Septoria nodorum blotch – disease of wheat and triticale caused by Parastagonospora nodorum fungus
Lidia Kowalska
(Poland)
https://orcid.org/0000-0002-1285-1182
Tomasz Góral
t.goral@ihar.edu.plInstytut Hodowli i Aklimatyzacji Roślin - Państwowy Instytut Badawczy (Poland)
https://orcid.org/0000-0001-9130-6109
Abstract
Parastagonospora nodorum is a necrotrophic fungal pathogen with a narrow host range that causes Septoria nodorum blotch, mainly of wheat and triticale. Although infections caused by P. nodorum are commonly observed in seedlings, they have the greatest effect on the adult plants. The pathogen reduces the assimilation area of green plant organs, thus limiting crop growth and yield, causing losses in 31%-50% yield. Infections caused by P. nodorum can also affect on the ear, resulting in glume blotch, which directly affects grain quality.
Reports of P. nodorum high evolutionary potential and its fungicides resistance , the increasing use of nitrogen and simplified cultivation, combined with changes in climate and agricultural environment, confirm that genetic plants resistance to Septoria nodorum blotch remains a high priority in many wheat and triticale cultivation regions.
This review summarizes current nformation on P. nodorum population structure and its parasitic specialization. Then recent advances in the genetics of host resistance to the pathogen and the necrotrophic protein effectors produced by P. nodorum during infection were reviewed. Finally, the available tools in plant breeding that contribute to the Septoria nodorum blotch reduction were presented.
Keywords:
Septoria nodorum blotch, protein effector, wheat, triticale, resistenceReferences
Abeysekara, N.S., Faris, J.D., Chao, S., McClean, P.E., Friesen, T.L., 2012. Whole-genome QTL analysis of Stagonospora nodorum blotch resistance and validation of the SnTox4–Snn4 interaction in hexaploid wheat. Phytopathology 102(1), 94-104. https://doi.org/10.1094/PHYTO-02-11-0040
Google Scholar
Abeysekara, N.S., Friesen, T.L., Keller, B., Faris, J.D. 2009. Identification and characterization of a novel host-toxin interaction in the wheat-Stagonospora nodorum pathosystem. Theor. Appl. Genet. 120, 117–126. https://doi.org/10.1007/s00122-009-1163-6
Google Scholar
Adhikari, T.B., Jackson, E.W., Gurung, S., Hansen, J.M., Bonman, J.M., 2011. Association mapping of quantitative resistance to Phaeosphaeria nodorum in spring wheat landraces from the USDA National Small Grains Collection. Phytopathology 101(11), 1301-1310. https://doi.org/10.1094/PHYTO-03-11-0076
Google Scholar
Aguilar, V., Stamp, P., Winzeler, M., Winzeler, H., Schachermayr, G., Keller, B., Zanette S., Messmer, M.M., 2005. Inheritance of field resistance to Stagonospora nodorum leaf and glume blotch and correlations with other morphological traits in hexaploid wheat (Triticum aestivum L.) Theor. Appl. Genet. 111, 325-336. https://doi.org/10.1007/s00122-005-2025-5
Google Scholar
Arseniuk, E., 2019. Recent developments in triticale breeding research and production-an overview. Ekin Journal of Crop Breeding and Genetics, 5(2), 68-73.
Google Scholar
Arseniuk, E., 2021. Toksyny białkowe Parastagonospora nodorum i ich związek z patogenicznością oraz odpornością pszenżyta i pszenicy na septoriozę liści i plew (SNB). Biul. IHAR 295, 55–62. https://doi.org/10.37317/biul-2021-00PB
Google Scholar
Arseniuk, E., Czembor, P.C., Czaplicki, A., Song, Q., Cregan, P.B., Hoffman, D.L., Ueng, P.P., 2004. QTL controlling partial resistance to Stagonospora nodorum leaf blotch in winter wheat cultivar Alba. Euphytica 137(2), 225-231. https://doi.org/10.1023/B:EUPH.0000041589.47544.de
Google Scholar
Arseniuk, E., Goral, T., Scharen, A.L., 1998. Seasonal patterns of spore dispersal of Phaeosphaeria spp. And Stagonospora spp. Plant Dis. 82, 187–194. https://doi.org/10.1094/PDIS.1998.82.2.187
Google Scholar
Arseniuk, E., Walczewski, J., 2014. Effect of dihaploid technology on resistance of winter wheat and winter triticale to Stagonospora nodorum blotch. W: Behl R.K., Arseniuk E. (red) Proceedings of the international conference on biotechnology and plant breeding perspectives towards food security and sustainability. IHAR-PIB Radzikow, Poland. Agrobios (International), New Delhi, pp 32-329
Google Scholar
Ballini. E., Tavaud. M., Ducasse. A., Sanchez. D., Paux. E., Kitt. J., Charmet. G., Audigeos. D., Roumet. P., David. J., Morel, J. B., 2020. Genome wide association mapping for resistance to multiple fungal pathogens in a panel issued from a broad composite cross-population of tetraploid wheat Triticum turgidum. Euphytica 216(6), 1-17. https://doi.org/10.1007/s10681-020-02631-9
Google Scholar
Bartosiak, S.F., Arseniuk, E., Szechyńska-Hebda, M., Bartosiak, E., 2021. Monitoring of natural occurrence and severity of leaf and glume blotch diseases of winter wheat and winter triticale incited by necrotrophic fungi Parastagonospora spp. and Zymoseptoria tritici. Agronomy 11, 967. https://doi.org/10.3390/agronomy11050967
Google Scholar
Bathgate, J.A., Loughman, R., 2001. Ascospores are a source of inoculum of Phaeosphaeria nodorum, P. avenaria f. sp. avenaria and Mycosphaerella graminicola in Western Australia. Australas. Plant Pathol. 30, 317–322. https://doi.org/10.1071/AP01043
Google Scholar
Bergstrom, G.C., 2010. Stagonospora nodorum blotch and Stagonospora avenae blotch. Compendium of Wheat Diseases and Pests, 75-77.
Google Scholar
Bhathal, J.S., Loughman, R., Speijers J., 2003. Yield reduction in wheat in relation to leaf disease from yellow (tan) spot and Septoria nodorum blotch. Eur. J. Plant Pathol. 109, 435-443. https://doi.org/10.1023/A:1024277420773
Google Scholar
Blixt, E., Djurle, A., Yuen, J., Olson, Å., 2009. Fungicide sensitivity in Swedish isolates of Phaeosphaeria nodorum. Plant Pathol. 58, 655–664. https://doi.org/10.1111/j.1365-3059.2009.02041.x
Google Scholar
Bostwick, D.E., Ohm, H.W., Samer, G., 1993. Inheritance of Septoria glume blotch resistance in wheat. Crop Sci. 33, 439-443. https://doi.org/10.2135/cropsci1993.0011183X003300030005x
Google Scholar
Breen, S., Williams, S.J., Winterberg, B., Kobe, B., Solomon, P.S., 2016. Wheat PR-1 proteins are targeted by necrotrophic pathogen effector proteins. Plant J. 88, 13–25. https://doi.org/10.1111/tpj.13228
Google Scholar
Brennan, R. M., 1985. Dispersal of Septoria nodorum pycnidiospores by simulated raindrops in still air. J. Phytopath. 112, 281-290. https://doi.org/10.1111/j.1439-0434.1985.tb00805.x
Google Scholar
Brodal, G., 1993. Fungicide treatment of cereal seeds according to need in the Nordic countries. Proceedings Crop Protection in Northern Britain 1993, Dundee University, 23-25 marca 1993.The Association for Crop Protection in Northern Britain, ss. 7-16.
Google Scholar
Chooi, Y.-H., Krill, C., Barrow, R.A., Chen, S., Trengove, R., Oliver, R.P., Solomon, P.S., 2015a. An In planta-expressed polyketide synthase produces (R)-mellein in the wheat pathogen Parastagonospora nodorum. Appl. Environ. Microbiol. 81, 177–186. https://doi.org/10.1128/AEM.02745-14
Google Scholar
Chooi, Y.-H., Muria-Gonzalez, M.J., Mead, O.L., Solomon, P.S., 2015b. SnPKS19 encodes the polyketide synthase for alternariol mycotoxin biosynthesis in the wheat pathogen Parastagonospora nodorum. Appl. Environ. Microbiol. 81, 5309–5317. https://doi.org/10.1128/AEM.00278-15
Google Scholar
Chooi, Y.-H., Muria-Gonzalez, M.J., Solomon, P.S., 2014. A genome-wide survey of the secondary metabolite biosynthesis genes in the wheat pathogen Parastagonospora nodorum. Mycology 5, 192–206. https://doi.org/10.1080/21501203.2014.928386
Google Scholar
Chooi, Y.-H., Zhang, G., Hu, J., Muria-Gonzalez, M.J., Tran, P.N., Pettitt, A., i in., 2017. Functional genomics-guided discovery of a light-activated phytotoxin in the wheat pathogen Parastagonospora nodorum via pathway activation. Environ. Microbiol. 19, 1975–1986. https://doi.org/10.1111/1462-2920.13711
Google Scholar
Cockram, J., Scuderi, A., Barber, T., Furuki, E., Gardner, K.A., Gosman, N., Kowalczyk, R., Phan, H.P., Rose, G.A., Tan, K.-C., Oliver, R.P., Mackay, I.J., 2015. Fine-mapping the wheat Snn1 locus conferring sensitivity to the Parastagonospora nodorum necrotrophic effector SnTox1 using an eight founder multiparent advanced generation inter-cross population. G3: Genes, Genomes, Genetics 5(11), 2257-2266. https://doi.org/10.1534/g3.115.021584
Google Scholar
Cowger, C., Murphy, J.P., 2007. Artificial inoculation of wheat for selecting resistance to Stagonospora nodorum blotch. Plant Dis. 91, 539-545. https://doi.org/10.1094/PDIS-91-5-0539
Google Scholar
Cunfer, B.M., Ueng, P.P., 1999. Taxonomy and identification of Septoria and Stagonospora species on small-grain cereals. Annu. Rev. Phytopathol. 37, 267–284. https://doi.org/10.1146/annurev.phyto.37.1.267
Google Scholar
Czembor, P.C., Arseniuk, E., Czaplicki, A., Song, Q., Cregan, P.B., Ueng, P.P., 2003. QTL mapping of partial resistance in winter wheat to Stagonospora nodorum blotch. Genome 46(4), 546-554. https://doi.org/10.1139/g03-036
Google Scholar
Czembor, P., Arseniuk, E., Radecka-Janusik, M., Piechota, U., Słowacki, P., 2019. Quantitative trait loci analysis of adult plant resistance to Parastagonospora nodorum blotch in winter wheat cv. Liwilla (Triticum aestivum L.) Eur. J. Plant Path. 155, 1001–1016. https://doi.org/10.1007/s10658-019-01829-5
Google Scholar
Downie, R.C., Bouvet, L., Furuki, E., Gosman, N., Gardner, K.A., Mackay, I.J. i in., 2018. Assessing European wheat sensitivities to Parastagonospora nodorum necrotrophic effectors and fine-mapping the Snn3-B1 locus conferring sensitivity to the effector SnTox3. Front. Plant Sci. 9, 881. https://doi.org/10.3389/fpls.2018.00881
Google Scholar
Downie, R.C., Lin, M., Corsi, B., Ficke, A., Lillemo, M., Oliver, R.P., Phan, H.T.T., Tan, K.C., Cockram, J., 2021. Septoria nodorum blotch of wheat: Disease management and resistance breeding in the face of shifting disease dynamics and a changing environment. Phytopathology 111, 906–920. https://doi.org/10.1094/PHYTO-07-20-0280-RVW
Google Scholar
Du, C.G., Nelson, L.R., McDaniel, M.E., 1999. Diallel analysis of gene effects conditioning resistance to Stagonospora nodorum (Berk.) in wheat. Crop Sci. 39, 686–690. https://doi.org/10.2135/cropsci1999.0011183X003900020014x
Google Scholar
Eyal, Z., Scharen, A.L., Prescot, J.M., Van Ginkel, M., 1987. The Septoria diseases of wheat. Concepts and methods of disease management. CIMMYT, Mexico, 52 strony.
Google Scholar
Faris, J.D., Friesen, T.L., 2009. Reevaluation of a tetraploid wheat population indicates that the Tsn1–ToxA interaction is the only factor governing Stagonospora nodorum blotch susceptibility. Phytopathology 99(8), 906-912. https://doi.org/10.1094/PHYTO-99-8-0906
Google Scholar
Faris, J.D., Zhang, Z., Lu, H., Lu, S., Reddy, L., Cloutier, S., Fellers, J.P., Meinhardt, S.W., Rasmussen, J.B., Xu, S.S., Oliver, R.P., Simons, K.J., Friesen, T.L., 2010. A unique wheat disease resistance-like gene governs effector-triggered susceptibility to necrotrophic pathogens. Proc. Natl. Acad. Sci. 107, 13544–13549. https://doi.org/10.1073/pnas.1004090107
Google Scholar
Ficke. A., Cowger. C., Bergstrom. G., Brodal. G., 2018. Understanding yield loss and pathogen biology to improve disease management: Septoria nodorum blotch – A case study in wheat. Plant Dis. 102, 696–707. https://doi.org/10.1094/PDIS-09-17-1375-FE
Google Scholar
Flor. H.H., 1956. The complementary genic system in flax and flax rust. Adv. Genet. 8, 29- 54.
Google Scholar
Francki. M.G., Shankar. M., Walker. E., Loughman. R., Golzar. H., Ohm. H., 2011. New quantitative trait loci in wheat for flag leaf resistance to Stagonospora nodorum blotch. Phytopathology 101(11), 1278-1284. https://doi.org/10.1094/PHYTO-02-11-0054
Google Scholar
Francki. M.G., Walker. E., McMullan. C.J., Morris. W.G., 2020. Multilocation evaluation of global wheat lines reveal multiple QTL for adult plant resistance to Septoria nodorum blotch (SNB) detected in specific environments and in response to different isolates. Front. Plant Sci. 11, 771. https://doi.org/10.3389/fpls.2020.00771
Google Scholar
Frecha. J.H., 1973. The inheritance of resistance to Septoria nodorum in wheat. Boletin Genetico 8, 29–30.
Google Scholar
Fried. P.M., Meister. E., 1987. Inheritance of leaf and head resistance of winter wheat to Septoria nodorum in a diallel cross. Phytopathology 77, 1371-1375.
Google Scholar
Friesen. T.L., Faris. J.D., 2012. Characterization of plant-fungal interactions involving necrotrophic effector-producing plant pathogens. Methods Mol. Biol. 835, 191–207. https://doi.org/10.1007/978-1-61779-501-5_12
Google Scholar
Friesen. T.L., Chu. C.G., Liu. Z.H., Xu. S.S., Halley. S., Faris. J.D., 2009. Host-selective toxins produced by Stagonospora nodorum confer disease susceptibility in adult wheat plants under field conditions. Theor. Appl. Genet. 118, 1489-1497. https://doi.org/10.1007/s00122-009-0997-2
Google Scholar
Friesen. T.L., Chu. C., Xu. S.S., Faris. J.D., 2012. SnTox5-Snn5: A novel Stagonospora nodorum effector-wheat gene interaction and its relationship with the SnToxA-Tsn1 and SnTox3-Snn3-B1 interactions. Mol. Plant Pathol. 13, 1101–1109. https://doi.org/10.1111/j.1364-3703.2012.00819.x
Google Scholar
Gao, Y., Faris, J.D., Liu, Z., Kim, Y.M., Syme, R.A., Oliver, R.P., i in., 2015. Identification and characterization of the SnTox6-Snn6 interaction in the Parastagonospora nodorum-wheat pathosystem. Mol. Plant-Microbe Interact. 28, 615–625. https://doi.org/10.1094/MPMI-12-14-0396-R
Google Scholar
Ghaderi, F., Sharifnabi, B., Javan-Nikkhah, M., Brunner, P.C., McDonald, B.A. 2020. SnToxA, SnTox1, and SnTox3 originated in Parastagonospora nodorum in the Fertile Crescent. Plant Pathol 69, 1482–1491. https://doi.org/10.1111/ppa.13233
Google Scholar
Gupta, P.K., Vasistha, N.K., Singh, S., Joshi, A.K. 2023. Genetics and breeding for resistance against four leaf spot diseases in wheat (Triticum aestivum L.). Front. Plant Sci. 14:1023824. https://doi.org/10.3389/fpls.2023.1023824
Google Scholar
Hafez, M., Gourlie, R., Despins, T., Turkington, T.K., Friesen, T.L., Aboukhaddour, R., 2020. Parastagonospora nodorum and related species in western Canada: genetic variability and effector genes. Phytopathology 110, 1946–1958. https://doi.org/10.1094/PHYTO-05-20-0207-R
Google Scholar
Halama, P., Lacoste, L., 1991. Déterminisme de la reproduction sexuée de Phaeosphaeria (Leptosphaeria) nodorum, agent de la septoriose du blé. I. Hétérothallisme et rôle des microspores. Can. J. Bot. 69, 95-99. https://doi.org/10.1139/b91-013
Google Scholar
Halder, J., Zhang, J., Ali, S., Sidhu, J.S., Gill, H.S., Talukder, S.K., Kleinjan, J., Turnipseed, B., Sehgal, S.K. 2019. Mining and genomic characterization of resistance to tan spot, Stagonospora nodorum blotch (SNB), and Fusarium head blight in Watkins core collection of wheat landraces. BMC Plant Biol. 19(1), 1-15. https://doi.org/10.1186/s12870-019-2093-3
Google Scholar
Hane, J.K., Paxman, J., Jones, D.A.B., Oliver, R.P., de Wit, P. 2020. “CATAStrophy,” a genom informed trophic classification of filamentous plant pathogens – how many different types of filamentous plant pathogens are there? Front Microbiol, 10, 3088. https://doi.org/10.3389/fmicb.2019.03088
Google Scholar
Hetman, A., Kowalczyk, S. 2018. Membrane receptors recognizing MAMP/PAMP and DAMP molecules that activate first line of defence in plant immune system (In Polish with English Abstract: Receptory błonowe wiążące cząsteczki typu MAMP/PAMP i DAMP aktywujące pierwszą linię obrony lokalnej układu odpornościowego roślin). Post Bioch, 64, 29-45.
Google Scholar
Hu. W., He. X., Dreisigacker. S., Sansaloni. C.P., Juliana. P., Singh. P.K., 2019. A wheat chromosome 5AL region confers seedling resistance to both tan spot and Septoria nodorum blotch in two mapping populations. Crop J. 7(6), 809-818. https://doi.org/10.1016/j.cj.2019.05.004
Google Scholar
John, E.; Lopez-Ruiz, F.; Rybak, K.; Mousley, C.J.; Oliver, R.P.; Tan, K.-C. 2016. Dissecting the role of histidine kinase and HOG1 mitogen-activated protein kinase signalling in stress tolerance and pathogenicity of Parastagonospora nodorum on wheat. Microbiology 162, 1023-1036, https://doi.org/10.1099/mic.0.000280
Google Scholar
Jørgensen, L.N., Clark, B., Marga, J., Antichi, G.D., Góral, T., Schepers, P.H., Lucas, P., Rolland, B., Gouache, D., Hornok, L. 2008., Using Cultivar Resistance to Reduce Fungicide Input in Wheat. ENDURE Wheat Case Study – Guide Number 1. [dostęp na stronie: http://www.endure-network.eu/endure_publications/endure_publications2].
Google Scholar
Kariyawasam, G.K., Richards, J.K., Wyatt, N.A., Running, K.L., Xu, S.S., Liu, Z., Borowicz, P., Faris, J.D., Friesen, T.L., 2022. The Parastagonospora nodorum necrotrophic effector SnTox5 targets the wheat gene Snn5 and facilitates entry into the leaf mesophyll. New Phytol. 233(1), 409-426. https://doi.org/10.1111/nph.17602
Google Scholar
Karjalainen, R., Lounatmaa, K., 1986. Ultrastructure of penetration and colonization of wheat leaves by Septoria nodorum. Physiol. Mol. Plant Pathol. 29, 263-270. https://doi.org/10.1016/S0048-4059(86)80026-1
Google Scholar
Katoch, S., Sharma, V., Sharma, D., Salwan, R., Rana, S.K., 2022. Biology and molecular interactions of Parastagonospora nodorum blotch of wheat. Planta, 255(1), 1-18. https://doi.org/10.1007/s00425-021-03796-w
Google Scholar
Kesselmeier, J., Staudt, M., 1999. Biogenic volatile organic compounds (VOC): an overview on emission, physiology and ecology. J. Atmos. Chem. 33, 23–88. https://doi.org/10.1023/A:1006127516791
Google Scholar
Korbas, M., Horoszkiewcz-Janka, J., Jajor, E., Głazek, M., 2011. Integrowana metoda ograniczenia sprawców chorób. W: Metodyka integrowanej ochrony pszenżyta ozimego i jarego. IOR — PIB Poznań: 111 — 159.
Google Scholar
Kourelis, J, van der Hoorn, R.A.L., 2018. Defended to the nines: 25 years of resistance gene cloning identifies nine mechanism for R protein function. Plant Cell 30, 285-299. https://doi.org/10.1105/tpc.17.00579
Google Scholar
Kryczyński, S., 2002. Podstawy fitopatologii. Fundacja Rozwój SGGW. Warszawa. Wyd. II.
Google Scholar
Kuleung, C., Baenziger, P.S., Dweikat, I., 2004. Transferability of SSR markers among wheat, rye, and triticale. Theor. Appl. Genet. 108, 1147–- 1150. https://doi.org/10.1007/s00122-003-1532-5
Google Scholar
Lenz, H.D., Haller, E., Melzer, E., Kober, K., Wurster, K., Stahl, M., Bassham, D.C., Vierstra, R.D., Parker, J.E., Bautor, J., Molina, A., Escudero, V., Shindo, T., van der Hoorn, R.A.L., Gust, A.A., Nürnberger, T., 2011. Autophagy differentially controls plant basal immunity to biotrophic and necrotrophic pathogens. Plant. J. 66, 818–830. https://doi.org/10.1111/j.1365-313X.2011.04546.x
Google Scholar
Lema-Rumińska, J., Kulus, D., 2012. Induction of somatic embryogenesis in Astrophytum asterias (Zucc.) Lem. In the aspect of light conditions and auxin 2,4-D concentrations. Acta Sci. Pol. – Hort. Cult. 11(4), 77-87.
Google Scholar
Li, H., Hu, J., Wei, H., Solomon, P.S., Vuong, D., Lacey, E., i in., 2018. Chemical ecogenomics-guided discovery of phytotoxic α-pyrones from the fungal wheat pathogen Parastagonospora nodorum. Org. Lett. 20, 6148–6152. https://doi.org/10.1021/acs.orglett.8b02617
Google Scholar
Lillemo, M., Dieseth, J. A., 2011. Wheat breeding in Norway. W: Angus W., Bonjean A.P., van Ginkel M. (red), The World Wheat Book: A history of wheat breeding, 2, ss. 45-79.
Google Scholar
Lin, M., Corsi, B., Ficke, A., Tan, K.C., Cockram, J., Lillemo, M., 2020a. Genetic mapping using a wheat multi-founder population reveals a locus on chromosome 2A controlling resistance to both leaf and glume blotch caused by the necrotrophic fungal pathogen Parastagonospora nodorum. Theor. Appl. Genet. 133(3), 785–808. https://doi.org/10.1007/s00122-019-03507-w
Google Scholar
Lin, M., Ficke, A., Cockram, J., Lillemo, M., 2020b. Genetic Structure of the Norwegian Parastagonospora nodorum Population. Front. Microbiol. 11, 1280. https://doi.org/10.3389/fmicb.2020.01280
Google Scholar
Lin, M., Stadlmeier, M., Mohler, V., Tan, K.C., Ficke, A., Cockram, J., Lillemo, M., 2021. Identification and cross-validation of genetic loci conferring resistance to Septoria nodorum blotch using a German multi-founder winter wheat population. Theor. Appl. Genet. 134(1), 125-142. https://doi.org/10.1007/s00122-020-03686-x
Google Scholar
Liu, Z., El-Basyoni, I., Kariyawasam, G., Zhang, G., Fritz, A., Hansen, J., Marais, F., Friskop, A., Chao, S., Akhunov, E., Baenziger, P.S., 2015. Evaluation and association mapping of resistance to tan spot and Stagonospora nodorum blotch in adapted winter wheat germplasm. Plant Dis. 99(10), 1333-1341. https://doi.org/10.1094/PDIS-11-14-1131-RE
Google Scholar
Liu, Z., Faris, J.D., Oliver, R.P., Tan, K.-C., Solomon, P.S., McDonald, M.C., McDonald, B.A., Nunez, A., Lu, S., Rasmussen, J.B., Friesen, T.L., 2009. SnTox3 acts in effector triggered susceptibility to induce disease on wheat carrying the Snn3 gene. PloS Pathog. 5 (9), e1000581. https://doi.org/10.1371/journal.ppat.1000581
Google Scholar
Liu Z., Gao Y., Kim Y.M., Faris J.D., Shelver W.L., de Wit P.J., Xu S.S., Friesen T.L. 2016. SnTox1, a Parastagonospora nodorum necrotrophic effector, is a dual-function protein that facilitates infection while protecting from wheat-produced chitinases. New Phytol. 211(3), 1052-64. https://doi.org/10.1111/nph.13959
Google Scholar
Liu Z., Zhang Z., Faris J.D., Oliver R.P., Syme R., McDonald M.C., McDonald B.A., Solomon P.S., Lu S., Shelver W.L. 2012. The cysteine rich necrotrophic effector SnTox1 produced by Stagonospora nodorum triggers susceptibility of wheat lines harboring Snn1. PloS Pathog. 8: e1002467. https://doi.org/10.1371/journal.ppat.1002467
Google Scholar
Loughman R., Wilson R.E., Goss I.M., Foster D.T. Murphy N.E.A. 1999. Varieties and advances lines resistant to Septoria diseases of wheat in Western Australia. W: van Ginkel M., McNab A., Krupinsky J. (red.) Septoria and Stagonospora Diseases of Cereals: A Compilation of Global Research. Mexico, D.F.: CIMMYT, pp. 145–147.
Google Scholar
Lu S., Faris J.D., Sherwood R., Friesen T.L., Edwards, M.C. 2014. A dimeric PR-1-type pathogenesis-related protein interacts with ToxA and potentially mediates ToxA-induced necrosis in sensitive wheat. Mol. Plant Pathol. 15, 650–663. https://doi.org/10.1111/mpp.12122
Google Scholar
Lu Q., Lillemo M. 2014. Molecular mapping of adult plant resistance to Parastagonospora nodorum leaf blotch in bread wheat lines ‘Shanghai-3/Catbird’and ‘Naxos’. Theor. App. Genet. 127(12), 2635-2644. https://doi.org/10.1007/s00122-014-2404-x
Google Scholar
Luke H.H., Barnett R.D., Pfahler P.L. 1986. Development of Septoria nodorum blotch on wheat from infected and treated seed. Plant Dis. 70, 252-254. https://doi.org/10.1094/PD-70-252
Google Scholar
McDonald, M.C., Razavi, M., Friesen, T.L., Brunner, P.C., McDonald, B.A., 2012. Phylogenetic and population genetic analyses of Phaeosphaeria nodorum and its close relatives indicate cryptic species and an origin in the Fertile Crescent. Fungal Genet. Biol. 49, 882–895. https://doi.org/10.1016/J.FGB.2012.08.001
Google Scholar
McDonald M.C., Oliver R.P., Friesen T.L., Brunner P.C., McDonald B.A. 2013. Global diversity and distribution of three necrotrophic effectors in Phaeosphaeria nodorum and related species. New Phytol. 199, 241–251. https://doi.org/10.1111/nph.12257
Google Scholar
McDonald B.A., Stukenbrock E.H. 2016. Rapid emergence of pathogens in agroecosystems: global threats to agricultural sustainability and food security. Philos. Trans. R. Soc. Lond. B 371(1709), 20160026. https://doi.org/10.1098/rstb.2016.0026
Google Scholar
Mehra L., Adhikari U., Cowger C., Ojiambo P.S. 2018. Septoria nodorum blotch of wheat. PeerJ Preprints 6, e27039v2. https://doi.org/10.7287/peerj.preprints.27039v2
Google Scholar
Mehra L.K., Cowger C., Gross K., Ojiambo P.S. 2016. Predicting pre-planting risk of Stagonospora nodorum blotch in winter wheat using machine learning models. Front. Plant Sci. 7, 390. https://doi.org/10.3389/fpls.2016.00390
Google Scholar
Mehra L.K., Cowger C., Weisz R., Ojiambo P.S. 2015. Quantifying the effects of wheat residue on severity of Stagonospora nodorum blotch and yield in winter wheat. Phytopathology 105(11):1417–1426. https://doi.org/10.1094/PHYTO-03-15-0080-R
Google Scholar
Muria-Gonzalez M.J., Chooi Y.-H., Breen S., Solomon P.S. 2015. The past, present and future of secondary metabolite research in the Dothideomycetes. Mol. Plant Pathol. 16, 92–107. https://doi.org/10.1111/mpp.12162
Google Scholar
Muria-Gonzalez M.J., Yeng Y., Breen S., Mead O., Wang C., Chooi Y.-H., Barrow R.A., Solomon P.S. 2020. Volatile Molecules Secreted by the Wheat Pathogen Parastagonospora nodorum Are Involved in Development and Phytotoxicity. Front. Microbiol. 11, 466. https://doi.org/10.3389/fmicb.2020.00466
Google Scholar
Nelson L.R., Gates C.E. 1982. Genetics of host plant resistance of wheat to Septoria nodorum. Crop Sci. 22:771-773. https://doi.org/10.2135/cropsci1982.0011183X002200040017x
Google Scholar
Nelson L.R., Holmes M.R., Cunfer B.M. 1976. Multiple regression accounting for wheat yield reduction by Septoria nodorum and other pathogens. Phytopathology 66, 1375-1379.
Google Scholar
Oleksiak, T. 2013. Stosowanie kwalifikowanego materiału siewnego a plonowanie zbóż ozimych. Biul. IHAR 268, 87-99. https://doi.org/10.37317/biul-2013-0035
Google Scholar
Oliver R.P., Friesen T.L., Faris J.D., Solomon P.S. 2012. Stagonospora nodorum: from pathology to genomics and host resistance. Annual Review of Phytopathology 50, 23-43. https://doi.org/10.1146/annurev-phyto-081211-173019
Google Scholar
Oliver R.P., Lichtenzveig J., Tan K.C., Waters O., Rybak K., Lawrence J., Friesen T., Burgess P. 2014. Absence of detectable yield penalty associated with insensitivity to Pleosporales necrotrophic effectors in wheat grown in the West Australian wheat belt. Plant Pathol. 63, 1027–1032. https://doi.org/10.1111/ppa.12191
Google Scholar
Pereira D.A., McDonald B.A., Brunner P.C. 2017. Mutations in the CYP51 gene reduce DMI sensitivity in Parastagonospora nodorum populations in Europe and China. Pest Manag. Sci. 73, 1503–1510. https://doi.org/10.1002/ps.4486
Google Scholar
Peever T.L., Brants A., Bergstrom G.C., Milgroom M.G. 1994. Selection for decreased sensitivity to propiconazole in experimental field populations of Stagonospora nodorum (syn. Septoria nodorum). Canadian Journal of Plant Pathology 16, 109–17. https://doi.org/10.1080/07060669409500767
Google Scholar
Peters Haugrud A.R., Zhang Z., Friesen T.L., Faris J.D. 2022. Genetics of resistance to tagonosa nodorum blotch in wheat. Theoretical and Applied Genetics 135, 3685-3707. https://doi.org/10.1007/s00122-022-04036-9
Google Scholar
Phan H.T., Rybak K., Bertazzoni S., Furuki E., Dinglasan E., Hickey L.T., Oliver R.P., Tan, K.C. 2018. Novel sources of resistance to Septoria nodorum blotch in the Vavilov wheat collection identified by genome-wide association studies. Theoretical and Applied Genetics, 131(6), 1223-1238. https://doi.org/10.1007/s00122-018-3073-y
Google Scholar
Phan H.T., Rybak K., Furuki E., Breen S., Solomon P.S., Oliver R.P., I in. 2016. Differential effector gene expression underpins epistasis in a plant fungal disease. The Plant Journal. 87, 343–54. https://doi.org/10.1111/tpj.13203
Google Scholar
Poland J.A., Balint-Kurti P.J., Wisser R.J., Pratt R.C., Nelson R.J. 2009. Shades of gray: the world of quantitative disease resistance. Trends in plant science, 14(1), 21-29. https://doi.org/10.1016/j.tplants.2008.10.006
Google Scholar
Quaedvlieg, W., Verkley, G.J.M., Shin, H.D., Barreto, R.W., Alfenas, A.C., Swart, W.J., Groenewald, J.Z., Crous, P.W., 2013. Sizing up Septoria. Stud. Mycol. 75, 307–390. https://doi.org/10.3114/SIM0017
Google Scholar
Reddy L., Friesen T.L., Meinhardt S.W., Chao S., Faris J.D. 2008. Genomic analysis of the Snn1 locus on wheat chromosome arm 1bs and the identification of candidate genes. Plant Genome 1, 55–66. https://doi.org/10.3835/plantgenome2008.03.0181
Google Scholar
Reszka E., Song Q., Arseniuk E., Cregan P.B., Ueng P.P. 2007. The QTL controlling partial resistance to Stagonospora nodorum blotch disease in winter triticale Bogo. Plant Pathology Bulletin, 16(3), 161-167.
Google Scholar
Richards J.K., Kariyawasam G., Seneviratne S., Wyatt N.A., Xu S.S., Liu Z., i in. 2021. A triple threat: the Parastagonospora nodorum SnTox267 effector exploits three distinct host genetic factors to cause disease in wheat. New Phytol. 233(1), 427-442. https://doi.org/10.1111/nph.17601
Google Scholar
Richards J.K., Stukenbrock E.H., Carpenter J., Liu Z., Cowger C. i. in. 2019. Local adaptation drives the diversification of effectors in the fungal wheat pathogen Parastagonospora nodorum in the United States. PloS Genet. 15(10):e1008223. https://doi.org/10.1371/journal.pgen.1008223
Google Scholar
Rosielle A.A., Brown A.G.P. 1980. Selection for resistance to Septoria nodorum in wheat. Euphytica, 29, 337–346. https://doi.org/10.1007/BF00025132
Google Scholar
Ruud A.K., Dieseth J.A., Ficke A., Furuki E., Phan H.T.T., Oliver R.P., Tan K.C. 2019. Genome-wide association mapping of resistance to Septoria nodorum leaf blotch in a Nordic spring wheat collection. The Plant Genome 12, 3. https://doi.org/10.3835/plantgenome2018.12.0105
Google Scholar
Ruud A.K., Dieseth J.A., Lillemo M. 2018. Effects of three Parastagonospora nodorum necrotrophic effectors on spring wheat under Norwegian field conditions. Crop Sci. 58, 159–168. https://doi.org/10.2135/cropsci2017.05.0281
Google Scholar
Ruud A.K., Lillemo M. 2018. Diseases affecting wheat: Septoria nodorum blotch. In: Integrated disease management of wheat and barley. Oliver, R. (Ed.). Burleigh Dodds Science Publishing, Cambridge, UK, 109–144. https://doi.org/10.1201/9780429201219
Google Scholar
Ruud, A.K., Windju, S., Belova, T., Friesen, T.L., Lillemo M., 2017. Mapping of SnTox3–Snn3 as a major determinant of field susceptibility to Septoria nodorum leaf blotch in the SHA3/CBRD × Naxos population. Theor. Appl. Genet. 130, 1361-1374. https://doi.org/10.1007/s00122-017-2893-5
Google Scholar
Shah D.A., Bergstrom G.C. 2000. Temperature dependent seed transmission of Stagonospora nodorum in wheat. Eur. J. Plant Pathol. 106, 837-842. https://doi.org/10.1023/A:1008723823196
Google Scholar
Shah D.A., Bergstrom G.C., Ueng, P.P. 1995. Initiation of Septoria nodorum blotch epidemics in winter wheat by seedborne Stagonospora nodorum. Phytopathology 85, 452-457. https://doi.org/10.1094/Phyto-85-452
Google Scholar
Shankar M., Reeves K., Bradley J., Varischetti R., Loughman R. 2021. Effect of varietal resistance on the yield loss function of wheat to nodorum blotch. Plant Pathol 70, 745–759. https://doi.org/10.1111/ppa.13317
Google Scholar
Shankar M., Walker E., Golzar H., Loughman R., Wilson R.E., Francki M.G. 2008. Quantitative trait loci for seedling and adult plant resistance to Stagonospora nodorum in wheat. Phytopathology 98(8), 886–893. https://doi.org/10.1094/PHYTO-98-8-0886
Google Scholar
Sharma J. S., Running K. L., Xu S. S., Zhang Q., Peters Haugrud A. R., Sharma S., McClean P.E., Faris, J. D. 2019., Genetic analysis of threshability and other spike traits in the evolution of cultivated emmer to fully domesticated durum wheat. Molec. Genet. Genomics 294(3), 757-771. https://doi.org/10.1007/s00438-019-01544-0
Google Scholar
Shi G., Friesen T.L., Saini J., Xu S.S., Rasmussen J.B., Faris J.D. 2015. The Wheat Snn7 Gene Confers Susceptibility on Recognition of the Parastagonospora nodorum Necrotrophic Effector SnTox7. Plant Genome 8 plantgenome2015.02.0007. https://doi.org/10.3835/plantgenome2015.02.0007
Google Scholar
Shi G., Zhang Z., Friesen T.L., Bansal U., Cloutier S., Wicker T., Rasmussen J.B., Faris J.D. 2016a. Marker development, saturation mapping, and high-resolution mapping of the Septoria nodorum blotch susceptibility gene Snn3-B1 in wheat. Molec. Genet. Genomics 291(1), 107-119. https://doi.org/10.1007/s00438-015-1091-x
Google Scholar
Shi G., Zhang Z., Friesen T.L., Raats D., Fahima T., Brueggeman, R.S., Lu S., Trick H.N., Liu Z., Chao W.s 2016b. The hijacking of a receptor kinase-driven pathway by a wheat fungal pathogen leads to disease. Sci. Adv. 2, e1600822. https://doi.org/10.1126/sciadv.1600822
Google Scholar
Singh B., Mehta S., Aggarwal S.K., Tiwari M., Bhuyan S.I., Bhatia S., Islam M.A.s 2019. Barley, disease resistance and molecular breeding approaches. W: Wani S.H. (red.) Disease resistance in crop plants. Springer Nature, Switzerland. ss. 261-299.
Google Scholar
Solomon P.S., Lowe R.G.T., Tan K.C., Waters O.D.C., Oliver R.P., 2006. Stagonospora nodorum: cause of Stagonospora nodorum blotch of wheat. Molec, Plant Pathol, 7 (3), 147-156. https://doi.org/10.1111/j.1364-3703.2006.00326.x
Google Scholar
Sommerhalder, R.J., McDonald, B.A., Mascher, F., Zhan, J., 2010. Sexual recombinants make a significant contribution to epidemics caused by the wheat pathogen Phaeosphaeria nodorum.
Google Scholar
https://doi.org/10.1094/PHYTO-100-9-0855
Google Scholar
Śnieżko R., 1991. Pylniki i pyłek w hodowli in vitro. Wiadomości Botaniczne, 35(1).
Google Scholar
Tan K.-C., Oliver R.P., 2017. Regulation of proteinaceous effector expression in phytopathogenic fungi. PloS Pathog. 13(4), e1006241. https://doi.org/10.1371/journal.ppat.1006241
Google Scholar
Tan K.-C., Phan,H.T.T., Rybak K., John E., Chooi Y.H., Solomon P.S., i in., 2015. Functional redundancy of necrotrophic effectors – consequences for exploitation for breeding. Front. Plant Sci. 6, 501. https://doi.org/10.3389/fpls.2015.00501
Google Scholar
Tan K.-C., Waters O., Rybak K., Antoni E., Furuki E., Oliver R., 2014. Sensitivity to three Parastagonospora nodorum necrotrophic effectors in current Australian wheat cultivars and the presence of further fungal effectors. Crop Pasture Sci. 65 (2), 150-158. https://doi.org/10.1071/CP13443
Google Scholar
Tanaka S. 1933. Studies on black spot disease of the Japanese pear (Pirus serotine Rehd.). Memoirs of the College of Agriculture, Kyoto Imperial University 28, 1-31.
Google Scholar
Tratwal A., Strażyński P., Mrówczyński M., 2017. Poradnik Sygnalizatora Ochrony Zbóż; Instytut Ochrony Roślin—PIB: Poznań, Polska.
Google Scholar
Vleeshouwers V.G.A.A., Oliver R.P., 2014. Effectors as tools in disease resistance breeding against Biotrophic, hemibiotrophic and necrotrophic plant pathogens. Mol. Plant-Microbe Interact. 27, 196–206. https://doi.org/10.1094/MPMI-10-13-0313-IA
Google Scholar
Vereet J.A., Hoffman G.M., 1990. A biologically oriented threshold decision model for control of epidemics of Septoria nodorum in wheat. Plant Dis. 74, 731-738. https://doi.org/10.1094/PD-74-0731
Google Scholar
Veselova S.V., Nuzhnaya T.V., Burkhanova G.F., Rumyantsev S.D., Khusnutdinova E.K., Maksimov I.V. 2021. Ethylene-cytokinin interaction determines early defense response of wheat against Stagonospora nodorum Berk. Biomolecules 11(2), 174. https://doi.org/10.3390/biom11020174
Google Scholar
Walczewski J., 2020. Prosta metoda selekcji materiałów hodowlanych pszenicy i pszenżyta z wykorzystaniem nieoczyszczonego filtratu zawierającego efektor Tox3. Biul. Inst. Hod. i Aklim. Roślin 290, 9-14. https://doi.org/10.37317/biul-2020-0012
Google Scholar
Wang, Z.; Ma, Y.; Chen, M.; Da, L.; Su, Z.; Zhang, Z.; Liu, X. 2023. Comparative genomics analysis of WAK/WAKL family in Rosaceae identify candidate WAKs involved in the resistance to Botrytis cinerea. BMC Genomics 24, https://doi.org/10.1186/s12864-023-09371-9.
Google Scholar
Waters O.D.C., Lichtenzveig J., Rybak K., Friesen T.L., Oliver R.P., 2011. Prevalence and importance of sensitivity to the Stagonospora nodorum necrotrophic effector SnTox3 in current Western Australian wheat cultivars. Crop Pasture Sci. 62, 556-562. https://doi.org/10.1071/CP11004
Google Scholar
Wicki W., Winzeler M., Schmid J.E., Stamp P., Messmer M. 1999. Inheritance of resistance to leaf and glume blotch caused By Septoria nodorum Berk. in winter wheat. Theor. Appl. Genet. 99, 1265-1272. https://doi.org/10.1007/s001220051332
Google Scholar
Wiese M.V. 1978. Compendium of wheat diseases. Soil Science 126(3), 190.
Google Scholar
Winterberg B., Du Fall L.A., Song X., Pascovici D., Care N., Molloy M., Ohms S., Solomon P.S. 2014. The necrotrophic effector protein SnTox3 re-programs metabolism and elicits a strong defence response in susceptible wheat leaves. BMC Plant Biol. 14, 215. https://doi.org/10.1186/s12870-014-0215-5
Google Scholar
Wolpert T.J., Dunkle L.D., Ciuffetti L.M. 2002. Host-selective toxins and avirulence determinants: what's in a name? Annu. Rev. Phytopathol. 40(1), 251-285. https://doi.org/10.1146/annurev.phyto.40.011402.114210
Google Scholar
Woś H., Strzembicka A. 2011. Znaczenie hodowli odpornościowej w integrowanej ochronie pszenżyta. W: Metodyka integrowanej ochrony pszenżyta ozimego i jarego. IOR — PIB Poznań: 27 — 49.
Google Scholar
Zhang Z., Friesen T.L., Simons K.J., Xu S.S., Fari, J.D. 2009. Development, identification, and validation of markers for marker-assisted selection against the Stagonospora nodorum toxin sensitivity genes Tsn1 and Snn2 in wheat. Mol. Breeding 23(1), 35-49. https://doi.org/10.1007/s11032-008-9211-5
Google Scholar
Zhang Z., Friesen T.L., Xu S.S., Shi G., Liu Z., Rasmussen J.B., Faris J.D. 2011. Two putatively homoeologous wheat genes mediate recognition of SnTox3 to confer effector-triggered susceptibility to Stagonospora nodorum. Plant J. 65, 27–38. https://doi.org/10.1111/j.1365-313X.2010.04407.x
Google Scholar
Zhang Y., Nan Z. 2018. First report of leaf blotch caused by Parastagonospora nodorum on Leymus chinensis (Chinese Rye Grass) in China. Plant Dis. 102.12, 2661. https://doi.org/10.1094/PDIS-06-18-0926-PDN
Google Scholar
Zhang Z., Running K.L., Seneviratne S., Peters Haugrud A. R., Szabo‐Hever A., Shi G., Brueggeman R., Xu S.S., Friesen T.L., Faris J. D. 2021. A protein kinase–major sperm protein gene hijacked by a necrotrophic fungal pathogen triggers disease susceptibility in wheat. Plant J. 106(3), 720-732. https://doi.org/10.1111/tpj.15194
Google Scholar
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Tomasz Góralt.goral@ihar.edu.pl
Instytut Hodowli i Aklimatyzacji Roślin - Państwowy Instytut Badawczy Poland
https://orcid.org/0000-0001-9130-6109
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