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Marasmius oreades agglutinin enhances resistance of Arabidopsis against plant-parasitic nematodes and a herbivorous insect

BACKGROUND: Plant-parasitic nematodes and herbivorous insects have a significant negative impact on global crop production. A successful approach to protect crops from these pests is the in planta expression of nematotoxic or entomotoxic proteins such as crystal proteins from Bacillus thuringiensis...

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Autores principales: Moradi, Aboubakr, Austerlitz, Tina, Dahlin, Paul, Robert, Christelle AM, Maurer, Corina, Steinauer, Katja, van Doan, Cong, Himmighofen, Paul Anton, Wieczorek, Krzysztof, Künzler, Markus, Mauch, Felix
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8408931/
https://www.ncbi.nlm.nih.gov/pubmed/34470613
http://dx.doi.org/10.1186/s12870-021-03186-0
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author Moradi, Aboubakr
Austerlitz, Tina
Dahlin, Paul
Robert, Christelle AM
Maurer, Corina
Steinauer, Katja
van Doan, Cong
Himmighofen, Paul Anton
Wieczorek, Krzysztof
Künzler, Markus
Mauch, Felix
author_facet Moradi, Aboubakr
Austerlitz, Tina
Dahlin, Paul
Robert, Christelle AM
Maurer, Corina
Steinauer, Katja
van Doan, Cong
Himmighofen, Paul Anton
Wieczorek, Krzysztof
Künzler, Markus
Mauch, Felix
author_sort Moradi, Aboubakr
collection PubMed
description BACKGROUND: Plant-parasitic nematodes and herbivorous insects have a significant negative impact on global crop production. A successful approach to protect crops from these pests is the in planta expression of nematotoxic or entomotoxic proteins such as crystal proteins from Bacillus thuringiensis (Bt) or plant lectins. However, the efficacy of this approach is threatened by emergence of resistance in nematode and insect populations to these proteins. To solve this problem, novel nematotoxic and entomotoxic proteins are needed. During the last two decades, several cytoplasmic lectins from mushrooms with nematicidal and insecticidal activity have been characterized. In this study, we tested the potential of Marasmius oreades agglutinin (MOA) to furnish Arabidopsis plants with resistance towards three economically important crop pests: the two plant-parasitic nematodes Heterodera schachtii and Meloidogyne incognita and the herbivorous diamondback moth Plutella xylostella. RESULTS: The expression of MOA does not affect plant growth under axenic conditions which is an essential parameter in the engineering of genetically modified crops. The transgenic Arabidopsis lines showed nearly complete resistance to H. schachtii, in that the number of female and male nematodes per cm root was reduced by 86–91 % and 43–93 % compared to WT, respectively. M. incognita proved to be less susceptible to the MOA protein in that 18–25 % and 26–35 % less galls and nematode egg masses, respectively, were observed in the transgenic lines. Larvae of the herbivorous P. xylostella foraging on MOA-expression lines showed a lower relative mass gain (22–38 %) and survival rate (15–24 %) than those feeding on WT plants. CONCLUSIONS: The results of our in planta experiments reveal a robust nematicidal and insecticidal activity of the fungal lectin MOA against important agricultural pests which may be exploited for crop protection. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12870-021-03186-0.
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spelling pubmed-84089312021-09-01 Marasmius oreades agglutinin enhances resistance of Arabidopsis against plant-parasitic nematodes and a herbivorous insect Moradi, Aboubakr Austerlitz, Tina Dahlin, Paul Robert, Christelle AM Maurer, Corina Steinauer, Katja van Doan, Cong Himmighofen, Paul Anton Wieczorek, Krzysztof Künzler, Markus Mauch, Felix BMC Plant Biol Research Article BACKGROUND: Plant-parasitic nematodes and herbivorous insects have a significant negative impact on global crop production. A successful approach to protect crops from these pests is the in planta expression of nematotoxic or entomotoxic proteins such as crystal proteins from Bacillus thuringiensis (Bt) or plant lectins. However, the efficacy of this approach is threatened by emergence of resistance in nematode and insect populations to these proteins. To solve this problem, novel nematotoxic and entomotoxic proteins are needed. During the last two decades, several cytoplasmic lectins from mushrooms with nematicidal and insecticidal activity have been characterized. In this study, we tested the potential of Marasmius oreades agglutinin (MOA) to furnish Arabidopsis plants with resistance towards three economically important crop pests: the two plant-parasitic nematodes Heterodera schachtii and Meloidogyne incognita and the herbivorous diamondback moth Plutella xylostella. RESULTS: The expression of MOA does not affect plant growth under axenic conditions which is an essential parameter in the engineering of genetically modified crops. The transgenic Arabidopsis lines showed nearly complete resistance to H. schachtii, in that the number of female and male nematodes per cm root was reduced by 86–91 % and 43–93 % compared to WT, respectively. M. incognita proved to be less susceptible to the MOA protein in that 18–25 % and 26–35 % less galls and nematode egg masses, respectively, were observed in the transgenic lines. Larvae of the herbivorous P. xylostella foraging on MOA-expression lines showed a lower relative mass gain (22–38 %) and survival rate (15–24 %) than those feeding on WT plants. CONCLUSIONS: The results of our in planta experiments reveal a robust nematicidal and insecticidal activity of the fungal lectin MOA against important agricultural pests which may be exploited for crop protection. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12870-021-03186-0. BioMed Central 2021-09-01 /pmc/articles/PMC8408931/ /pubmed/34470613 http://dx.doi.org/10.1186/s12870-021-03186-0 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Moradi, Aboubakr
Austerlitz, Tina
Dahlin, Paul
Robert, Christelle AM
Maurer, Corina
Steinauer, Katja
van Doan, Cong
Himmighofen, Paul Anton
Wieczorek, Krzysztof
Künzler, Markus
Mauch, Felix
Marasmius oreades agglutinin enhances resistance of Arabidopsis against plant-parasitic nematodes and a herbivorous insect
title Marasmius oreades agglutinin enhances resistance of Arabidopsis against plant-parasitic nematodes and a herbivorous insect
title_full Marasmius oreades agglutinin enhances resistance of Arabidopsis against plant-parasitic nematodes and a herbivorous insect
title_fullStr Marasmius oreades agglutinin enhances resistance of Arabidopsis against plant-parasitic nematodes and a herbivorous insect
title_full_unstemmed Marasmius oreades agglutinin enhances resistance of Arabidopsis against plant-parasitic nematodes and a herbivorous insect
title_short Marasmius oreades agglutinin enhances resistance of Arabidopsis against plant-parasitic nematodes and a herbivorous insect
title_sort marasmius oreades agglutinin enhances resistance of arabidopsis against plant-parasitic nematodes and a herbivorous insect
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8408931/
https://www.ncbi.nlm.nih.gov/pubmed/34470613
http://dx.doi.org/10.1186/s12870-021-03186-0
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