Effect of the host-specific toxin SnTOX3 from Stagonospora nodorum on ethylene signaling pathway regulation and redox-state in common wheat

The fungus Stagonospora nodorum Berk. is the causative agent of Septoria nodorum blotch (SNB) of wheat. The most important factors of Stagonospora nodorum virulence include numerous fungal necrotrophic effectors (NEs) encoded by SnTox genes. They interact with the matching products of host susceptib...

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Main Authors: S. V. Veselova, G. F. Burkhanova, T. V. Nuzhnaya, S. D. Rumyantsev, I. V. Maksimov
Format: Article
Language:English
Published: Siberian Branch of the Russian Academy of Sciences, Federal Research Center Institute of Cytology and Genetics, The Vavilov Society of Geneticists and Breeders 2019-11-01
Series:Вавиловский журнал генетики и селекции
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Online Access:https://vavilov.elpub.ru/jour/article/view/2337
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author S. V. Veselova
G. F. Burkhanova
T. V. Nuzhnaya
S. D. Rumyantsev
I. V. Maksimov
author_facet S. V. Veselova
G. F. Burkhanova
T. V. Nuzhnaya
S. D. Rumyantsev
I. V. Maksimov
author_sort S. V. Veselova
collection DOAJ
description The fungus Stagonospora nodorum Berk. is the causative agent of Septoria nodorum blotch (SNB) of wheat. The most important factors of Stagonospora nodorum virulence include numerous fungal necrotrophic effectors (NEs) encoded by SnTox genes. They interact with the matching products of host susceptibility genes (Snn). SnTox-Snn interactions are mirror images of classical gene-for-gene interactions and lead to the development of disease. We have studied the SnTox3-Snn3 interaction, resulting in the development of infection on leaves and formation of extensive lesions. The mechanism of SnTox3 action is likely to be linked to the regulation of redox metabolism and the influence on ethylene synthesis in the wheat plants, although the molecular mechanisms are not fully unveiled. To characterize the SnTox3-Snn3 interaction, we used S. nodorum isolates differing in the expression of the NEs genes SnTox3 (SnB (Tox3+), Sn4VD (Tox3–)) and two soft spring wheat (Triticum aestivum L.) cultivars, contrasting in resistance to the SNB agent and differing in the allelic composition of the susceptibility locus Snn3-B1: Kazakhstanskaya 10 (susceptible) and Omskaya 35 (resistant). We carried out a comparative assessment of the transcriptional activity patterns of genes responsible for ethylene biosynthesis (TaACS1, TaACО) and signaling pathway (TaEIL1, TaERF1) by real-time PCR and estimated the redox state of wheat plants infected with different isolates of S. nodorum by spectrometry. The induction of ethylene biosynthesis and signaling has been shown to result from gene-for-gene interaction between Snn3-B1 and SnTox3. The results of plant redox status estimation showed that ethylene inhibited accumulation of hydrogen peroxide in SnTox3-sensitive genotypes by regulating the operation of various pro-/antioxidant enzymes at the transcriptional and posttranslational levels. Our results suggest that NE SnTox3 influences ethylene biosynthesis and signaling, thereby regulating redox metabolism in infected wheat plants as necessary for successful host colonization at the initial phases of infection, which ultimately leads to extensive lesions due to fast pathogen reproduction.
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spelling doaj.art-41b1189bec2b473ead0204be76c16e3d2024-04-11T15:31:01ZengSiberian Branch of the Russian Academy of Sciences, Federal Research Center Institute of Cytology and Genetics, The Vavilov Society of Geneticists and BreedersВавиловский журнал генетики и селекции2500-32592019-11-0123785686410.18699/VJ19.559982Effect of the host-specific toxin SnTOX3 from Stagonospora nodorum on ethylene signaling pathway regulation and redox-state in common wheatS. V. Veselova0G. F. Burkhanova1T. V. Nuzhnaya2S. D. Rumyantsev3I. V. Maksimov4Institute of Biochemistry and Genetics – Subdivision of the Ufa Federal Research Centre, RASInstitute of Biochemistry and Genetics – Subdivision of the Ufa Federal Research Centre, RASInstitute of Biochemistry and Genetics – Subdivision of the Ufa Federal Research Centre, RASInstitute of Biochemistry and Genetics – Subdivision of the Ufa Federal Research Centre, RASInstitute of Biochemistry and Genetics – Subdivision of the Ufa Federal Research Centre, RASThe fungus Stagonospora nodorum Berk. is the causative agent of Septoria nodorum blotch (SNB) of wheat. The most important factors of Stagonospora nodorum virulence include numerous fungal necrotrophic effectors (NEs) encoded by SnTox genes. They interact with the matching products of host susceptibility genes (Snn). SnTox-Snn interactions are mirror images of classical gene-for-gene interactions and lead to the development of disease. We have studied the SnTox3-Snn3 interaction, resulting in the development of infection on leaves and formation of extensive lesions. The mechanism of SnTox3 action is likely to be linked to the regulation of redox metabolism and the influence on ethylene synthesis in the wheat plants, although the molecular mechanisms are not fully unveiled. To characterize the SnTox3-Snn3 interaction, we used S. nodorum isolates differing in the expression of the NEs genes SnTox3 (SnB (Tox3+), Sn4VD (Tox3–)) and two soft spring wheat (Triticum aestivum L.) cultivars, contrasting in resistance to the SNB agent and differing in the allelic composition of the susceptibility locus Snn3-B1: Kazakhstanskaya 10 (susceptible) and Omskaya 35 (resistant). We carried out a comparative assessment of the transcriptional activity patterns of genes responsible for ethylene biosynthesis (TaACS1, TaACО) and signaling pathway (TaEIL1, TaERF1) by real-time PCR and estimated the redox state of wheat plants infected with different isolates of S. nodorum by spectrometry. The induction of ethylene biosynthesis and signaling has been shown to result from gene-for-gene interaction between Snn3-B1 and SnTox3. The results of plant redox status estimation showed that ethylene inhibited accumulation of hydrogen peroxide in SnTox3-sensitive genotypes by regulating the operation of various pro-/antioxidant enzymes at the transcriptional and posttranslational levels. Our results suggest that NE SnTox3 influences ethylene biosynthesis and signaling, thereby regulating redox metabolism in infected wheat plants as necessary for successful host colonization at the initial phases of infection, which ultimately leads to extensive lesions due to fast pathogen reproduction.https://vavilov.elpub.ru/jour/article/view/2337stagonospora nodorumtriticum aestivumpolymerase chain reactionreal-time polymerase chain reactionnecrotrophic effectorsethyleneredox-metabolismgene-for-gene interactionnonspecific resistance
spellingShingle S. V. Veselova
G. F. Burkhanova
T. V. Nuzhnaya
S. D. Rumyantsev
I. V. Maksimov
Effect of the host-specific toxin SnTOX3 from Stagonospora nodorum on ethylene signaling pathway regulation and redox-state in common wheat
Вавиловский журнал генетики и селекции
stagonospora nodorum
triticum aestivum
polymerase chain reaction
real-time polymerase chain reaction
necrotrophic effectors
ethylene
redox-metabolism
gene-for-gene interaction
nonspecific resistance
title Effect of the host-specific toxin SnTOX3 from Stagonospora nodorum on ethylene signaling pathway regulation and redox-state in common wheat
title_full Effect of the host-specific toxin SnTOX3 from Stagonospora nodorum on ethylene signaling pathway regulation and redox-state in common wheat
title_fullStr Effect of the host-specific toxin SnTOX3 from Stagonospora nodorum on ethylene signaling pathway regulation and redox-state in common wheat
title_full_unstemmed Effect of the host-specific toxin SnTOX3 from Stagonospora nodorum on ethylene signaling pathway regulation and redox-state in common wheat
title_short Effect of the host-specific toxin SnTOX3 from Stagonospora nodorum on ethylene signaling pathway regulation and redox-state in common wheat
title_sort effect of the host specific toxin sntox3 from stagonospora nodorum on ethylene signaling pathway regulation and redox state in common wheat
topic stagonospora nodorum
triticum aestivum
polymerase chain reaction
real-time polymerase chain reaction
necrotrophic effectors
ethylene
redox-metabolism
gene-for-gene interaction
nonspecific resistance
url https://vavilov.elpub.ru/jour/article/view/2337
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