Expression of the ToxA and PtrPF2 genes of the phytopathogenic fungus Pyrenophora tritici-repentis at the beginning of the infection process

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Abstract


Background. Pyrenophora tritici-repentis causing a tan spot of wheat produces host-specific toxins.

Materials and methods. Two P. tritici-repentis isolates with different ability to cause necrosis on the leaves of wheat cultivar Glenlea (nec+ and nec) and with different expression level of ToxA and PtrPf2 (factor transcription gene) in vitro were used for analysis. ToxA gene expression in P. tritici-repentis isolates in planta was characterized using quantitative PCR.

Results. The expression of the ToxA gene in P. tritici-repentis ToxA+ isolates significantly increased when infected the wheat leaves compared to ToxA expression results obtained in vitro. The levels of ToxA expression in both isolates differed significantly after 24, 48 and 96 h after inoculation, however, the dynamics of the trait change over time were similar. However, the highest ToxA expression in the virulent (nec+) isolate in contrast with the avirulent (nec) isolate was observed at a point of 48 h. Whereas the expression of regulating transcription factor PtrPf2 in planta differed imperceptibly from expression in vitro throughout the observation period.

Conclusion. Obviously, the role of the fungal transcription factor in regulating the effector gene expression weakens in planta, and other mechanisms regulating the expression of pathogen genes at the biotrophic stage of the disease develop.


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About the authors

Nina V. Mironenko

All-Russian Institute for Plant Protection

Author for correspondence.
Email: nina2601mir@mail.ru
SPIN-code: 2047-7349

Russian Federation, Pushkin, Saint Petersburg

Doctor of Science, Leading Researcher, Laboratory of Plant Resistance to Diseases

Aleksandra S. Orina

All-Russian Institute for Plant Protection

Email: orina-alex@yandex.ru
SPIN-code: 8590-0092

Russian Federation, Pushkin, Saint Petersburg

PhD, Researcher, Laboratory of Mycology and Phytopathology

Nadezhda M. Kovalenko

All-Russian Institute for Plant Protection

Email: nadyakov@mail.ru
SPIN-code: 9610-4614

Russian Federation, Pushkin, Saint Petersburg

PhD, Senior Researcher, Laboratory of Plant Resistance to Diseases

References

  1. Ciuffetti LM, Tuori RP, Gaventa JM. A single gene encodes a selective toxin causal to the development of tan spot of wheat. Plant Cell. 1997;9(2):135-144. https://doi.org/10.1105/tpc.9.2.135.
  2. Martinez JP, Ottum SA, Ali S, et al. Characterization of the ToxB gene from Pyrenophora tritici-repentis. Mol Plant Microbe Interact. 2001;14(5):675-677. https://doi.org/10.1094/MPMI.2001.14.5.675.
  3. Lamari L, Gilbert J, Tekauz A. Race differentiation in Pyrenophora tritici-repentis and survey of physiologic variation in western Canada. Can J Plant Pathol. 1998;20(4):396-400. https://doi.org/10.1080/07060669809500410.
  4. Lamari L, Strelkov SE, Yahyaoui A, et al. The identification of two new races of Pyrenophora tritici-repentis from the host center of diversity confirms a one-to-one relationship in tan spot of wheat. Phytopathology. 2003;93(4):391-396. https://doi.org/10.1094/PHYTO.2003.93.4.391.
  5. Andrie RM, Pandelova I, Ciuffetti LM. A combination of phenotypic and genotypic characterization strengthens Pyrenophora tritici-repentis race identification. Phytopathology. 2007;97(6):694-701. https://doi.org/10.1094/PHYTO-97-6-0694.
  6. Мироненко Н.В., Баранова О.А., Коваленко Н.М., Михайлова Л.А. Частота гена ToxA в популяциях Pyrenophora tritici-repentis на Северном Кавказе и северо-западе России // Микология и фитопатология. – 2015. – Т. 49. – № 5. – С. 325–329. [Mironenko NV, Baranova OA, Kovalenko NM, Mikhailova LA. Frequency of ToxA gene in North Caucasian and North-West Russian populations of Pyrenophora tritici-repentis. Mikologiya i fitopatologiya. 2015;49(5):325-329. (In Russ.)]
  7. Moreno MV, Stenglein S, Perello AE. Distribution of races and Tox genes in Pyrenophora tritici-repentis isolates from wheat in Argentina. Trop Plant Pathol. 2015;40(2):141-146. https://doi.org/10.1007/s40858-015-0011-2.
  8. See PT, Marathamuthu KA, Iagallo EM, et al. Evaluating the importance of the tan spot ToxA-Tsn1 interaction in Australian wheat varieties. Plant Pathol. 2018;67(5):1066-1075. https://doi.org/10.1111/ppa.12835.
  9. Guo J, Shi G, Liu Z. Characterizing virulence of the Pyrenophora tritici-repentis isolates lacking both ToxA and ToxB genes. Pathogens. 2018;7(3):74. https://doi.org/10.3390/pathogens7030074.
  10. Мироненко Н.В., Коваленко Н.М., Баранова О.А. Характеристика географически отдаленных популяций Pyrenophora tritici-repentis по вирулентности и генам токсинообразования ToxA и ToxB // Вестник защиты растений. – 2019. – № 1. – C. 24–29. [Mironenko NV, Kovalenko NM, Baranova OA. Characteristics of the geographically distant populations of Pyrenophora tritici-repentis in terms of virulence and ToxA and ToxB toxin-forming gene. Plant Protection News. 2019;(1):24-29 (In Russ.)]. https://doi.org/10.31993/2308-6459-2019-1(99)-24-29.
  11. Strelkov SE, Lamari L. Host-parasite interactions in tan spot (Pyrenophora tritici-repentis) of wheat. Can J Plant Pathol. 2003;25(4):339-449. https://doi.org/10.1080/07060660309507089.
  12. Faris JD, Zhang Z, Lu H, et al. A unique wheat disease resistance-like gene governs effector-triggered susceptibility to necrotrophic pathogens. Proc Natl Acad Sci USA. 2010;107(30):13544-13549. https://doi.org/ 10.1073/pnas.1004090107.
  13. Friesen TL, Stukenbrock EH, Liu Z, et al. Emergence of a new disease as a result of interspecific virulence gene transfer. Nat Genet. 2006;38(8):953-956. https://doi.org/10.1038/ng1839.
  14. Rybak K, See PT, Phan HT, et al. A functionally conserved Zn2Cys6 binuclear cluster transcription factor class regulates necrotrophic effector gene expression and host specific virulence of two major Pleosporales fungal pathogens of wheat. Mol Plant Pathol. 2017;18(3):420-434. https://doi.org/10.1111/mpp.12511.
  15. Мироненко Н.В., Орина А.С., Коваленко Н.М. Межштаммовые различия Pyrenophora tritici-repentis по экспрессии генов ToxA и PtrPf2 в культуре // Генетика. – 2020. – Т. 56. – № 4. – С. 488–492. [Mironenko NV, Orina AS, Kovalenko NM. Differences among Pyrenophora tritici-repentis isolatesin the expression of ToxA and PtrPf2 genes in culture (in vitro). Genetika. 2020;56(4)488-492. (In Russ.)]. https://doi.org/10.31857/S0016675820040086.
  16. Михайлова Л.А., Мироненко Н.В., Коваленко Н.М. Желтая пятнистость пшеницы. – СПб.: ВИЗР, 2012. – 56 с. [Mikhailova LA, Mironenko NV, Kovalenko NM. Zheltaya pyatnistost’ pshenicy. Saint Petersburg: VIZR; 2012. 56 p. (In Russ.)]
  17. Rees RG, Platz GJ, Mayer RJ. Susceptibility of Australian wheats to Pyrenophora tritici-repentis. Aust J Agric Res. 1988;39(2):141-151. https://doi.org/10.1071/AR9880141.
  18. Moolhuijzen PM, See PT, Oliver R, Moffat CS. Genomic distribution of a novel Pyrenophora tritici-repentis ToxA insertion element. PLoS One. 2018;13(10): e0206586. https://doi.org/10.1371/journal.pone.0206586.
  19. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods. 2001;25(4):402-408. https://doi.org/ 10.1006/meth.2001.1262.
  20. Aboukhaddour R, Turkington TK, Strelkov SE. Race structure of Pyrenophora tritici-repentis (tan spot of wheat) in Alberta, Canada. Can J Plant Pathol. 2013;35(2):256-268. https://doi.org/10.1080/07060661.2013. 782470.
  21. Ali S, Gurung S, Adhikari TB. Identification and characterization of novel isolates of Pyrenophora tritici-repentis from arkansas. Plant Dis. 2010;94(2):229-235. https://doi.org/10.1094/PDIS-94-2-0229.
  22. Leišova-Svobodova L, Hanzalova A, Kucer L. Expansion and variability of the Ptr Tox A gene in populations of Pyrenophora tritici-repentis and Pyrenophora teres. J Plant Pathol. 2010;92(3): 729-735. http://dx.doi.org/10.4454/jpp.v92i3.319.
  23. Benslimane H. Virulence phenotyping and molecular characterization of a new virulence type of Pyrenophora tritici-repentis the causal agent of tan spot. Plant Pathol J. 2018;34(2):139-142. https://doi.org/10.5423/PPJ.NT.07.2017.0150.
  24. Friesen TL, Holmes DJ, Bowden RL, Faris JD. ToxA is present in the U.S. Bipolaris sorokiniana population and is a significant virulence factor on wheat harboring Tsn1. Plant Dis. 2018;102(12):2446-2452. https://doi.org/10.1094/pdis-03-18-0521-re.
  25. McDonald MC, Ahren D, Simpfendorfer S, et al. The discovery of the virulence gene ToxA in the wheat and barley pathogen Bipolaris sorokiniana. Mol Plant Pathol. 2018;19(2):432-439. https://doi.org/10.1111/mpp.12535.
  26. Shelest E. Transcription factors in fungi. FEMS Microbiol Lett. 2008;286(2):145-151. https://doi.org/10.1111/j.1574-6968.2008.01293.x.
  27. Todd RB, Zhou M, Ohm RA, et al. Prevalence of transcription factors in ascomycete and basidiomycete fungi. BMC Genomics. 2014;15:214. https://doi.org/10.1186/1471-2164-15-214.
  28. Faris JD, Zhang Z, Rasmussen JB, Friesen TL. Variable expression of the Stagonospora nodorum effector SnToxA among isolates is correlated with levels of disease in wheat. Mol Plant Microbe Interact. 2011;24(12): 1419-1426. https://doi.org/10.1094/MPMI- 04-11-0094.
  29. Phan HT, Rybak K, Furuki E, et al. Differential effector gene expression underpins epistasis in a plant fungal disease. Plant J. 2016;87(4): 343-354. https://doi.org/10.1111/tpj.13203.
  30. Virdi SK, Liu Z, Overlander ME, et al. New insights into the roles of host gene-necrotrophic effector interactions in governing susceptibility of durum wheat to tan spot and Septoria nodorum blotch. G3 (Bethesda). 2016;6(12):4139-4150. https://doi.org/10.1534/g3.116.036525.
  31. Palma-Guerrero J, Ma X, Torriani SF, et al. Comparative transcriptome analyses in Zymoseptoria tritici reveal significant differences in gene expression among strains during plant infection. Mol Plant Microbe Interact. 2017;30(3): 231-244. https://doi.org/10.1094/MPMI-07-16-0146-R.

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Copyright (c) 2020 Mironenko N.V., Orina A.S., Kovalenko N.M.

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