 187, no. 1, pp. 133–143. https://doi.org/10.1007/S10681-012-0667-3/FIGURES/4
Pitrat, M., Linkage groups in Cucumis melo L., J. Hered., 1991, vol. 82, no. 5, pp. 406—411. https://doi.org/10.1093/oxfordjournals.jhered.a111112
Xin, M., Qin, Z., Wang, L., et al., Genetic identification of a dwarf mutant in cucumber (Cucumis sativus L.), Afr. J. Biotechnol., 2012, vol. 11, no. 20, pp. 4493—4498. https://doi.org/10.5897/AJB11.968
Hou, S., Niu, H., Tao, Q., et al., A mutant in the CsDET2 gene leads to a systemic brassinosteriod deficiency and super compact phenotype in cucumber (Cucumis sativus L.), Theor. Appl. Genet., 2017, vol. 130, no. 8, pp. 1693—1703. https://doi.org/10.1007/s00122-017-2919-z
Wang, H., Li, W., Qin, Y., et al., The cytochrome P450 gene CsCYP85A1 is a putative candidate for super compact-1 (Scp-1) plant architecture mutation in cucumber (Cucumis sativus L.), Front. Plant Sci., 2017, vol. 8, pp. 1—13. https://doi.org/10.3389/fpls.2017.00266
Kauffman, C.S. and Lower, R.L., Inheritance of an extreme dwarf plant type in the cucumber, J. Am. Soc. Hortic. Sci., 1976, vol. 101, no. 2, pp. 150—151.
Kubicki, B., Soltysiak, U., and Korzeniewska, A., Induced mutation in cucumber (Cucumis sativus L.): V. Compact type of growth, Genet. Pol., 1986, vol. 27, pp. 3—4.
Lin, T., Wang, S., Zhong, Y., et al., A truncated F-box protein confers the dwarfism in cucumber, J. Genet. Genomics, 2016, vol. 43, no. 4, pp. 223—226. https://doi.org/10.1016/j.jgg.2016.01.007
Xu, L., Wang, C., Cao, W., et al., CLAVATA1-type receptor-like kinase CsCLAVATA1 is a putative candidate gene for dwarf mutation in cucumber, Mol. Genet. Genomics, 2018, vol. 293, no. 6, pp. 1393—1405. https://doi.org/10.1007/s00438-018-1467-9
Li, Y., Yang, L., Pathak, M., et al., Fine genetic mapping of cp: a recessive gene for compact (dwarf) plant architecture in cucumber, Cucumis sativus L., Theor. Appl. Genet., 2011, vol. 123, no. 6, pp. 973—983. https://doi.org/10.1007/s00122-011-1640-6
Van der Linden, L., Patent WO/2017/042272, 2018.
Liu, P.B.W. and Loy, J.B., Inheritance and morphology of two dwarf mutants in watermelon, Am. Soc. Hortic. Sci. J., 1972, pp. 745—748.
Mohr, H.C. and Sandhu, M.S., Inheritance and morphological traits of a double recessive dwarf in watermelon, Citrullus lanatus (Thunb.) Mansf., J. Am. Soc. Hortic. Sci., 1975, vol. 100, no. 2, pp. 135—137.
Dyutin, K.E. and Afanasyeva, E.A., Inheritance of the short vine trait in watermelon, Tsitol. Genet., 1987, vol. 21, no. 3, pp. 227—229.
Hexun, H., Xiaoqi, Z., Zhencheng, W., et al., Inheritance of male-sterility and dwarfism in watermelon (Citrullus lanatus (Thunb.) Matsum. et Nakai), Sci. Hortic. (Amsterdam), 1998, vol. 74, no. 3, pp. 175—181. https://doi.org/10.1016/S0304-4238(97)00102-7
Dong, W., Wu, D., Li, G., et al., Next-generation sequencing from bulked segregant analysis identifies a dwarfism gene in watermelon, Sci. Rep., 2018, vol. 8, no. 1, p. 2908. https://doi.org/10.1038/s41598-018-21293-1
Dong, W., Wu, D., Wang, C., et al., Characterization of the molecular mechanism underlying the dwarfism of dsh mutant watermelon plants, Plant Sci., 2021, vol. 313, p. 111074. https://doi.org/10.1016/j.plantsci.2021.111074
Zhu, H., Zhang, M., Sun, S., et al., A single nucleotide deletion in an ABC transporter gene leads to a dwarf phenotype in watermelon, Front. Plant Sci., 2019, vol. 10, pp. 1—13. https://doi.org/10.3389/fpls.2019.01399
Cho, Y., Lee, S., Park, J., et al., Identification of a candidate gene controlling semi-dwarfism in watermelon, Citrullus lanatus, using a combination of genetic linkage mapping and QTL-seq, Hortic. Environ. Biotechnol., 2021, vol. 62, no. 3, pp. 447—459. https://doi.org/10.1007/S13580-020-00330-X/TABLES/3
Gebremeskel, H., Dou, J., Li, B., et al., Molecular mapping and candidate gene analysis for GA3 responsive short internode in watermelon (Citrullus lanatus), Int. J. Mol. Sci., 2019, vol. 21, no. 1, p. 290. https://doi.org/10.3390/ijms21010290
Wei, C., Zhu, C., Yang, L., et al., 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., 2019, vol. 6, no. 1, p. 132. https://doi.org/10.1038/s41438-019-0213-8
Zhang, T., Liu, J., Amanullah, S., et al., Fine mapping of Cla015407 controlling plant height in watermelon, J. Am. Soc. Hortic. Sci., 2021, vol. 146, no. 3, pp. 196—205. https://doi.org/10.21273/JASHS04934-20
Sun, Y., Zhang, H., Fan, M., et al., A mutation in the intron splice acceptor site of a GA3ox gene confers dwarf architecture in watermelon (Citrullus lanatus L.), Sci. Rep., 2020, vol. 10, no. 1, p. 14915. https://doi.org/10.1038/s41598-020-71861-7
Kong, Q., Yuan, J., Gao, L., et al., Evaluation of appropriate reference genes for gene expression normalization during watermelon fruit development, PLoS One, 2015, vol. 10, no. 6. e0130865. https://doi.org/10.1371/journal.pone.0130865
Tekhanovich, G.A., Elatskova, A.G., and Elatskov, Yu.A., The role of the world collection of cultivated cucurbits of VIR in breeding, Tr. Prikl. Bot., Genet. Sel., 2012, vol. 169, pp. 289—294.
Guo, S., Zhang, J., Sun, H., et al., The draft genome of watermelon (Citrullus lanatus) and resequencing of 20 diverse accessions, Nat. Genet., 2013, vol. 45, no. 1, pp. 51—58. https://doi.org/10.1038/ng.2470
Guo, S., Zhao, J., Sun, H., et al., Resequencing of 414 cultivated and wild watermelon accessions identifies selection for fruit quality traits, Nat. Genet., 2019, vol. 51, no. 11, pp. 1616—1623. https://doi.org/10.1038/s41588-019-0518-4
Dou, J., Zhao, S., Lu, X., et al., Genetic mapping reveals a candidate gene (ClFS1) for fruit shape in watermelon (Citrullus lanatus L.), Theor. Appl. Genet., 2018, vol. 131, no. 4, pp. 947—958. https://doi.org/10.1007/s00122-018-3050-5
Legendre, R., Kuzy, J., and McGregor, C., Markers for selection of three alleles of ClSUN25-26-27a (Cla011257) associated with fruit shape in watermelon, Mol. Breed., 2020, vol. 40, no. 2, p. 19. https://doi.org/10.1007/s11032-020-1104-2
Tian, S., Jiang, L., Gao, Q., et al., Efficient CRISPR/ Cas9-based gene knockout in watermelon, Plant Cell Rep., 2017, vol. 36, no. 3, pp. 399—406. https://doi.org/10.1007/s00299-016-2089-5
Wang, Y., Wang, J., Guo, S., et al., CRISPR/Cas9-mediated mutagenesis of ClBG1 decreased seed size and promoted seed germination in watermelon, Hortic. Res., 2021, vol. 8, no. 1, p. 70. https://doi.org/10.1038/s41438-021-00506-1
Tian, S., Jiang, L., Cui, X., et al., Engineering herbicide-resistant watermelon variety through CRISPR/ Cas9-mediated base-editing, Plant Cell Rep., 2018, vol. 37, no. 9, pp. 1353—1356. https://doi.org/10.1007/s00299-018-2299-0
Zhang, J., Guo, S., Ji, G., et al., A unique chromosome translocation disrupting ClWIP1 leads to gynoecy in watermelon, Plant J., 2020, vol. 101, no. 2, pp. 265—277. https://doi.org/10.1111/tpj.14537
Zhang, M., Liu, Q., Yang, X., et al., CRISPR/Cas9-mediated mutagenesis of Clpsk1 in watermelon to confer resistance to Fusarium oxysporum f.sp. niveum, Plant Cell Rep., 2020, vol. 39, no. 5, pp. 589—595. https://doi.org/10.1007/s00299-020-02516-0
Tekhanovich, G.A., Elatskova, A.G., and Elatskov, Yu.A., New sources of the genetic collection of cultivated cucurbits, in Nauchnoe obespechenie proizvodstva sel’skokhozyaistvennykh kul’tur v sovremennykh usloviyakh (Scientific Support for the Production of Agricultural Crops in Modern Conditions), 2016, pp. 198—203.
Miao, H., Zhang, S., Wang, M., et al., Fine mapping of virescent leaf gene v-1 in cucumber (Cucumis sativus L.), Int. J. Mol. Sci., 2016, vol. 17, no. 10, p. 1602. https://doi.org/10.3390/ijms17101602
Zhang, K., Li, Y., Zhu, W., et al., Fine mapping and transcriptome analysis of virescent leaf gene v-2 in cucumber (Cucumis sativus L.), Front. Plant Sci., 2020, vol. 11, p. 1458. https://doi.org/10.3389/FPLS.2020.570817/BIBTEX
ACKNOWLEDGMENTS
We thank Anastasia Yanyshevskaya (student at St. Petersburg University) for technical support.
Funding
Identification of the dw-1 donors in the collection of watermelon of VIR using DNA markers was carried out under support of the Ministry of Science and Higher Education of the Russian Federation, project no. 075-15-2020-911 from November 16, 2020, which provided the grant in the form of subsidy from the federal budget in order to provide governmental support for foundation and development of the world-level scientific center Agrotechnologies of the Future. Screening of new genes of watermelon bushiness was performed within the framework of research project no. 0481-2019-0001/0481-2022-0007.
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Strygina, K.V., Elatskova, A.G., Elatskov, Y.A. et al. Analysis of the Genes That Determine the Dwarf Form of Watermelon Citrullus lanatus (Thunb.) Matsum. & Nakai in the VIR Collection. Russ J Genet 58, 1457–1472 (2022). https://doi.org/10.1134/S1022795422120134
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DOI: https://doi.org/10.1134/S1022795422120134