Skip to main content
SpringerLink
Log in

Development and characterization of microsatellite markers for the rubber tree powdery mildew pathogen Oidium heveae

  • Published:
European Journal of Plant Pathology Aims and scope Submit manuscript

Abstract

Powdery mildew, caused by Oidium heveae, is a major threat to rubber plantations worldwide. Population studies are scarce for this pathogen due to the lack of polymorphic molecular markers. In this study, sixteen polymorphic microsatellite loci were identified using DNA extracted from single lesions based on the whole-genome sequences of the pathogen. Primers of these loci were applied to 138 O. heveae samples from five counties in Hainan, China. The number of alleles per locus ranged from 2 to 11 and the gene diversity varied from 0.014 to 0.728. In total, 119 multilocus genotypes (MLGs) were observed for the 138 samples. However, only one sample was significantly distinct from the other samples base on DAPC analysis. Further study indicated that there were three subclusters for the other 137 samples, but no evidence for regional genotypic subdivision was identified. The microsatellite markers developed are very useful to study the genetic structure and the dispersal route of O. heveae, especially as it can use DNA extracted directly from infected leaves.

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

Similar content being viewed by others

References

  • Ali, S., Gautier, A., Leconte, M., Enjalbert, J., & de Vallavieille-Pope, C. (2011). A rapid genotyping method for an obligate fungal pathogen, Puccinia striiformis f. sp. tritici, based on DNA extraction from infected leaf and multiplex PCR genotyping. BMC Research Notes, 4, 240.

    Article  CAS  Google Scholar 

  • Ali, S., Gladieux, P., Leconte, M., Gautier, A., Justesen, A. F., Hovmøller, M. S., Enjalbert J., & Vallavieille, C. (2014) Origin, migration routes and worldwide population genetic structure of the wheat yellow rust pathogen Puccinia striiformis f.sp. tritici. PLoS Pathogens, 10(1), e1003903.

  • Benson, G. (1999). Tandem repeats finder: A program to analyze DNA sequences. Nucleic Acids Research, 27(2), 573–580.

    Article  CAS  Google Scholar 

  • Chen, X. M., Chen, H. L., Li, W. G., & Liu, S. J. (2016). Remote sensing monitoring of spring phenophase of natural rubber forest in Hainan province. Chinese Journal of Agrometeorology, 37(1), 111–116.

    Google Scholar 

  • Frenkel, O., Portillo, I., Brewer, M. T., Pèros, J. P., Cadle-Davidson, L., & Milgroom, M. G. (2012). Development of microsatellite markers from the transcriptome of Erysiphe necator for analyzing population structure in North America and Europe. Plant Pathology, 61, 106–119.

    Article  CAS  Google Scholar 

  • Glawe, D. A. (2008). The powdery mildews: A review of the world’s most familiar (yet poorly known) plant pathogens. Annual Review of Phytopathology, 46, 27–51.

    Article  CAS  Google Scholar 

  • Grover, A., & Sharma, P. C. (2016). Development and use of molecular markers: Past and present. Critical Reviews in Biotechnology, 36(2), 290–302.

    Article  CAS  Google Scholar 

  • Grünwald, N. J., Everhart, S. E., Knaus, B. J., & Kamvar, Z. N. (2017). Best practices for population genetic analyses. Phytopathology, 107(9), 1000–1010.

    Article  Google Scholar 

  • Jombart, T., Devillard, S., & Balloux, F. (2010). Discriminant analysis of principal components: A new method for the analysis of genetically structured populations. BMC Genetics, 11, 94.

    Article  Google Scholar 

  • Kamvar, Z. N., Tabima, J. F., & Grünwald, N. J. (2014). Poppr: An R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction. Peer J, 2, e281.

    Article  Google Scholar 

  • Khan, M. R., Rehman, Z. U., Nazir, S. N., Tshewang, S., & Ali, S. (2019). Genetic divergence and diversity in himalayan Puccinia striiformis populations from Bhutan, Nepal, and Pakistan. Phytopathology, 109(10), 1793–1800.

    Article  Google Scholar 

  • Lederson, G. B., Peever, T. L., Evans, K., & Amiri, A. (2021). High genetic diversity in predominantly clonal populations of the powdery mildew fungus Podosphaera leucotricha from U.S. apple orchards. Applied and Environmental Microbiology, 87(15), e0046921.

    Article  Google Scholar 

  • Limkaisang, S., Komun, S., Furtado, E. L., Liew, K. W., Salleh, B., Sato, Y., & Takamatsu, S. (2005). Molecular phylogenetic and morphological analyses of Oidium heveae, a powdery mildew of rubber tree. Mycoscience, 46, 220–226.

    Article  CAS  Google Scholar 

  • Liu, S. J., Zhou, G. S., & Fang, S. B. (2015). Climatic suitability regionalization of rubber plantation in China. Scientia Agricultura Sinica, 48, 2335–2345.

    Google Scholar 

  • Liyanage, K. K., Khan, S., Mortimer, P. E., Hyde, K. D., Xu, J., Brooks, S., & Ming, Z. (2016). Powdery mildew disease of rubber tree. Forest Pathology, 46, 90–103.

    Article  Google Scholar 

  • Liyanage, K. K., Khan, S., Brooks, S., Mortimer, P. E., Karunarathna, S. C., Xu, J., & Hyde, K. D. (2017). Taxonomic revision and phylogenetic analyses of rubber powdery mildew fungi. Microbial Pathogenesis, 105, 185–195.

    Article  CAS  Google Scholar 

  • Maddalena, G., Delmotte, F., Bianco, P. A., Lorenzis, G. D., & Toffolatti, S. L. (2020). Genetic structure of italian population of the grapevine downy mildew agent, plasmopara viticola. Annals of Applied Biology, 176(3), 257–267.

    Article  Google Scholar 

  • Nicolaisen, M., West, J. S., Sapkota, R., Canning, G. G. M., Schoen, C., & Justesen, A. F. (2017). Fungal communities in near surface air are similar across northwestern Europe. Frontiers in Microbiology, 8, 1729.

    Article  Google Scholar 

  • Qin, Y. X., Zhou, H. Z., Chen, J., Yang, J. H., Hu, Y. S., & Tang, C. R. (2017). Predominant ontamination agents in rubber tree tissue culture and its elimination. Botanical Research, 6(3), 167–174.

    Article  Google Scholar 

  • Szpiech, Z. A., Jakobsson, M., & Rosenberg, A. N. A. (2008). Adze: A rarefaction approach for counting alleles private to combinations of populations. Bioinformatics, 24(21), 2498–2504.

    Article  CAS  Google Scholar 

  • Tam, L. T. T., Dung, P. N., & Liem, N. V. (2016). First report of powdery mildew caused by Erysiphe quercicola on mandarin in Vietnam. Plant Disease, 100, 1777.

    Article  Google Scholar 

  • Tu, M., Cai, H. B., Hua, Y. W., Sun, A. H., & Huang, H. S. (2012). In vitro culture method of powdery mildew (Oidium heveae Steinmann) of Hevea brasiliensis. African Journal of Biotechnology, 11(68), 13167–13172.

    Article  CAS  Google Scholar 

  • Tucker, M. A., Moffat, C. S., Ellwood, S. R., Tan, K. C., & Oliver, R. P. (2015). Development of genetic SSR markers in Blumeria graminis f. sp. hordei and application to isolates from Australia. Plant Pathology, 64(2), 337–343.

    Article  CAS  Google Scholar 

  • Wang, M., Xue, F., Yang, P., Duan, X. Y., Zhou, Y. L., Sheng, C. Y., Zhang, G. Z., & Wang, B. T. (2014). Development of SSR markers for a phytopathogenic fungus, Blumeria graminis f.sp. tritici, using a fiasco protocol. Journal of Integrative Agriculture, 13(1), 100–104.

    Article  Google Scholar 

  • Wu, H., Pan, Y., Di, R., He, Q., Rajaofera, M. J. N., Liu, W., & Miao, W. (2019). Molecular identification of the powdery mildew fungus infecting rubber trees in China. Forest Pathology, 49, e12519.

    Article  Google Scholar 

  • Wyman, C. R., Hadziabdic, D., Boggess, S. L., Rinehart, T. A., & Trigiano, R. N. (2019). Low genetic diversity suggests the recent introduction of dogwood powdery mildew to North America. Plant Disease, 103(11), 2903–2912.

    Article  CAS  Google Scholar 

Download references

Funding

This work was funded by the National Natural Science Foundation of China (31972212, 31701731) and Central Public-interest Scientific Institution Basal Research Fund for Chinese Academy of Tropical Agricultural Sciences (No. 1630042017003). The authors have no conflict of interest to declare.

Author information

Authors and Affiliations

  1. State Key Laboratory Breeding Base of Green Pesticide and Agricultural Bioengineering, Key Laboratory of Green Pesticide and Agricultural Bioengineering, Ministry of Education, Guizhou University, Guiyang, 550025, People’s Republic of China

    Qiaohui Han

  2. Key Laboratory of Integrated Pest Management on Tropical Crops, Ministry of Agriculture, Environment and Plant Protection Institute, Chinese Academy of Tropical Agricultural Sciences, Haikou, 571001, People’s Republic of China

    Qiaohui Han, Haiyan Che, Daquan Luo & Xueren Cao

  3. College of Plant Protection, Hainan University, Haikou, 570228, People’s Republic of China

    Yongxiang He

  4. Rothamsted Research, Harpenden, AL5 2JQ, UK

    Jonathan S. West

Authors
  1. Qiaohui Han
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yongxiang He
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Haiyan Che
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Daquan Luo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jonathan S. West
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Xueren Cao
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Xueren Cao.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Supplementary Information

Fig. S1

The genotype accumulation curve for 138 rubber tree powdery mildew samples from Hainan, China. The boxplots represent the range of MLG numbers observed for each random sample of loci. (PNG 616 kb)

High Resolution Image (TIF 686 kb)

Fig. S2

Discriminant analysis of principal components (DAPC) of the 137 rubber tree powdery mildew samples from Hainan, China. A, Value of Bayesian information criteria (BIC); B, Scatterplot of DAPC. (PNG 75.9 kb)

High Resolution Image (TIF 1441 kb)

ESM 1

(XLS 23.3 kb)

Rights and permissions

Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Han, Q., He, Y., Che, H. et al. Development and characterization of microsatellite markers for the rubber tree powdery mildew pathogen Oidium heveae. Eur J Plant Pathol 164, 253–262 (2022). https://doi.org/10.1007/s10658-022-02555-1

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10658-022-02555-1

Keywords

Search

Navigation