Spot blotch, caused by the pathogen Bipolaris sorokiniana, is an important foliar disease of wheat in warm and humid regions worldwide. The fungal virulence factor ToxA interacts with Tsn1 in wheat and leads to a susceptible reaction. ToxA has been found in B. sorokiniana populations of Australia, the USA, and India, and here we report its occurrence in Mexico, based on analysis of a collection of 196 Mexican isolates of B. sorokiniana. The isolates were collected from experimental stations and farmers’ fields in nine states of Mexico, during the period from 1992 to 2017. A PCR assay with the ToxA-specific marker was conducted, and the results revealed the presence of ToxA in 20 isolates (10.2%). Culture filtrate infiltration experiments confirmed that all the 20 isolates were able to induce necrosis reaction on Glenlea, a wheat genotype with Tsn1. This is the first report on the occurrence of ToxA in Mexican B. sorokiniana population, which is key information for breeding wheat for resistance against spot blotch.
This is a preview of subscription content, access via your institution.
Buy single article
Instant access to the full article PDF.
Tax calculation will be finalised during checkout.
Subscribe to journal
Immediate online access to all issues from 2019. Subscription will auto renew annually.
Tax calculation will be finalised during checkout.
Acharya K, Dutta AK, Pradhan P (2011) Bipolaris sorokiniana (Sacc.) Shoem.: the most destructive wheat fungal pathogen in the warmer areas. Australian Journal of Crop Science 5:1064–1071
Adhikari TB, Bai J, Meinhardt SW, Gurung S, Myrfield M, Patel J, Ali S, Gudmestad NC, Rasmussen JB (2009) Tsn1-mediated host responses to ToxA from Pyrenophora tritici-repentis. Molecular Plant-Microbe Interactions 22:1056–1068
Antoni EA, Rybak K, Tucker MP, Hane JK, Solomon PS, Drenth A, Shankar M, Oliver RP (2010) Ubiquity of ToxA and absence of ToxB in Australian populations of Pyrenophora tritici-repentis. Australasian Plant Pathology 39:63–68
Ciuffetti LM, Francl LJ, Ballance GM, Bockus WW, Lamari L, Meinhardt SW, Rasmussen JB (1998) Standardization of toxin nomenclature in the Pyrenophora tritici-repentis/wheat interaction. Canadian Journal of Plant Pathology 20:421–424
Duveiller E, Kandel YR, Sharma RC, Shrestha SM (2005) Epidemiology of foliar blights (spot blotch and tan spot) of wheat in the plains bordering the himalayas. Phytopathology 95:248–256
Faris JD, Zhang Z, Lu H, Lu S, Reddy L, Cloutier S, Fellers JP, Meinhardt SW, Rasmussen JB, Xu SS, Oliver RP, Simons KJ, Friesen TL (2010) A unique wheat disease resistance-like gene governs effector-triggered susceptibility to necrotrophic pathogens. Proceedings of the National Academy of Sciences of the United States of America 107:13544–13549
Friesen TL, Stukenbrock EH, Liu Z, Meinhardt S, Ling H, Faris JD, Rasmussen JB, Solomon PS, McDonald BA, Oliver RP (2006) Emergence of a new disease as a result of interspecific virulence gene transfer. Nature Genetics 38:953–956
Friesen TL, Holmes DJ, Bowden RL, Faris JD (2018) ToxA is present in the U.S. Bipolaris sorokiniana population and is a significant virulence factor on wheat harboring Tsn1. Plant Disease 102:2446–2452
Gilchrist-Saavedra L, Fuentes-Dávila G, Martínez-Cano C, López-Atilano RM, Duveiller E, Singh RP, Henry M, García IA (2006) Practical guide to the identification of selected diseases of wheat and barley, 2nd edn. CIMMYT, Mexico
Han Q, Huang L, Buchenauer H, Wang C, Kang Z (2010) Cytological study of wheat spike infection by Bipolaris sorokiniana. Journal of Phytopathology 158:22–29
Hu W, He X, Dreisigacker S, Sansaloni CP, Juliana P, Singh PK (2019) A wheat chromosome 5AL region confers seedling resistance to both tan spot and Septoria nodorum blotch in two mapping populations. Crop Journal 7:809–818
Kumar J, Schäfer P, Hückelhoven R, Langen G, Baltruschat H, Stein E, Nagarajan S, Kogel KH (2002) Bipolaris sorokiniana, a cereal pathogen of global concern: cytological and molecular approaches towards better control. Molecular Plant Pathology 3:185–195
Liu ZH, Faris JD, Meinhardt SW, Ali S, Rasmussen JB, Friesen TL (2004) Genetic and physical mapping of a gene conditioning sensitivity in wheat to a partially purified host-selective toxin produced by Stagonospora nodorum. Phytopathology 94:1056–1060
Manning VA, Ciuffetti LM (2005) Localization of Ptr ToxA produced by Pyrenophora tritici-repentis reveals protein import into wheat mesophyll cells. Plant Cell 17:3203–3212
Manning VA, Hardison LK, Ciuffetti LM (2007) Ptr ToxA interacts with a chloroplast-localized protein. Molecular Plant-Microbe Interactions 20:168–177
McDonald MC, Razavi M, Friesen TL, Brunner PC, McDonald BA (2012) Phylogenetic and population genetic analyses of Phaeosphaeria nodorum and its close relatives indicate cryptic species and an origin in the Fertile Crescent. Fungal Genetics and Biology 49:882–895
McDonald MC, Oliver RP, Friesen TL, Brunner PC, McDonald BA (2013) Global diversity and distribution of three necrotrophic effectors in Phaeosphaeria nodorum and related species. New Phytologist 199:241–251
McDonald MC, Ahren D, Simpfendorfer S, Milgate A, Solomon PS (2018) The discovery of the virulence gene ToxA in the wheat and barley pathogen Bipolaris sorokiniana. Molecular Plant Pathology 19:432–439
McDonald MC, Taranto AP, Hill E, Schwessinger B, Liu Z, Simpfendorfer S, Milgate A, Solomon PS (2019) Transposon-mediated horizontal transfer of the host-specific virulence protein ToxA between three fungal wheat pathogens. mBio 10:e01515–e01519
Miki S, Matsui K, Kito H, Otsuka K, Ashizawa T, Yasuda N, Fukiya S, Sato J, Hirayae K, Fujita Y, Nakajima T, Tomita F, Sone T (2009) Molecular cloning and characterization of the AVR-Pia locus from a Japanese field isolate of Magnaporthe oryzae. Molecular Plant Pathology 10:361–374
Nakajima H, Toratsu Y, Fujii Y, Ichinoe M, Hamasaki T (1998) Biosynthesis of sorokinianin a phytotoxin of Bipolaris sorokiniana: evidence of mixed origin from the sesquiterpene and TCA pathways. Tetrahedron Letters 39:1013–1016
Navathe S, Yadav PS, Chand R, Mishra VK, Vasistha NK, Meher PK, Joshi AK, Gupta PK (2020) ToxA-Tsn1 interaction for spot blotch susceptibility in Indian wheat: an example of inverse gene-for-gene relationship. Plant Disease 104:71–81
Nicholson P, Simpson DR, Weston G, Rezanoor HN, Lees AK, Parry DW, Joyce D (1998) Detection and quantification of Fusarium culmorum and Fusarium graminearum in cereals using PCR assays. Physiological and Molecular Plant Pathology 53:17–37
SAGARPA (2016) Anuario estadístico de la producción agrícola. Available at: http://infosiap.siap.gob.mx/aagricola_siap_gb/icultivo/index.jsp. Accessed 6 Aug 2020
Singh PK, Zhang Y, He X, Singh RP, Chand R, Mishra VK, Malaker PK, Reza MA, Rahman MM, Islam R, Chowdhury AK, Bhattacharya PM, Kalappanavar IK, Crossa J, Joshi AK (2015) Development and characterization of the 4th CSISA-spot blotch nursery of bread wheat. European Journal of Plant Pathology 143:595–605
Singh RP, Singh PK, Rutkoski J, Hodson DP, He X, Jørgensen LN, Hovmøller MS, Huerta-Espino J (2016) Disease impact on wheat yield potential and prospects of genetic control. Annual Review of Phytopathology 54:303–322
Singh P, He X, Sansaloni C, Juliana P, Dreisigacker S, Duveiller E, Kumar U, Joshi A, Singh R (2018) Resistance to spot blotch in two mapping populations of common wheat is controlled by multiple QTL of minor effects. International Journal of Molecular Sciences 19:4054
Sultana S, Adhikary SK, Islam MM, Rahman SMM (2018) Evaluation of pathogenic variability based on leaf blotch disease development components of Bipolaris sorokiniana in Triticum aestivum and agroclimatic origin. Plant Pathology Journal 34:93–103
The authors would like to express their gratitude to Drs. Etienne Duveiller, Monica Mezzalama, Karim Ammar, and Julio Huerta, CIMMYT, for their contribution in the collection of B. sorokiniana isolates. Technical supports from Maria Elena Lemus, Monica Preciado, Javier Segura, and Francisco Lopez are highly acknowledged.
The authors received financial support through the CGIAR Research Program on WHEAT, National Natural Science Foundation of China (31561143004) and Natural Science Foundation of Jiangsu Province, China (BK20170609).
Conflict of interest
The authors declare that they have no conflict of interest.
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
About this article
Cite this article
Wu, L., He, X., Lozano, N. et al. ToxA, a significant virulence factor involved in wheat spot blotch disease, exists in the Mexican population of Bipolaris sorokiniana. Trop. plant pathol. 46, 201–206 (2021). https://doi.org/10.1007/s40858-020-00391-4
- Cochliobolus sativus
- Disease resistance
- Triticum aestivum