Skip to main content
SpringerLink
Log in

Identification and mapping of CpPM10.1, a major gene involved in powdery mildew (race 2 France of Podosphaera xanthii) resistance in zucchini (Cucurbita pepo L.)

  • Original Article
  • Published:
Theoretical and Applied Genetics Aims and scope Submit manuscript

Key message

Powdery mildew resistance in zucchini is controlled by one major dominant locus, CpPM10.1. CpPM10.1 was fine mapped. The expression of candidate gene Cp4.1LG10g02780 in resistant individuals was significantly upregulated after inoculation with the powdery mildew.

Abstract

Powdery mildew (PM) is one of the most destructive fungal diseases, reducing the productivity of Cucurbita crops globally. PM influences the photosynthesis, growth and development of infected zucchini and seriously reduces fruit yield and quality. In the present study, the zucchini inbred line ‘X10′ had highly stable PM resistance, and the inbred line 'Jin234′ was highly susceptible to PM in the seedling stage and adult stages. Genetic analysis revealed that PM resistance in ‘X10′ is controlled by one major dominant locus. Based on the strategy of QTL-seq combined with linkage analysis and developed molecular markers, the major locus was found to be located in a 382.9-kb candidate region on chromosome 10; therefore, the major locus was named CpPM10.1. Using 1,400 F2 individuals derived from a cross between ‘X10′ and ‘JIN234′ and F2:3 offspring of the recombinants, the CpPM10.1 locus was defined in a region of approximately 20.9 kb that contained 5 coding genes. Among them, Cp4.1LG10g02780 contained a conserved domain (RPW8), which controls resistance to a broad range of PM pathogens. Cp4.1LG10g02780 also had nonsynonymous SNPs between the resistant ‘X10′ and susceptible ‘Jin234.′ Furthermore, the expression of Cp4.1LG10g02780 was strongly positively involved in PM resistance in the key period of inoculation. Further allelic diversity analysis in zucchini germplasm resources indicated that PM resistance was associated with two SNPs in the Cp4.1LG10g02780 RPW8 domain. This study not only provides highly stable PM resistance gene resources for cucurbit crops but also lays the foundation for the functional analysis of PM resistance and resistance breeding in zucchini.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Alfandi M, Luo JJ, Qi XH, Xu Q, Chen XH (2012) Expression of WRKY and MYB genes during infection with powdery mildew in cucumber (Cucumis sativus L). Afr J Biotechnol 11(47):10703–10710

    CAS  Google Scholar 

  • Abe A, Kosugi S, Yoshida K, Natsume S, Takagi H, Kanzaki H et al (2012) Genome sequencing reveals agronomically important loci in rice using MutMap. Nat Biotechnol 30:174–178

    Article  CAS  PubMed  Google Scholar 

  • Bonardi V, Tang S, Stallmann A, Roberts M, Cherkis K, Dangl JL (2011) Expanded functions for a family of plant intracellular immune receptors beyond specific recognition of pathogen effectors. Proc Natl Acad Sci USA 108(39):16463–16468

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Burkhardt A, Buchanan A, Cumbie JS, Savory EA, Chang JH, Day B (2015) Alternative splicing in the obligate biotrophic oomycete pathogen Pseudoperonospora cubensis. Mol Plant Microbe interact 28(3):298–309

    Article  CAS  PubMed  Google Scholar 

  • Burkhardt A, Day B (2016) Transcriptome and small RNAome dynamics during a resistant and susceptible interaction between cucumber and downy mildew. Plant Genome 9(1):1940–3372

    Article  CAS  Google Scholar 

  • ÇALIŞ Ö (2004) A novel broad spectrum resistance gene (RPW8) controls powdery mildews. Mediterr Agr Sci 21:2528–9675

    Google Scholar 

  • Cohen R, Hanan A, Paris HS (2003) Single-gene resistance to powdery mildew in zucchini squash (Cucurbita pepo). Euphytica 130:433–441

    Article  CAS  Google Scholar 

  • Cui J, Jiang N, Zhou X, Hou X, Yang G, Meng J, Luan Y (2018) Tomato MYB49 enhances resistance to Phytophthora infestans and tolerance to water deficit and salt stress. Planta 248(6):1487–1503

    Article  CAS  PubMed  Google Scholar 

  • Ding W, Wang Y, Qi C, Luo Y, Wang C, Xu W, Qu S (2021) Fine mapping identified the gibberellin 2-oxidase gene CpDw leading to a dwarf phenotype in squash (Cucurbita pepo L.). Plant Sci 306:110857

    Article  CAS  PubMed  Google Scholar 

  • Guo WL, Chen BH, Chen XJ, Guo YY, Yang HL, Li XZ et al (2018) Transcriptome profiling of pumpkin (Cucurbita moschata Duch.) leaves infected with powdery mildew. PLoS ONE 13(1):e0190175

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gurvitz A, Hartig A, Ruis H, Hamilton B, Couet HG (2002) Preliminary characterisation of DML1, an essential Saccharomyces cerevisiae gene related to misato of Drosophila melanogaster. FEMS Yeast Rse 2(2):123–135

    CAS  Google Scholar 

  • Hieno A, Naznin HA, Hyakumachi M, HiguchiTakeuchi M, Matsui M, Yamamoto YY (2016) Possible involvement of MYB44-mediated stomatal regulation in systemic resistance induced by Penicillium simplicissimum GP17-2 in Arabidopsis. Microbes Environ 31(2):154–159

    Article  PubMed  PubMed Central  Google Scholar 

  • Holdsworth WL, LaPlant KE, Bell DC, Jahn MM (2016) Cultivar-based introgression mapping reveals wild species-derived Pm-0, the major powdery mildew resistance locus in squash. PLoS ONE 11(12):1–20

    Article  CAS  Google Scholar 

  • Javier MP, José B, Aureliano B, Peio Z, Cristina E, Carlos MG, María F, Pedro G, Manuel J, Lukas M, Belén P, Joaquín C (2018) De-novo assembly of zucchini genome reveals a whole genome duplication associated with the origin of the Cucurbita genus. Plant Biotechnol J 16(6):1161–1171

    Article  CAS  Google Scholar 

  • Kimura M, Okano Y (2007) Human misato regulates mitochondrial distribution and morphology. Exp Cell Res 313(7):1393–1404

    Article  CAS  PubMed  Google Scholar 

  • Koller T, Brunner S, Herren G, Hurni S, Keller B (2018) Pyramiding of transgenic Pm3 alleles in wheat results in improved powdery mildew resistance in the field. Theor Appl Genet 131(4):861–871

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li H, Durbin R (2009) Fast and accurate short read alignment with burrows wheeler transform. Bioinformatics 25:1754–1760

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li X, Zhu D et al (2005) Descriptors and data standard for cucumber (Cucumis sativus L.). Agricultural Press of China, Peking

    Google Scholar 

  • Liu C, Zhang X, Wang Y (2018) Cloning and analysis of a powdery mildew responsive gene CmSAMDC from Cucumis melo L. Sheng Wu Gong Cheng Xue Bao 34(6):928–936

    PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-∆∆CT method. Methods 25(4):402–408

    Article  CAS  PubMed  Google Scholar 

  • Ma X, Li Y, Sun J, Wang T, Fan J, Lei Y et al (2014) Ectopic expression of RESISTANCE TO POWDERY MILDEW8.1 confers resistance to fungal and oomycete pathogens in Arabidopsis. Plant Cell Physiol 55(8):1484–1496

    Article  CAS  PubMed  Google Scholar 

  • Mccreight JD (2003) Genes for resistance to powdery mildew races 1 and 2U.S. in melon PI 313970. Hort Sci 38:591–594

    Google Scholar 

  • McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A et al (2010) The genome analysis toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genom Res 20:1297–1303

    Article  CAS  Google Scholar 

  • Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8(19):4321–4325

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nie J, He H, Peng J, Yang X, Bie B, Zhao J, Wang Y, Si L, Pan J, Cai R (2015a) Identification and fine mapping of pm5.1: a recessive gene for powdery mildew resistance in cucumber (Cucumis sativus L.). Mol Breed 35:7

    Article  CAS  Google Scholar 

  • Nie J, Wang Y, He H, Guo C, Zhu W, Pan J, Li D, Lian H, Pan J, Cai R (2015b) Loss-of-function mutations in CsMLO1 confer durable powdery mildew resistance in cucumber (Cucumis sativus L.). Front Plant Sci 6:1155

    Article  PubMed  PubMed Central  Google Scholar 

  • Qu S, Qi C, Wang Y, Jiang Y, Xu W, Cui C (2018) Identification of resistance to pathogens and germplasm resources of pumpkin powdery mildew. J Northeast Agr Univ 49(12):9–17

    Google Scholar 

  • Rasheed A, He Z, Gao F, Zhai SN, Jin H, Liu JD et al (2016) Development and validation of KASP assays for genes underpinning key economic traits in bread wheat. Theor Appl Genet 129:1843–1860

    Article  CAS  PubMed  Google Scholar 

  • Salari M, Panjehkeh N, Nasirpoor Z, Abkhoo J (2012) Reaction of melon (Cucumis melo L.) cultivars to soilborne plant pathogenic fungi in Iran. Afr J Biotechnol 11(87):15324–15329

    Google Scholar 

  • Semagn K, Babu R, Hearne S, Olsen M (2014) Single nucleotide polymorphism genotyping using kompetitive allele specific PCR (KASP): overview of the technology and its application in crop improvement. Mol Breed 33:1–14

    Article  CAS  Google Scholar 

  • Seo PJ, Park CM (2010) MYB96-mediated abscisic acid signals induce pathogen resistance response by promoting salicylic acid biosynthesis in Arabidopsis. New Phytol 186(2):471–483

    Article  CAS  PubMed  Google Scholar 

  • Wang W, Devoto A, Turner JG, Xiao S (2007) Expression of the membrane-associated resistance protein RPW8 enhances basal defense against biotrophic pathogens. Mol Plant Microbe Interact 20(8):966–976

    Article  CAS  PubMed  Google Scholar 

  • Wang X, Guan L, Gao X, Xiong L, Wang W, Han R (2011) Powdery mildew resistance gene (Pm-AN) located in a segregation distortion region of melon LGV. Euphytica 180(3):421–428

    Article  Google Scholar 

  • Xiao S, Brown S, Patrick E, Brearley C, Turner JG (2003) Enhanced transcription of the Arabidopsis disease resistance genes RPW8.1 and RPW8.2 via a salicylic acid-dependent amplification circuit is required for hypersensitive cell death. Plant Cell 15(1):33–45

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xiao S, Calis O, Patrick E, Zhang G, Charoenwattana P, Muskett P, Parker JE, Turner JG (2005) The atypical resistance gene, RPW8, recruits components of basal defence for powdery mildew resistance in Arabidopsis. Plant J 42(1):95–110

    Article  CAS  PubMed  Google Scholar 

  • Xiao S, Ellwood S, Calis O, Patrick E, Li T, Coleman M, Turner JG (2001) Broad-spectrum mildew resistance in Arabidopsis thaliana mediated by RPW8. Science 291(5501):118–120

    Article  CAS  PubMed  Google Scholar 

  • Xu X, Yu T, Xu R, Shi Y, Lin X, Xu Q, Qi X, Weng Y, Chen X (2016) Fine mapping of a dominantly inherited powdery mildew resistance major-effect QTL, Pm1.1, in cucumber identifies a 41.1 kb region containing two tandemly arrayed cysteine-rich receptor-like protein kinase genes. Theor Appl Genet 129:507–516

    Article  CAS  PubMed  Google Scholar 

  • Xu XW, Liu XL, Yan YL, Wang W, Gebretsadik K, Qi XH, Xu Q, Chen XH (2019) Comparative proteomic analysis of cucumber powdery mildew resistance between a single-segment substitution line and its recurrent parent. Hortic Res 6:115

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yuste-Lisbona FJ, Capel C, Gómez-Guillamón ML, Capel J, López-Sesé AI, Lozano R (2011a) Codominant PCR-based markers and candidate genes for powdery mildew resistance in melon (Cucumis melo L.). Theor Appl Genet 122(4):747–758

    Article  CAS  PubMed  Google Scholar 

  • Yuste-Lisbona FJ, Capel C, Sarria E, Torreblanca R, Gómez-Guillamón ML, Capel J, Lozano R, López-Sesé AI (2011b) Genetic linkage map of melon (Cucumis melo L.) and localization of a major QTL for powdery mildew resistance. Mol Breed 27(2):181–192

    Article  Google Scholar 

  • Zhang C, Anarjan MB, Win KT, Begum S, Lee SH (2021) QTL-seq analysis of powdery mildew resistance in a Korean cucumber inbred line. Theor Appl Genet 134(2):435–451

    Article  CAS  PubMed  Google Scholar 

  • Zhang K, Wang X, Zhu W, Qin X, Xu J, Cheng C, Lou Q, Li J, Chen J (2018) 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. Theor Appl Genet 131(10):2229–2243

    Article  CAS  PubMed  Google Scholar 

  • Zhao Minxue (2017) Fine mapping and candidate gene analysis of powdery mildew resistant in squash (Cucurbita pepo L). Dissertation, Hebei University of Engineering

  • Zhu Q, Gao P, Wan Y, Cui H, Fan C, Liu S, Luan F (2018) Comparative transcriptome profiling of genes and pathways related to resistance against powdery mildew in two contrasting melon genotypes. Sci Hortic 227(3):169–180

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by grants from the National Natural Science Foundation of China (32002051); the Postdoctoral Science Foundation of China (2019M661244); the Natural Science Foundation of Heilongjiang Province of China (C2018027); the Academic Backbone Foundation of Northeast Agricultural University (20XG03).

Author information

Authors and Affiliations

  1. Key Laboratory of Biology and Genetic Improvement of Horticultural Crops (Northeast Region), Ministry of Agriculture and Rural Affairs, Northeast Agricultural University, Harbin, 150030, China

    Yunli Wang, Cong Qi, Yusong Luo, Feng Zhang & Shuping Qu

  2. College of Horticulture and Landscape Architecture, Northeast Agricultural University, Harbin, 150030, China

    Yunli Wang, Cong Qi, Yusong Luo, Feng Zhang & Shuping Qu

  3. Anhui Jianghuai Horticulture Seeds Corporation Limited, Hefei, 230031, China

    Zuyun Dai & Man Li

Authors
  1. Yunli Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Cong Qi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yusong Luo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Feng Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Zuyun Dai
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Man Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Shuping Qu
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

SQ was the corresponding author, oversaw all activities related to the project implementation and manuscript development. YW performed the research, analyzed the data and prepared a draft of the manuscript. CQ and YL performed mapping of the candidate gene. FZ participated in the experiments. ML and ZD provided germplasm resources planting materials. All authors reviewed and approved this submission.

Corresponding author

Correspondence to Shuping Qu.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

The experiments comply with the current laws of the country in which we were performed.

Additional information

Communicated by Sandra Elaine Branham.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, Y., Qi, C., Luo, Y. et al. Identification and mapping of CpPM10.1, a major gene involved in powdery mildew (race 2 France of Podosphaera xanthii) resistance in zucchini (Cucurbita pepo L.). Theor Appl Genet 134, 2531–2545 (2021). https://doi.org/10.1007/s00122-021-03840-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-021-03840-z

Keywords

Search

Navigation