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Microsatellite loci reveal distinct populations with high diversity for the pathogenic fungus Pseudocercospora ulei from North-Western Amazonia

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Abstract

South American Leaf Blight (SALB) is caused by the Ascomycota fungus Pseudocercospora ulei. This disease is recognized as the main threat to Hevea brasiliensis plantations and the major phytosanitary challenge for the rubber industry in Latin America. Despite this, little is known about the pathogen’s genetic diversity and population structure in rubber-producing areas. Characterizing diversity in pathogen populations is essential for understanding their adaptation potential. This information is necessary for developing resistance improvement programs, as it helps estimate Hevea’s durable resistance. With this in mind, we characterized P. ulei’s genetic diversity and population structure in the northwest of Colombia’s Amazon. We used eight microsatellite loci (SSR) to evaluate the pathogens’ populations. Samples were obtained from four high-SALB incidence locations planted with the susceptible clone IAN 873. We found high genetic diversity in P. ulei populations. Although there is no evidence showing that sexual reproduction occurs in Caquetá’s P. ulei populations, our results suggest that, to some extent, genetic recombination is happening, as is the case for other Pseudocercospora species. Our findings support the idea that while asexual conidia are responsible for propagation within plantations, ascospores play a role in establishing P.ulei populations. More research is necessary to test this idea. Moreover, population structure correlated with different environmental conditions for both clone-corrected (Mantel statistic R = 0.053, p = 0.010) and non-clone-corrected data (Mantel statistic R = 0.060, p = 0.001) suggesting, that climate conditions might be contributing to P. ulei diversification. These results highlight the need to develop rubber plantations’ management strategies to reduce pathogen’s genetic diversity. This study is the first characterization of P. ulei populations in Colombia and thus, will provide crucial information for the H. brasiliensis resistance improvement program in the region.

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References

  • Adhikari, T. B., Muzhinji, N., Halterman, D., & Louws, F. J. (2021). Genetic diversity and population structure of Alternaria species from tomato and potato in North Carolina and Wisconsin. Scientific Reports, 11(1), 1–19. https://doi.org/10.1038/s41598-021-95486-6

    Article  CAS  Google Scholar 

  • Ahmadpour, A., Castell-Miller, C., Javan-Nikkhah, M., Naghavi, M. R., Dehkaei, F. P., Leng, Y., Puri, K. D., & Zhong, S. (2018). Population structure, genetic diversity, and sexual state of the rice brown spot pathogen Bipolaris oryzae from three Asian countries. Plant Pathology, 67(1), 181–192. https://doi.org/10.1111/ppa.12714

    Article  CAS  Google Scholar 

  • Ali, B., Sharmac, S., Lecontea, M., Shahd, S. J. A., Duveillere, E., Enjalbertf, J., & Deallavieille-Popea, V. C. (2016). Low pathotype diversity in a recombinant Puccinia striiformis population through convergent selection at the eastern part of Himalayan Centre of diversity (Nepal). International Journal of Laboratory Hematology, 38(1), 42–49. https://doi.org/10.1111/ijlh.12426

    Article  Google Scholar 

  • Apodaca, J. J., Rissler, L. J., & Godwin, J. C. (2012). Population structure and gene flow in a heavily disturbed habitat: Implications for the management of the imperilled Red Hills salamander (Phaeognathus hubrichti). Conservation Genetics, 13(4), 913–923. https://doi.org/10.1007/s10592-012-0340-3

    Article  Google Scholar 

  • Balloux, F., Lehmann, L., & De Meeûs, T. (2003). The population genetics of clonal and partially clonal diploids. Genetics, 164(4), 1635–1644.

    Article  Google Scholar 

  • Barrès, B., Carlier, J., Seguin, M., Fenouillet, C., Cilas, C., & Ravigné, V. (2012). Understanding the recent colonization history of a plant pathogenic fungus using population genetic tools and approximate Bayesian computation. Heredity, 109(5), 269–279. https://doi.org/10.1038/hdy.2012.37

    Article  PubMed  PubMed Central  Google Scholar 

  • Bevenuto, J. A., De Souza, J. R., & Furtado, E. L. (2017). Microcyclus ulei races in Brazil. Summa Phytopathologica, 43(4), 326–336. https://doi.org/10.1590/0100-5405/172339

    Article  Google Scholar 

  • Dray, S., Dufour, A. B., Thioulouse, J. (2020). ade4: analysis of Ecological Data: Exploratory and Euclidean Methods in Environmental Sciences. R package version 1.7–16. , 403.

  • Earl, D. A., & vonHoldt, B. M. (2012). STRUCTURE HARVESTER: A website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources, 4(2), 359–361. https://doi.org/10.1007/s12686-011-9548-7

    Article  Google Scholar 

  • Evanno, G., Regnaut, S., & Goudet, J. (2005). Detecting the number of clusters of individuals using the software STRUCTURE: A simulation study. Molecular Ecology, 14(8), 2611–2620. https://doi.org/10.1111/j.1365-294X.2005.02553.x

    Article  CAS  PubMed  Google Scholar 

  • Excoffier, L., & Lischer, H. (2015). Manual Arlequin Version 3.5. http://cmpg.unibe.ch/software/arlequin35.

  • Feldmann, F., Junqueira, N. T. ., & Meier, U. (2005). Phenological growth stages of the rubber tree Hevea brasiliensis (Willd. Ex Adr. de Juss.) Muell.-Arg.: Codification and description according to the BBCH scale, 14. http://dnb.ddb.de

  • Gasparotto, L., Ferreira, F. A., Santos, Á. F., Rezende-Pereira, J. C., & Furtado, E. L. (2012). Doenças das folhas. Brasilia. www.cpaa.embrapa.br

  • Gomes, L., Douhan, G., Lehner, M., Bibiano, L., & Mizubuti, E. (2018). Yellow Sigatoka epidemics caused by a panmictic population of Mycosphaerella musicola in Brazil. Plant Pathology, 67, 295–302.

    Article  Google Scholar 

  • Guo, X., & Mrázek, J. (2008). Long simple sequence repeats in host-adapted pathogens localize near genes encoding antigens, housekeeping genes, and pseudogenes. Journal of Molecular Evolution, 67(5), 497–509. https://doi.org/10.1007/s00239-008-9166-5

    Article  CAS  PubMed  Google Scholar 

  • Guyot, J., & Eveno, P. (2015). Maturation of perithecia and ascosporesdischarge in south American leaf blight of rubber tree. Eur. J. PlantPathol., 143, 427–436.

    Article  CAS  Google Scholar 

  • Guyot, J., & Le Guen, V. (2018). A review of a century of studies on south American leaf blight of the rubber tree. Plant Disease, 102(6), 1052–1065. https://doi.org/10.1094/PDIS-04-17-0592-FE

    Article  PubMed  Google Scholar 

  • Guyot, J., Condina, V., Doaré, F., Cilas, C., & Sache, I. (2014). Role of ascospores and conidia in the initiation and spread of south American leaf blight in a rubber tree plantation. Plant Pathology, 63(3), 510–518. https://doi.org/10.1111/ppa.12126

    Article  Google Scholar 

  • Halle, F., Oldeman, R. A. A., & Tomlinson, P. B. (1978). Tropical trees and forests an architectural analysis. Springer-Verlag., 441.

  • Hartmann, F. E., McDonald, B. A., & Croll, D. (2018). Genome-wide evidence for divergent selection between populations of a major agricultural pathogen. Molecular Ecology, 27(12), 2725–2741. https://doi.org/10.1111/mec.14711

    Article  PubMed  PubMed Central  Google Scholar 

  • Hora Junior, B. T. (2012). Molecular phylogeny and population genetics of Microcyclus ulei, causal agent of the south american leaf blight of Hevea brasiliensis. Universidad Federal de Vicosa- Brasil.

  • Hora Júnior, B. T. D., De Macedo, D. M., Barreto, R. W., Evans, H. C., Mattos, C. R. R., Maffia, L. A., & Mizubuti, E. S. G. (2014). Erasing the past: A new identity for the damoclean pathogen causing south American leaf blight of rubber. PLoS One, 9(8). https://doi.org/10.1371/journal.pone.0104750

  • IRSG. (2019). International rubber study group. Rubber Statiscal bulletin., (228), 12. http://www.rubberstudy.com/statistics.aspx

  • Junqueira, N. T. V., Chaves, G. M., Zambolim, L., Romeiro, R., & Gasparotto, L. (1984). Isolamento, cultivo e esporulação de Microcyclus ulei, agente etiológico do mal-das-folhas da seringueira. Revista Ceres, 31, 322–331.

    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. PeerJ, 2013(1), 1–14. https://doi.org/10.7717/peerj.281

    Article  Google Scholar 

  • Manzo-Sánchez, G., Orozco-Santos, M., Islas-Flores, I., Martínez-Bolaños, L., Guzmán-González, S., Leopardi-Verde, C. L., & Canto-Canché, B. (2019). Genetic variability of Pseudocercospora fijiensis, the black Sigatoka pathogen of banana (Musa spp.) in Mexico. Plant Pathology, 68(3), 513–522. https://doi.org/10.1111/ppa.12965

    Article  Google Scholar 

  • Maurice, S., Montes, M. S., Nielsen, B. J., Bødker, L., Martin, M. D., Jønck, C. G., Kjøller, R., & Rosendahl, S. (2019). Population genomics of an outbreak of the potato late blight pathogen, Phytophthora infestans , reveals both clonality and high genotypic diversity. Molecular Plant Pathology, 20, 1134–1146. https://doi.org/10.1111/mpp.12819

    Article  PubMed  PubMed Central  Google Scholar 

  • McDonald, B. A., & Linde, C. (2002). Pathogen population genetics, evolutionary potential, and durable resistance. Annual Review of Phytopathology, 40(1), 349–379. https://doi.org/10.1146/annurev.phyto.40.120501.101443

    Article  CAS  PubMed  Google Scholar 

  • Milgroom, M. G. (2015). Population biology of plant pathogens. The American Phytopathologican Society, 151, 84–148. https://doi.org/10.1145/3132847.3132886

    Article  Google Scholar 

  • Nei, M. (1978). Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics, 89(3), 583–590.

    Article  CAS  Google Scholar 

  • Parada-Rojas, C. H., & Quesada-Ocampo, L. M. (2018). Analysis of microsatellites from transcriptome sequences of Phytophthora capsici and applications for population studies. Scientific Reports, 8(1), 1–12. https://doi.org/10.1038/s41598-018-23438-8

    Article  CAS  Google Scholar 

  • Peever, T. L., Olsen, L., Ibañez, A., & Timmer, L. W. (2000). Genetic differentiation and host specificity among populations of Alternaria spp. causing brown spot of grapefruit and tangerine x grapefruit hybrids in Florida. Phytopathology, 90(4), 407–414. https://doi.org/10.1094/PHYTO.2000.90.4.407

    Article  CAS  PubMed  Google Scholar 

  • Pritchard, J., Wen, X., & Falush, D. (2010). Documentation for structure software : Version 2 . 3. Structure.

  • Sniegowski, P. D., Gerrish, P. J., Johnson, T., & Shaver, A. (2000). The evolution of mutation rates: Separating causes from consequences. Bioessays, 22, 1057–1066. https://doi.org/10.1002/1521-1878(200012)22:12<1057::AID-BIES3>3.0.CO;2-W

    Article  CAS  PubMed  Google Scholar 

  • Stenberg, P., Lundmark, M., & Saura, A. (2003). MLGsim: a program for detecting clones using a simulation approach. Molecular Ecology Notes. https://doi.org/10.1046/j.1471-8286.2003.00408.x

  • Sterling, A., & Melgarejo, L. M. (2018). Leaf gas exchange and chlorophyll a fluorescence in Hevea brasiliensis in response to Pseudocercospora ulei infection. Physiological and Molecular Plant Pathology, 103(July), 143–150. https://doi.org/10.1016/j.pmpp.2018.07.006

    Article  CAS  Google Scholar 

  • Sterling, A., & Rodriguez, C. (2011). Nuevos clones de caucho natural para la Amazonia colombiana: énfasis en la resistencia al mal suramericano de las hojas (Microcyclus ulei). (I. SINCHI, Ed.). Bogotá- Colombia.

  • Sterling, A. S., & Rodríguez, C. H. (2012). Ampliación de la base genética de caucho natural con proyección para la Amazonia colombiana: fase de evaluación en periodo improductivo a gran escala. Bogotá, Colombia.

  • Sterling, A., & Rodriguez, C. (2017). Bases técnicas para la selección, propagación y establecimiento de materiales regionales elite de caucho en Caquetá. Bogotá, Colombia.

  • Sterling, C. A., & Rodríguez, L. C. H. (2018). Estrategias de manejo para las principales enfermedades y plagas del cultivo del caucho con énfasis en la amazonia colombiana. Instituto Amazónico de Investigaciones Científicas SINCHI. Bogotá.

    Google Scholar 

  • Sterling, A., Rodríguez, O. L., & Quintero, L. (2010). Variabilidad fisiológica de aislamientos de Microcyclus ulei de la Amazonia colombiana. Momentos de Ciencia, 7(1), 30–35.

    Google Scholar 

  • Sterling, A., Galindo-Rodríguez, L. C., Suárez-Córdoba, Y. D., Velasco-Anacona, G., Andrade-Ramírez, T., & Gómez-Torres, A. K. (2019a). Early assessing performance and resistance of Colombian rubber tree genotypes under high south American leaf blight pressure in Amazon. Industrial Crops and Products, 141(March), 111775. https://doi.org/10.1016/j.indcrop.2019.111775

    Article  CAS  Google Scholar 

  • Sterling, A., Martínez-Viuche, E. J., Pimentel-Parra, G. A., Suárez-Córdoba, Y. D., Fonseca-Restrepo, J. A., & Virguez-Díaz, Y. R. (2019b). Dynamics of adaptive responses in growth and resistance of rubber tree clones under south American leaf blight non-escape conditions in the Colombian Amazon. Industrial Crops and Products, 141(April), 111811. https://doi.org/10.1016/j.indcrop.2019.111811

    Article  CAS  Google Scholar 

  • Stirling, D. (2004). DNA extraction from fungi, yeast, and bacteria. Methods in molecular biology (Clifton, N.J.), 226, 53–54. https://doi.org/10.1385/1-59259-384-4:53

    Article  Google Scholar 

  • Venkatachalam, P., Geetha, N., Sangeetha, P., & Thulaseedharan, A. (2013). Natural rubber producing plants : An overview. African Journal of Biotechnology, 12(12), 1297–1310. https://doi.org/10.5897/AJBX12.016

    Article  CAS  Google Scholar 

  • Weir, B., & C. Cockerham. (2008). Estimating F-Statistics for the Analysis of Population Structure Author ( s ): B . S . Weir and C . Clark Cockerham Published by : Society for the Study of Evolution Stable URL: http://www.jstor.org/stable/2408641, 38(6), 1358–1370.

  • Zhan, J., & Mcdonald, B. A. (2013). Field-based experimental evolution of three cereal pathogens using a mark-release-recapture strategy. Plant Pathology, 62(S1), 106–114. https://doi.org/10.1111/ppa.12130

    Article  Google Scholar 

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Acknowledgements

The authors would like to thank the project: “Ampliación de la base genética de caucho natural, Caquetá, Amazonia” for financing this study. The study was supported by Fondo de Ciencia, Tecnología e Innovación – FCTel del Sistema General de Regalías –SGR - Contract No. 59 -2013 - Instituto Amazónico de Investigaciones Científicas SINCHI - Gobernación del Caquetá. The project was co-executed by Universidad de la Amazonia and Asociación de Reforestadores y Cultivadores de Caucho del Caquetá (ASOHECA).

Funding

This study was funded by Fondo de Ciencia, Tecnología e Innovación – FCTel del Sistema General de Regalías –SGR - Contract No. 59–2013 - Instituto Amazónico de Investigaciones Científicas SINCHI – the Gobernación del Caquetá – the Universidad de la Amazonia, and the Asociación de Reforestadores y Cultivadores de Caucho del Caquetá ASOHECA.

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All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by GPV-A, AS and AR-B. The first draft of the manuscript was written by GPV-A and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

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Correspondence to Alejandro Reyes-Bermúdez.

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Supplementary material

Online resource 1

Isolate Information (DOCX 33 kb)

Online resource 2

Loci characterization (DOCX 14 kb)

Online resource 3

List of alleles found in eight microsatellite loci (SSR) evaluated in 100 P. ulei isolates from four H. brasiliensis clonal fields in the department of Caquetá, Colombian Amazon. (DOCX 34 kb)

Online resource 4

Probability of the occurrence and repeated occurrence of multilocus haplotypes (MLH) in the Pseudocercospora ulei dataset. (DOCX 25 kb)

Online resource 5

Analysis of Molecular Variance (AMOVA). (DOCX 14 kb)

Online resource 6

Delta K values of the 80 haplotypes of P. ulei. (DOCX 133 kb)

Online resource 7

Rarefaction curve to calculate the expected multilocus genotypes (eMLG) in five Pseudocercospora ulei populations from Brazil, Ecuador, Guatemala, French Guiana (Barres et al., 2012) and Colombia. (DOCX 130 kb)

Online Resource 8

Indices of genetic diversity of Pseudocercospora ulei populations from Brazil, Ecuador, Guatemala, French Guiana (Barres et al., 2012) and Colombia. (DOCX 16 kb)

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Velasco-Anacona, G.P., Sterling, A. & Reyes-Bermúdez, A. Microsatellite loci reveal distinct populations with high diversity for the pathogenic fungus Pseudocercospora ulei from North-Western Amazonia. Eur J Plant Pathol 163, 827–839 (2022). https://doi.org/10.1007/s10658-022-02520-y

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