Abstract
Since 2015, the leaf blight of taro caused by Phytophthora colocasiae has resulted in severe economic loss in Japan. In order to investigate the causes of disease expansion and persistence, we need to clarify the mating type distribution of this pathogen, and to characterize each mating type. We collected 317 P. colocasiae isolates from 99 agricultural plots in seven prefectures from 2014 to 2020. We examined the mating type of each isolate and the distribution of mating types in each region and location. Five mating types were identified: heterothallic A1 and A2 and self-fertile (SF) A1, A2, and A1/A2. We found complex mating type distributions in some plots, and some leaves with multiple lesions carried more than one mating type. In addition, the variability of each mating type was checked after growth of single colonies from hyphal tips, zoosporangia, and zoospores. The SF type isolates were genetically unstable and segregated into both heterothallic and SF types after propagation. On the other hand, the heterothallic A1 and A2 isolates were stable. In pathogenicity tests, the heterothallic A1 isolates were less pathogenic than the heterothallic A2 and SF isolates. The SF strains can self-fertilize or mate with the heterothallic strains and produced abundant oospores. Therefore, the SF strains have the ability to reproduce at high rates and survive long term in the environment. The characteristics suggest that one possible causal factor for the rapid expansion and persistence of this disease is the appearance of the SF mating types in Japan.
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References
Afandi A, Hieno A, Wibowo A, Subandiyah S, Afandi SH, Tsuchida K, Kageyama K (2019) Genetic diversity of Phytophthora nicotianae reveals pathogen transmission mode in Japan. J Gen Plant Path 85:189–200
Ann PJ, Ko WH (1989) Effect of chloroneb and ethazol on mating type of Phytophthora parasitica and P. cinnamomi. Bot Bull Acad Sinica 30:207–210
Ann PJ, Kao CW, Ko WH (1986) Mating-type distribution of Phytophthora colocasiae in Taiwan. Mycopathologia 93:193–194. https://doi.org/10.1007/BF00443524
Brooks F (2005) Taro leaf blight. In: Oomycetes. American Phytopathological Society https ://www.apsne t.org/edcen ter/intro pp/lesso ns/fungi /Oomyc etes/Pages /TaroL eafBl ight.aspx. Cited 4 September 2018
Brooks F (2008) Detached-leaf bioassay for evaluating taro resistance to Phytophthora colocasiae. Plant Dis 92:126–131. https://doi.org/10.1094/PDIS-92-1-0126
Fyfe AM, Shaw DS (1992) An analysis of self-fertility in field isolates of Phytophthora infestans. Mycol Res 96:390–394. https://doi.org/10.1016/S0953-7562(09)80958-1
Gallegly ME (1970) Genetics of Phytophthora. Phytopathology 60:135–141. https://doi.org/10.1094/Phyto-60-1135
Cohen Y, Farkash S, Reshit Z, Baider A (1997) Oospore production of Phytophthora infestans in potato and tomato leaves. Phytopathology 87:191–196. https://doi.org/10.1094/PHYTO.1997.87.2.191
Gollifer DE, Jackson GVH, Newhook FJ (1980) Survival of inoculum of the leaf blight fungus Phytophthora colocasiae infecting taro, Colocasia esculenta in the Solomon Islands. Ann Appl Biol 94:379–390. https://doi.org/10.1111/j.1744-7348.1980.tb03953.x
Gómez ET (1925) Leaf Blight of Gabi Philipp Agric 14:429–440
Jung T, Jung MH, Scanu B, Seress D, Kovács GM, Maia C, Pérez-Sierra A, Chang T-T, Chandelier A, Heungens K, van Poucke K, Abad-Campos P, Léon M, Cacciola SO, Bakonyi J (2017) Six new Phytophthora species from ITS Clade 7a including two sexually functional heterothallic hybrid species detected in natural ecosystems in Taiwan. Persoonia 38:100–135
Ko WH (1979) Mating-type distribution of Phytophthora colocasiae on the island of Hawaii. Mycologia 71:434–437. https://doi.org/10.1080/00275514.1979.12021021
Ko WH (1988) Hormonal heterothallism and homothallism in Phytophthora. Ann Rev Phytopathol 26:57–73
Ko WH (1994) An alternative possible origin of the A2 mating type of Phytophthora infestans outside mexico. Phytopathology 84:1224–1227. https://doi.org/10.1094/Phyto-84-1224
Ko WH (2007) Hormonal regulation of sexual reproduction in Phytophthora. Bot Stud 48:365–375. https://doi.org/10.1099/00221287-116-2-459
Kurogi S (2017) The occurrences of taro leaf blight caused by Phytophthora colocasiae in Miyazaki prefecture and its control measures (in Japanese). Plant Protect 71:458–462
Lin MJ, Ko WH (2008) Occurrence of isolates of Phytophthora colocasiae in Taiwan with homothallic behavior and its significance. Mycologia 100:727–734. https://doi.org/10.3852/08-070
Masanto HA, Wibowo A, Subandiyah S, Shimizu M, Suga H, Kageyama K (2019) Genetic diversity of Phytophthora palmivora isolates from Indonesia and Japan using rep-PCR and microsatellite markers. J Gen Plant Path 85:367–381
Mellow KD, Tyson JL, Fullerton RA, Tugaga A, Maslen-Miller A (2018) Mating types of Phytophthora colocasiae on the island of Upolu Samoa. New Zeal Plant Prot 71:289–292. https://doi.org/10.30843/nzpp.2018.71.143
Morita Y, Tojo M (2007) Modifications of PARP medium using fluazinam, miconazole, and nystatin for detection of Pythium spp. in soil. Plant Dis 91:1591–1599. https://doi.org/10.1094/PDIS-91-12-1591
Mortimer AM, Shaw DS, Sansome ER (1977) Genetical studies of secondary homothallism in Phytophthora drechsleri. Arch Microbiol 111:255–259. https://doi.org/10.1007/BF00549363
Narula KL, Mehrotra RS (1980) Occurrence of A1 mating type of Phytophthora colocasiae. Indian Phytopathol 33:603–604
Quitugua RJ, Trujillo EE (1998) Survival of Phytophthora colocasiae in field soil at various temperatures and water matric potentials. Plant Dis 82:203–207. https://doi.org/10.1094/pdis.1998.82.2.203
Raciborski M (1900) Parasitic algae and fungi. Java Batavia Bull 19:189
Schmitthenner AF (1985) Problems and progress in control of Phytophthora root rot of soybean. Plant Dis 69:362–368. https://doi.org/10.1094/PD-69-362
Shrestha S, Hu J, Fryxell RT, Mudge J, Lamour K (2014) SNP markers identify widely distributed clonal lineages of Phytophthora colocasiae in Vietnam, Hawaii and Hainan Island, China. Mycologia 106:676–685
Shrestha SK, Miyasaka SC, Shintaku M, Kelly H, Lamour K (2017) Phytophthora colocasiae from Vietnam, China, Hawaii and Nepal: intra- and inter-genomic variations in ploidy and a long-lived, diploid Hawaiian lineage. Mycol Progress 16:893–904. https://doi.org/10.1007/s11557-017-1323-z
Singh D, Jackson G, Hunter D, Fullerton R, Lebot V, Taylor M, Iosefa T, Okpul T, Tyson J (2012) Taro leaf blight—a threat to food security. Agriculture 2:182–203. https://doi.org/10.3390/agriculture2030182
Sivamani E, Anuratha CS, Gnanamanickam SS (1987) Toxicity of Pseudomonas fluorescens towards bacterial plant pathogens of banana (Pseudomonas solanacearum) and rice (Xanthomonas campestris pv. oryzae). Curr Sci (bangalore) 56:547–548
Sneh B, McIntosh DL (1974) Studies on the behavior and survival of Phytophthora cactorum in soil. Revue Canadienne De Botanique 52:795–802. https://doi.org/10.1139/b74-103
Timmer LW, Castro J, Erwin DC, Belser WL, Zentmyer GA (1970) Genetic evidence for zygotic meiosis in Phytophthora capsici. Am J Bot 57:1211–1218. https://doi.org/10.1002/j.1537-2197.1970.tb09926.x
Tchameni SN, Mbiakeu SN, Sameza ML, Jazet PMD, Tchoumbougnang F (2017) Using citrus aurantifolia essential oil for the potential biocontrol of Colocasia esculenta (taro) leaf blight caused by Phytophthora colocasiae. Environ Sci Pollut Res 25:29929–29935
Tyson JL, Fullerton RA (2007) Mating types of Phytophthora colocasiae from the Pacific region, India and South-east Asia. Australas Plant Dis Notes 2:111–112. https://doi.org/10.1071/DN07046
Weste G (1983) Population dynamics and survival of Phytophthora. In: Erwin DC, Bartnicki-Garcia S, Tsao PH (eds) Phytophthora: its biology, taxonomy, ecology, and pathology. American Phytopathological Society, St. Paul, pp 237–258
Zhang KM, Zheng FC, Li YD, Ann PJ, Ko WH (1994) Isolates of Phytophthora colocasiae from Hainan island in China: evidence suggesting an Asian origin of this species. Mycologia 86:108–112. https://doi.org/10.2307/3760724
Acknowledgements
This study was supported by “Grant-in-Aid from the Ministry of Agriculture, Forestry, and Fisheries of Japan”. We thank T. Matsuda, H. Shibata, S. Yorozu, T. Nakagawa, Y. Murakami, K. Mouri and S. Yamamoto at Ehime Prefectural Government Agriculture, Forestry; S. Kurogi, Y. Kushima, K. Kuno and K. Shimoozono at Miyazaki Prefectural Agricultural Experiment Station; and Y. Nishi, K. Nishioka and T. Yuda at Kagoshima Prefectural Institute for Agricultural Development for providing the diseased taro leaf samples and isolates of P. colocasiae.
Funding
This research was supported by the Project of the NARO Bio-oriented Technology Research Advancement Institution (Research program on development of innovative technology), grant no. 29018C and Natural Science Special (Special Post) Scientific Research Fund Project of Guizhou University, grant no. 2020(12).
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WF, KO, and KK performed the experiments and analyzed the data. WF, AH, KO, SH, and KK conceived, drafted, and edited the manuscript. All authors have approved the final version of the manuscript.
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11557_2021_1762_MOESM1_ESM.docx
Supplementary file1 Table S1 Compositions of mating types in agricultural plots where two or more isolates were collected. (DOCX 17.1 KB)
11557_2021_1762_MOESM2_ESM.xlsx
Supplementary file2 Table S2 List of Phytophthora colocasiae isolates used for propagation from single hyphae, zoosporangia, and zoospores. (XLSX 11.0 KB)
11557_2021_1762_MOESM3_ESM.xlsx
Supplementary file3 Table S3 Comparison of pathogenicity between different mating-types of Phytophthora colocasiae. (XLSX 12.3 KB)
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Feng, W., Hieno, A., Otsubo, K. et al. Emergence of self-fertile Phytophthora colocasiae is a possible reason for the widespread expansion and persistence of taro leaf blight in Japan. Mycol Progress 21, 49–58 (2022). https://doi.org/10.1007/s11557-021-01762-0
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DOI: https://doi.org/10.1007/s11557-021-01762-0