Population genetic structure of the sheath blight pathogen Rhizoctonia solani AG-1 IA from rice fields in China, Japan and the Philippines

Christian Joseph Rili  Cumagun; Bruce Alan McDonald; Masao Arakawa; Vanina Lilian Castroagudín; Alexandre Magno Sebbenn; Paulo Cezar Ceresini

doi:10.4025/actasciagron.v42i1.42457

Christian Joseph Rili Cumagun University of the Philippines Los Banos
Bruce Alan McDonald Swiss Federal Institute of Technology
Masao Arakawa Meijo University
Vanina Lilian Castroagudín Universidade Estadual Paulista
Alexandre Magno Sebbenn Instituto Florestal de São Paulo
Paulo Cezar Ceresini Universidade Estadual Paulista http://orcid.org/0000-0003-2381-2792

DOI: https://doi.org/10.4025/actasciagron.v42i1.42457

Abstract

Sheath blight, caused by the fungal pathogen Rhizoctonia solani AG-1 IA is one of the most important rice diseases worldwide. The objetives of this study was to determine the predominant reproductive system and the genetic structure of 18 rice-infecting populations of R. solani sampled from China, Japan and the Philippines, the most important rice production countries in Asia. Knowledge about the population genetic structure of the pathogen in Asia is useful in identifying sources of infection and formulating sustainable management strategies for rice sheath blight. From a total of 717 isolates, 423 unique multilocus genotypes were detected based on nine microsatellite loci. The three country populations of R. solani AG-1 IA exhibited a mixed reproductive system, which included both sexual and asexual components. A moderate degree of clonality indicated that the asexual sclerotia represent important source of inoculum. Population subdivision varied within and among countries, fitting the isolation by distance model. While no subdivision was found among populations within Japan or within the Philippines, subdivision was detected among populations within China. Historic migration indicated high influx of immigrants from Japan into Northern, Central and Eastern China populations. Southern China contributed a high number of immigrants to the populations from the Philippines.

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References

Agapow, P.-M., & Burt, A. (2001). Indices of multilocus linkage disequilibrium. Molecular Ecology Notes, 1(1-2), 101-102. DOI: 10.1046/J.1471-8278.2000.00014.X

Anderson, J. B., & Kohn, L. M. (1995). Clonality in soilborne, plant-pathogenic fungi. Annual Review of Phytopatholology, 33(3), 369-91. DOI: 10.1146/Annurev.Py.33.090195.002101

Balloux, F., & Lugon-Moulin, N. (2002). The estimation of population differentiation with microsatellite markers. Molecular Ecology, 11(2), 155-165. DOI: 10.1046/J.0962-1083.2001.01436.X

Beerli, P. (2006). Comparison of bayesian and maximum-likelihood inference of population genetic parameters. Bioinformatics, 22(3), 341-345. DOI: 10.1093/Bioinformatics/Bti803

Beerli, P. (2009). How to use migrate or why are markov chain monte carlo programs difficult to use? In G. Bertorelle, M. W. Bruford, H. C. Hauffe, & A. Rizzoli (Eds.), Population genetics for animal conservation (p. 49-72). Cambridge, UK: Cambridge University Press.

Beerli, P., & Felsenstein, J. (1999). Maximun-likelihood estimation of migration rates and effective population numbers in two populations using a coalescent approach. Genetics, 152(2), 763-773.

Beerli, P., & Felsenstein, J. (2001). Maximum likelihood estimation of a migration matrix and effective population sizes in n subpopulations by using a coalescent approach. Pnas, 98(8), 4563-4568. DOI: 10.1073/Pnas.081068098

Beerli, P., & Palczewski, M. (2010). Unified framework to evaluate panmixia and migration direction among multiple sampling locations. Genetics, 185(1), 313-332. DOI: 10.1534/Genetics.109.112532

Bernardes de Assis, J., Peyer, P., Rush, M. C., Zala, M., McDonald, B. A., & Ceresini, P. C. (2008). Divergence between sympatric rice- and soybean-infecting populations of Rhizoctonia solani anastomosis group-1 Ia. Phytopathology, 98(12), 1326-1333. DOI: 10.1094/Phyto-98-12-1326

Bernardes de Assis, J., Storari, M., Zala, M., Wang, W., Jiang, D., Shidong, L., … Ceresini, P. C. (2009). Genetic structure of populations of the rice-infecting pathogen Rhizoctonia solani Ag-1 ia from China. Phytopathology, 99(9), 1090-1099. DOI: 10.1094/Phyto-99-9-1090

Bonferroni, C. E. (1935). Il calcolo delle assicurazioni su gruppi di teste. Rome, IT: Tipografia Del Senato.

Brown, A. H. D., Feldman, M. W., & Nevo, E. (1980). Multilocus structure of natural populations of Hordeum spontaneum. Genetics, 96(2), 523–536.

Chavarro Mesa, E., Ceresini, P. C., Ramos Molina, L. M., Pereira, D. A. S., Schurt, D. A., Vieira, J. R., ... McDonald, B. A. (2015). The urochloa foliar blight and collar rot pathogen Rhizoctonia solani ag-1 ia emerged in south america via a host shift from rice. Phytopathology, 105(11), 1475-1486. DOI: 10.1094/Phyto-04-15-0093-R

Cunningham, A. A., Daszak, P., & Rodríguez, J. P. (2003). Pathogen pollution: defining a parasitological threat to biodivesity conservation. Journal of Parasitology, 89(Supplement), 78-83.

Das, S. K. (2017). Rice cultivation under changing climate with mitigation practices: a mini review. Universal Journal of Agricultural Research, 5(6), 333-337. DOI: 10.13189/Ujar.2017.050603

Eizenga, G. C., Lee, F. N., & Rutger, J. N. (2002). Screening Oryza species plants for rice sheath blight resistance. Plant Disease, 86(7), 808-812. DOI: 10.1094/Pdis.2002.86.7.808

Excoffier, L., Laval, G., & Schneider, S. (2005). Arlequin (Version 3.0): an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online, 1(1), 47-50.

Fasola, M., Galeotti, P., Dong, Y., Dai, N., & Zhang, Y. (2004). Large numbers of breeding egrets and herons in China. Waterbirds, 27(1), 126-128.

Fukazu, R., Kashizaki, T., & Hirayama, S. (1960). Studies on secondary spread of rice sheath blight caused by basidiospores of pellicularia filamentosa. Bulletin of the Kochi Prefecture Agricultural Experiment Station, 2(1), 26-38.

Gnanamanickam, S. S. (2009). Biological control of rice diseases: Biological control of sheath blight (Shb) of rice. In H. M. T. Hokkanen, & I. Hokkanen (Eds.), Progress in biological control (p. 79-89). Dordrecht, GE: Springer.

González-Vera, A. D., Bernardes-De-Assis, J., Zala, M., McDonald, B. A., Correa-Victoria, F., Graterol-Matute, E. J., & Ceresini, P. C. (2010). Divergence between sympatric rice- and maize-infecting populations of Rhizoctonia solani ag 1 ia from Latin America. Phytopathology, 100(2), 172-182. DOI: 10.1094/Phyto-100-2-0172

Guo, S. W., & Thompson, E. A. (1992). Performing the exact test of hardy-weinberg proportions for multiple alleles. Biometrics, 48(2), 361-372. DOI: 10.2307/2532296

Jia, Y., Liu, G., Costanzo, S., Lee, S. H., & Dai, Y. T. (2009). Current progress on genetic interactions of rice with rice blast and sheath blight fungi. Frontiers of Agriculture in China, 3(3), 231-239. DOI: 10.1007/S11703-009-0062-6

Kauserud, H., & Schumacher, T. (2001). Outcrossing or inbreeding: DNA markers provide evidence for type of reproductive mode in Phellinus nigrolimitatus. Mycological Research, 105(6), 676–683. DOI: 10.1017/S0953756201004191

Lee, F. N., & Rush, M. C. (1983). Rice sheath blight: a major rice disease. Plant Disease, 67(7), 829-832. DOI: 10.1094/Pd-67-829

Linde, C. C., Zala, M., Paulraj, R. S. D., McDonald, B. A., & Gnanamanickam, S. S. (2005). Population structure of the rice sheath blight pathogen Rhizoctonia solani ag-1 ia from India. European Journal of Plant Pathology, 112(2), 113-121. DOI: 10.1007/S10658-005-1753-3

Liu, G., Jia, Y., Mcclung, A., Oard, J. H., Lee, F. N., & Correll, J. C. (2013). Confirming qtls and finding additional loci responsible for resistance to rice sheath blight disease. Plant Disease, 97(1), 113-117. DOI: 10.1094/ Pdis-05-12-0466-Re

Mantel, N. A. (1967). The detection of disease clustering and a generalized regression approach. Cancer Research, 27(2), 209-220.

Matsumoto, M. (2002). Trials of direct detection and identification of Rhizoctonia solani ag 1 and ag 2 subgroups using specifically primed pcr analysis. Mycoscience, 43(2), 185-189. DOI: 10.1007/S102670200

Maynard Smith, J., Smith, N. H., O’rourke, M., & Spratt, B. G. (1993). How clonal are bacteria? Pnas, 90(10), 4384-4388. DOI: 10.1073/Pnas.90.10.4384

McDonald, B. A., & Linde, C. (2002). Pathogen population genetics, evolutionary potential, and durable resistance. Annual Review of Phytopathology, 40(1), 349-379. DOI: 10.1146/Annurev.Phyto.40.120501.101443

Meirmans, P. G., & Van Tienderen, P. H. (2004). Genotype and genodive: two programs for the analysis of genetic diversity of asexual organisms. Molecular Ecology Notes, 4(4), 792-794. DOI: 10.1111/J.1471-8286.2004.00770.X

Milgroom, M. G. (1996). Recombination and the multilocus structure of fungal populations. Annual Review of Phytopathology, 34(1), 457-477.

Miyasaka, A., & Nakajima, T. (2009). Development of hymenia and basidiospore of Thanatephorus cucumeris (ag1-ia of Rhizoctonia solani) on rice in paddy fields. Kyushu Plant Protection Research, 55(1), 18-24. DOI: 10.4241/Kyubyochu.55.18

Ou, S. H. (1985). Rice diseases (2nd ed.). Farnham Royal: Commonwealth Agricultural Bureaux.

Padasht-Dehkaei, F., Zala, M., Okhovvat, S. M., Nikkhah, M. J., McDonald, B. A., & Ceresini, P. C. (2010). Population genetic evidence that basidiospores play an important role in the disease cycle of rice-infecting populations of Rhizoctonia solani ag-1 ia in Iran. Plant Pathology, 62(1), 49-58. DOI: 10.1111/J.1365-3059.2012.02613.X

Pascual, C. B., & Hyakumachi, M. (2000). Distribution of vegetatively compatible populations of Rhizoctonia solani ag-1 ia in a field planted with different host species. Journal of General Plant Pathology, 66(3), 206-209. DOI: 10.1007/Pl00012946

Pascual, C. B., Toda, T., Raymondo, A. D., & Hyakumachi, M. (2000). Characterization by conventional techniques and pcr of Rhizoctonia solani isolates causing banded leaf sheath blight in maize. Plant Pathology, 49(1), 108-118. DOI: 10.1046/J.1365-3059.2000.00429.X

Pritchard, J. K., Stephens, M., & Donnelly, P. (2000). Inference of population structure using multilocus genotype data. Genetics, 155(2), 945-959.

Raymond, M., & Rousset, F. (1995). Genepop (Version 1.2): Population genetics software for exact tests and ecumenicism. Journal of Heredity, 86(3), 248-249. DOI: 10.1093/Oxfordjournals.Jhered.A111573

Ren, C. M., Gao, B. D., & He, Y. C. (2001). Advance In rice resistance to rice sheath blight. Plant Protection, 27(1), 32-36.

Rosewich, U. L., Pettway, R. E., McDonald, B. A., & Kistler, H. C. (1999). High levels of gene flow and heterozygote excess characterize Rhizoctonia solani ag-1 Ia (Thanatephorus cucumeris) from Texas. Fungal Genetics and Biology, 28(3), 148-159. DOI: 10.1006/Fgbi.1999.1174

Rousset, F. (1997). Genetic differentiation and estimation of gene flow from f-statistics under isolation by distance. Genetics, 145(4), 1219-1228.

Singh, R., Sunder, S., & Kumar, P. (2016). Sheath blight of rice: current status and perspectives. Indian Phytopathology, 69(4), 340-351.

Sivalingam, P. N., Vishwakarma, S. N., & Singh, U. S. (2006). Role of seed-borne inoculum of Rhizoctonia solani in sheath blight of rice. Indian Phytopathology, 59(4), 445-452.

Slatkin, M. (1995). A measure of population subdivision based on microsatellite allele frequencies. Genetics, 139(1), 457-462.

Sumner, D. R. (1996). Sclerotia formation by Rhizoctonia species and their survival. In B. Sneh, Jabaji-Hare, S. Neate, & G. Dijst (Eds.), Rhizoctonia species: taxonomy, molecular biology, ecology, pathology and disease control (p. 207-215). Dordrecht, GE: Kluwer Academic Publishers.

Tang, S., Ding, L., & Bonjean, A. P. A. (2010 ). Rice production and genetic improvement in China. In Z. He, & A. P. A. Bonjean (Eds.), Cereals in China (p. 15-34). Mexico City, ME: Cimmyt Centro Internacional de Mejoramiento de Maíz y Trigo.

Tang, S. X., Wei, X. H., & Javier, E. (2004). Introduction and utilization of inger rice germplasm in China. Agricultural Science in China, 3(8), 561-567.

Wood, C., Qiao, Y., Li, P., Ding, P., Lu, B., & Xi, Y. (2010). Implications of rice agriculture for wild birds in China. Waterbirds, 33(Special Publication 1), 30-43.

Zala, M., McDonald, B. A., Bernardes De Assis, J., Ciampi, M. B., Storari, M., Peyer, P., & Ceresini, P. C. (2008). Highly polymorphic microsatellite loci in the maize- and rice-infecting fungal pathogen Rhizoctonia solani anastomosis group 1 ia. Molecular Ecology Resources, 8(3), 686-689. DOI: 10.1111/J.1471-8286.2007.02048.X

Zhan, J., Pettway, R. E., & McDonald, B. A. (2003). The global genetic structure of the wheat pathogen Mycosphaerella graminicola is characterized by high nuclear diversity, low mitochondrial diversity, regular recombination, and gene flow. Fungal Genetics and Biology, 38(3), 286-297. DOI: 10.1016/S1087-1845(02)00538-8

Zuo, S. M., Zhang, Y. F., Chen, Z. X., Chen, X., & Pan, X.-B. (2010). Current progress on genetics and breeding in resistance to rice sheath blight. Scientia Sinica Vitae, 40(11), 1014-1023. DOI: 10.1360/zc2010-40-11-1014