Low Amplitude Boom-and-Bust Cycles Define the Septoria Nodorum Blotch Interaction

Introduction: Septoria nodorum blotch (SNB) is a complex fungal disease of wheat caused by the Dothideomycete fungal pathogen Parastagonospora nodorum. The fungus infects through the use of necrotrophic effectors (NEs) that cause necrosis on hosts carrying matching dominant susceptibility genes. The...

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Main Authors: Phan, Huyen T. T., Jones, Darcy, Rybak, Kasia, Dodhia, Kejal, Lopez-Ruiz, Francisco, Valade, R., Gout, L., Lebrun, M.H., Brunner, P.C., Oliver, Richard, Tan, Kar-Chun
Format: Journal Article
Language:English
Published: FRONTIERS MEDIA SA 2020
Subjects:
Online Access:http://hdl.handle.net/20.500.11937/83209
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author Phan, Huyen T. T.
Jones, Darcy
Rybak, Kasia
Dodhia, Kejal
Lopez-Ruiz, Francisco
Valade, R.
Gout, L.
Lebrun, M.H.
Brunner, P.C.
Oliver, Richard
Tan, Kar-Chun
author_facet Phan, Huyen T. T.
Jones, Darcy
Rybak, Kasia
Dodhia, Kejal
Lopez-Ruiz, Francisco
Valade, R.
Gout, L.
Lebrun, M.H.
Brunner, P.C.
Oliver, Richard
Tan, Kar-Chun
author_sort Phan, Huyen T. T.
building Curtin Institutional Repository
collection Online Access
description Introduction: Septoria nodorum blotch (SNB) is a complex fungal disease of wheat caused by the Dothideomycete fungal pathogen Parastagonospora nodorum. The fungus infects through the use of necrotrophic effectors (NEs) that cause necrosis on hosts carrying matching dominant susceptibility genes. The Western Australia (WA) wheatbelt is a SNB “hot spot” and experiences significant under favorable conditions. Consequently, SNB has been a major target for breeders in WA for many years. Materials and Methods: In this study, we assembled a panel of 155 WA P. nodorum isolates collected over a 44-year period and compared them to 23 isolates from France and the USA using 28 SSR loci. Results: The WA P. nodorum population was clustered into five groups with contrasting properties. 80% of the studied isolates were assigned to two core groups found throughout the collection location and time. The other three non-core groups that encompassed transient and emergent populations were found in restricted locations and time. Changes in group genotypes occurred during periods that coincided with the mass adoption of a single or a small group of widely planted wheat cultivars. When introduced, these cultivars had high scores for SNB resistance. However, the field resistance of these new cultivars often declined over subsequent seasons prompting their replacement with new, more resistant varieties. Pathogenicity assays showed that newly emerged isolates non-core are more pathogenic than old isolates. It is likely that the non-core groups were repeatedly selected for increased virulence on the contemporary popular cultivars. Discussion: The low level of genetic diversity within the non-core groups, difference in virulence, low abundance, and restriction to limited locations suggest that these populations more vulnerable to a population crash when the cultivar was replaced by one that was genetically different and more resistant. We characterize the observed pattern as a low-amplitude boom-and-bust cycle in contrast with the classical high amplitude boom-and-bust cycles seen for biotrophic pathogens where the contrast between resistance and susceptibility is typically much greater. Implications of the results are discussed relating to breeding strategies for more sustainable SNB resistance and more generally for pathogens with NEs.
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institution Curtin University Malaysia
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spelling curtin-20.500.11937-832092021-05-06T02:46:41Z Low Amplitude Boom-and-Bust Cycles Define the Septoria Nodorum Blotch Interaction Phan, Huyen T. T. Jones, Darcy Rybak, Kasia Dodhia, Kejal Lopez-Ruiz, Francisco Valade, R. Gout, L. Lebrun, M.H. Brunner, P.C. Oliver, Richard Tan, Kar-Chun Science & Technology Life Sciences & Biomedicine Plant Sciences septoria nodorum blotch SSR effector population wheat STAGONOSPORA-NODORUM PHAEOSPHAERIA-NODORUM MATING-TYPE SEXUAL REPRODUCTION GENETIC-VARIABILITY GENOTYPIC DIVERSITY PLANT-PATHOGENS WHEAT DISEASE POPULATIONS Introduction: Septoria nodorum blotch (SNB) is a complex fungal disease of wheat caused by the Dothideomycete fungal pathogen Parastagonospora nodorum. The fungus infects through the use of necrotrophic effectors (NEs) that cause necrosis on hosts carrying matching dominant susceptibility genes. The Western Australia (WA) wheatbelt is a SNB “hot spot” and experiences significant under favorable conditions. Consequently, SNB has been a major target for breeders in WA for many years. Materials and Methods: In this study, we assembled a panel of 155 WA P. nodorum isolates collected over a 44-year period and compared them to 23 isolates from France and the USA using 28 SSR loci. Results: The WA P. nodorum population was clustered into five groups with contrasting properties. 80% of the studied isolates were assigned to two core groups found throughout the collection location and time. The other three non-core groups that encompassed transient and emergent populations were found in restricted locations and time. Changes in group genotypes occurred during periods that coincided with the mass adoption of a single or a small group of widely planted wheat cultivars. When introduced, these cultivars had high scores for SNB resistance. However, the field resistance of these new cultivars often declined over subsequent seasons prompting their replacement with new, more resistant varieties. Pathogenicity assays showed that newly emerged isolates non-core are more pathogenic than old isolates. It is likely that the non-core groups were repeatedly selected for increased virulence on the contemporary popular cultivars. Discussion: The low level of genetic diversity within the non-core groups, difference in virulence, low abundance, and restriction to limited locations suggest that these populations more vulnerable to a population crash when the cultivar was replaced by one that was genetically different and more resistant. We characterize the observed pattern as a low-amplitude boom-and-bust cycle in contrast with the classical high amplitude boom-and-bust cycles seen for biotrophic pathogens where the contrast between resistance and susceptibility is typically much greater. Implications of the results are discussed relating to breeding strategies for more sustainable SNB resistance and more generally for pathogens with NEs. 2020 Journal Article http://hdl.handle.net/20.500.11937/83209 10.3389/fpls.2019.01785 English http://creativecommons.org/licenses/by/4.0/ FRONTIERS MEDIA SA fulltext
spellingShingle Science & Technology
Life Sciences & Biomedicine
Plant Sciences
septoria nodorum blotch
SSR
effector
population
wheat
STAGONOSPORA-NODORUM
PHAEOSPHAERIA-NODORUM
MATING-TYPE
SEXUAL REPRODUCTION
GENETIC-VARIABILITY
GENOTYPIC DIVERSITY
PLANT-PATHOGENS
WHEAT
DISEASE
POPULATIONS
Phan, Huyen T. T.
Jones, Darcy
Rybak, Kasia
Dodhia, Kejal
Lopez-Ruiz, Francisco
Valade, R.
Gout, L.
Lebrun, M.H.
Brunner, P.C.
Oliver, Richard
Tan, Kar-Chun
Low Amplitude Boom-and-Bust Cycles Define the Septoria Nodorum Blotch Interaction
title Low Amplitude Boom-and-Bust Cycles Define the Septoria Nodorum Blotch Interaction
title_full Low Amplitude Boom-and-Bust Cycles Define the Septoria Nodorum Blotch Interaction
title_fullStr Low Amplitude Boom-and-Bust Cycles Define the Septoria Nodorum Blotch Interaction
title_full_unstemmed Low Amplitude Boom-and-Bust Cycles Define the Septoria Nodorum Blotch Interaction
title_short Low Amplitude Boom-and-Bust Cycles Define the Septoria Nodorum Blotch Interaction
title_sort low amplitude boom-and-bust cycles define the septoria nodorum blotch interaction
topic Science & Technology
Life Sciences & Biomedicine
Plant Sciences
septoria nodorum blotch
SSR
effector
population
wheat
STAGONOSPORA-NODORUM
PHAEOSPHAERIA-NODORUM
MATING-TYPE
SEXUAL REPRODUCTION
GENETIC-VARIABILITY
GENOTYPIC DIVERSITY
PLANT-PATHOGENS
WHEAT
DISEASE
POPULATIONS
url http://hdl.handle.net/20.500.11937/83209