Fine mapping and identification of candidate genes associated with powdery mildew resistance in melon (Cucumis melo L.)

Xiaoyu Duan , Yue Yuan , Núria Real , Mi Tang , Jian Ren , Jiaqi Wei , Bin Liu , Xuejun Zhang

Horticulture Research ›› 2024, Vol. 11 ›› Issue (10) : 222

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Horticulture Research ›› 2024, Vol. 11 ›› Issue (10) :222 DOI: 10.1093/hr/uhae222
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Fine mapping and identification of candidate genes associated with powdery mildew resistance in melon (Cucumis melo L.)
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Abstract

Powdery mildew (PM), a common disease of many major crop species, including melon (Cucumis melo L.), affects plant growth and fruit quality and seriously reduces production. Using a combined morphological and molecular approach, we attribute the PM pathogen that naturally occurs in melon to Podosphaera xanthii, and specifically to physiological race 1. An investigation into the genetic basis of PM resistance in melon using the resistant accession ‘PI 164637’ and susceptible counterpart ‘HDZ’ reveals dominant inheritance of PM resistance at the seedling stage, supported by F2 and backcross population segregation ratios. Adult plant assessments indicate a major gene with an additive effect for PM resistance. Bulk segregant analysis coupled with high-throughput sequencing identified a significant quantitative trait locus on chromosome 6 that is associated with PM resistance. Genetic mapping narrowed down the candidate region to 63.5 kb using InDel molecular markers, harboring 12 candidate genes. The marker chr06_indel_5 047 127 demonstrated high accuracy in screening PM resistance in an F2 segregating population and 30 inbred lines as natural populations. Functional annotation and expression analysis of candidate genes revealed that MYB transcription factor MELO3C006700, GATA transcription factor MELO3C028829 and heparanase-like protein MELO3C006697 are promising candidate genes for PM resistance in melon. The genetic architecture underlying this resistance in melon offers valuable insights for breeding programs, and the identified markers, especially chr06_indel_5 047 127, may enable practical applications for marker-assisted selection in developing PM-resistant melon varieties.

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Xiaoyu Duan, Yue Yuan, Núria Real, Mi Tang, Jian Ren, Jiaqi Wei, Bin Liu, Xuejun Zhang. Fine mapping and identification of candidate genes associated with powdery mildew resistance in melon (Cucumis melo L.). Horticulture Research, 2024, 11 (10) : 222 DOI:10.1093/hr/uhae222

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Acknowledgements

This study was financially supported by the China Agriculture Research System of MOF and MARA (Grant No. CARS-25); the specific research fund of The Innovation Platform for Academicians of Hainan Province (Grant No. YSPTZX202141); the earmarked fund for XinJiang Agriculture Research System (Grant No. XJARS-06). Project of Fund for Stable Support to Agricultural Sci-Tech Renovation (Grant no. xjnkywdzc-2022001-6).

Author contributions

X.Z. and M.T. designed the experiment project; X.D. wrote the original manuscript and created the graphs.; Y.Y. completed the major experiment; J.R. and J.W. assisted in completing the experiment. B.L. contributed to data analysis, N.R. revised the draft manuscript; X.Z. supervised the experiments. All authors have read and agreed to the published version of the manuscript.

Data availability

The data supporting this article are available within the article itself and its supplementary material online.

Conflict of interest statement

The authors declare no conflict of interest.

Supplementary Data

Supplementary data is available at Horticulture Research online.

References

[1]

Jenks MA, Bebeli PJ. Breeding for Fruit Quality. New Jersey, NJ: John Wiley & Sons; 2011

[2]

Chikh-Rouhou H, Tlili I, Ilahy R. et al. Fruit quality assessment and characterization of melon genotypes. Int J Veg Sci. 2021; 27: 3-19

[3]

Elliott C, Zhou F, Spielmeyer W. et al. Functional conservation of wheat and rice Mlo orthologs in defense modulation to the powdery mildew fungus. Mol Plant-Microbe Interact. 2002; 15:1069-77

[4]

Kunova A, Pizzatti C, Saracchi M. et al. Grapevine powdery mildew: fungicides for its management and advances in molecular detection of markers associated with resistance. Microorganisms. 2021; 9:1541

[5]

Kusch S, Németh MZ, Vaghefi N. et al. A short-read genome assembly resource for Leveillula taurica causing powdery mildew disease of sweet pepper (Capsicum annuum). Mol Plant-Microbe Interact. 2020; 33:782-6

[6]

Boissot N, Chovelon V, Rittener-Ruff V. et al. A highly diversified NLR cluster in melon contains homologs that confer powdery mildew and aphid resistance. Horticulture Research. 2023; 11:uhad256

[7]

Kuzuya M, Yashiro K, Tomita K. et al. Powdery mildew (Podosphaera xanthii) resistance in melon is categorized into two types based on inhibition of the infection processes. J Exp Bot. 2006; 57:2093-100

[8]

Ivanova Z, Vasileva K, Velkov N. et al. Evaluation of powdery mildew resistance in melon (Cucumis melo L.). Journal of Agricultural Sciences and Technology. 2019; 10:279-84

[9]

Cui L, Siskos L, Wang C. et al. Breeding melon (Cucumis melo) with resistance to powdery mildew and downy mildew. Horticultural Plant Journal. 2022a; 8:545-61

[10]

Diao Q, Cao Y, Jiang X. et al. Effect of powdery mildew on physiological and biochemical indexes of different melon varieties. International Journal of Horticulture. 2023; 13:4

[11]

Lebeda A, Krístková E, Sedláková B. et al. Gaps and perspectives of pathotype and race determination in Golovinomyces cichoracearum and Podosphaera xanthii. Mycoscience. 2011; 52:159-64

[12]

Lebeda A, Křístková E, Sedláková B. et al. Cucurbit powdery mildews: methodology for objective determination and denomination of races. Eur J Plant Pathol. 2016; 144:399-410

[13]

McCreight JD. Melon-powdery mildew interactions reveal variation in melon cultigens and Podosphaera xanthii races 1 and 2. J Am Soc Hortic Sci. 2006; 131:59-65

[14]

McCreight JD, Coffey MD. Inheritance of resistance in melon PI 313970 to cucurbit powdery mildew incited by Podosphaera xanthii race S. HortScience. 2011; 46:838-40

[15]

Kobori RF, Suzuki O, Wierzbicki R. et al. Occurrence of Podosphaera xanthii race 2 on Cucumis melo in Brazil. Plant Dis. 2004; 88:1161-1

[16]

Teixeira APM, Barreto FAS, Camargo LEA. An AFLP marker linked to the Pm-1 gene that confers resistance to Podosphaera xanthii race 1 in Cucumis melo. Genet Mol Biol. 2008; 31:547-50

[17]

Rabelo HO, Santos LS, Diniz GMM. et al. Cucurbits powdery mildew race identity and reaction of melon genotypes. Pesquisa Agropecuária Tropical. 2017; 47:440-7

[18]

Hosoya K, Kuzuya M, Murakami T. et al. Impact of resistant melon cultivars on Sphaerotheca fuliginea. Plant Breed. 2000; 119:286-8

[19]

Hong YJ, Hossain MR, Kim HT. et al. Identification of two new races of Podosphaera xanthii causing powdery mildew in melon in South Korea. The plant pathology journal. 2018; 34:182-90

[20]

Zhang C, Ren Y, Guo S. et al. Application of comparative genomics in developing markers tightly linked to the Pm-2F gene for powdery mildew resistance in melon (Cucumis melo L.). Euphytica. 2013; 190:157-68

[21]

Cui H, Fan C, Ding Z. et al. CmPMRl and CmPMrs are responsible for resistance to powdery mildew caused by Podosphaera xanthii race 1 in melon. Theor Appl Genet. 2022b; 135:1209-22

[22]

Křístková E, Lebeda A, Sedláková B. Species spectra, distribution and host range of cucurbit powdery mildews in the Czech Republic, and in some other European and Middle Eastern countries. Phytoparasitica. 2009; 37:337-50

[23]

Michelmore RW, Paran I, Kesseli RV. Identification of markers linked to disease-resistance genes by bulked segregant analysis: a rapid method to detect markers in specific genomic regions by using segregating populations. Proc Natl Acad Sci. 1991; 88:9828-32

[24]

Takagi H, Abe A, Yoshida K. et al. QTL-seq: rapid mapping of quantitative trait loci in rice by whole genome resequencing of DNA from two bulked populations. Plant J. 2013; 74:174-83

[25]

Liu L, Chen Y, Su Z. et al. A sequence-amplified characterized region marker for a single, dominant gene in melon PI 134198 that confers resistance to a unique race of Podosphaera xanthii in China. HortScience. 2010; 45:1407-10

[26]

Li B, Zhao Y, Zhu Q. et al. Mapping of powdery mildew resistance genes in melon (Cucumis melo L.) by bulked segregant analysis. Sci Hortic. 2017; 220:160-7

[27]

Cui H, Ding Z, Fan C. et al. Genetic mapping and nucleotide diversity of two powdery mildew resistance loci in melon (Cucumis melo). Phytopathology. 2020; 110:1970-9

[28]

Cao Y, Diao Q, Chen Y. et al. Development of KASP markers and identification of a QTL underlying powdery mildew resistance in melon (Cucumis melo L.) by bulked segregant analysis and RNA-seq. Front Plant Sci. 2021; 11:593207

[29]

Gao YR, Han YT, Zhao FL. et al. Identification and utilization of a new Erysiphe necator isolate NAFU1 to quickly evaluate powdery mildew resistance in wild Chinese grapevine species using detached leaves. Plant Physiol Biochem. 2016; 98:12-24

[30]

Dong S, Liu X, Han J. et al. CsMLO8/11 are required for full susceptibility of cucumber stem to powdery mildew and interact with CsCRK2 and CsRbohD. Horticulture Research. 2024; 11:uhad295

[31]

Marmolejo J, Siahaan SAS, Takamatsu S. et al. Three new records of powdery mildews found in Mexico with one genus and one new species proposed. Mycoscience. 2018; 59:1-7

[32]

Mc, Creight JD, Coffey MD, Ando K. et al. Cucurbit powdery mildew races on melon: current status in the US. In: Proceedings of the American Society of Horticulture Science Meeting. Orlando, FL, USA, 31 July-4 August 2018.

[33]

Borges RCF, Fonseca MEN, Boiteux LS. et al. Powdery mildew of chayote (Sechium edule) caused by Podosphaera xanthii race 2 in Brazil. J Phytopathol. 2023; 171:583-8

[34]

Bradshaw M, Tobin PC. Sequencing herbarium specimens of a common detrimental plant disease (powdery mildew). Phytopathology. 2020; 110:1248-54

[35]

Nanjundan J, Manjunatha C, Radhamani J. et al. Identification of new source of resistance to powdery mildew of Indian mustard and studying its inheritance. The Plant Pathology Journal. 2020; 36:111-20

[36]

Chen Q, Yu G, Wang X. et al. Genetics and resistance mechanism of the cucumber (Cucumis sativus L.) against powdery mildew. J Plant Growth Regul. 2021; 40:147-53

[37]

Epinat C, Pitrat M, Bertrand F. Genetic analysis of resistance of five melon lines to powdery mildews. Euphytica. 1992; 65:135-44

[38]

Kim HT, Park JI, Robin AHK. et al. Identification of a new race and development of DNA markers associated with powdery mildew in melon. Plant breeding and biotechnology. 2016; 4:225-33

[39]

Ning X, Wang X, Gao X. et al. Inheritances and location of powdery mildew resistance gene in melon Edisto 47. Euphytica. 2014; 195:345-53

[40]

Cackett L, Luginbuehl LH, Schreier TB. et al. Chloroplast development in green plant tissues: the interplay between light, hormone, and transcriptional regulation. The New phytologist. 2022; 233:2000-16

[41]

Yin Z, Liao W, Li J. et al. Genome-wide identification of GATA family genes in Phoebe bournei and their transcriptional analysis under abiotic stresses. Int J Mol Sci. 2023; 24:10342

[42]

Du X, Lu Y, Sun H. et al. Genome-wide analysis of wheat GATA transcription factor genes reveals their molecular evolutionary characteristics and involvement in salt and drought tolerance. Int J Mol Sci. 2022; 24:27

[43]

Schwechheimer C, Schröder PM, Blaby-Haas CE. Plant GATA factors: their biology, phylogeny, and phylogenomics. Annu Rev Plant Biol. 2022; 73:123-48

[44]

Zhang K, Wang X, Zhu W. et al. Complete resistance to powdery mildew and partial resistance to downy mildew in a Cucumis hystrix introgression line of cucumber were controlled by a co-localized locus. Der Züchter. 2018; 131:2229-43

[45]

Zhang K, Jia L, Yang D. et al. Genome-wide identification, phylogenetic and expression pattern analysis of GATA family genes in cucumber (Cucumis sativus L.). Plan Theory. 2021; 10:1626

[46]

Eudes A, Mouille G, Thévenin J. et al. Purification, cloning and functional characterization of an endogenous beta-glucuronidase in Arabidopsis thaliana. Plant Cell Physiol. 2008; 49:1331-41

[47]

Pechanova O, Hsu CY, Adams JP. et al. Apoplast proteome reveals that extracellular matrix contributes to multistress response in poplar. Genomics. 2010; 11:674

[48]

Witzel K, Shahzad M, Matros A. et al. Comparative evaluation of extraction methods for apoplastic proteins from maize leaves. Plant Methods. 2011; 7:48

[49]

Delaunois B, Colby T, Belloy N. et al. Large-scale proteomic analysis of the grapevine leaf apoplastic fluid reveals mainly stress-related proteins and cell wall modifying enzymes. BMC Plant Biol. 2013; 13:24

[50]

Zheng H, Dong L, Han X. et al. The TuMYB46L-TuACO3 module regulates ethylene biosynthesis in einkorn wheat defense to powdery mildew. New Phytol. 2020; 225:2526-41

[51]

Yu Y, Guo D, Li G. et al. The grapevine R2R3-type MYB transcription factor VdMYB1 positively regulates defense responses by activating the stilbene synthase gene 2 (VdSTS2). BMC Plant Biol. 2019; 19:1-15

[52]

Hosoya K, Narisawa K, Pitrat M. et al. Race identification in powdery mildew (Sphaerotheca fuliginea) on melon (Cucumis melo) in Japan. Plant Breed. 1999; 118:259-62

[53]

Kumar S, Stecher G, Li M. et al. Mega X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol. 2018; 35:1547-9

[54]

Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution. 1985; 39:783-91

[55]

Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987; 4:406-25

[56]

Allen GC, Flores-Vergara MA, Krasynanski S. et al. A modified protocol for rapid DNA isolation from plant tissues using cetyltrimethylammonium bromide. Nat Protoc. 2006; 1:2320-5

[57]

Li H, Handsaker B, Wysoker A. et al. The sequence alignment/map format and SAMtools. Bioinformatics. 2009; 25:2078-9

[58]

Chrambach A, Rodbard D. Polyacrylamide gel electrophoresis. Science. 1971; 172:440-51

[59]

Meng L, Li H, Zhang L. et al. QTL IciMapping: integrated software for genetic linkage map construction and quantitative trait locus mapping in biparental populations. The Crop Journal. 2015; 3:269-83

[60]

Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods. 2001; 25:402-8

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