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Augmenting Sulfur Metabolism and Herbivore Defense in Arabidopsis by Bacterial Volatile Signaling

Sulfur is an element necessary for the life cycle of higher plants. Its assimilation and reduction into essential biomolecules are pivotal factors determining a plant’s growth and vigor as well as resistance to environmental stress. While certain soil microbes can enhance ion solubility via chelatin...

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Autores principales: Aziz, Mina, Nadipalli, Ranjith K., Xie, Xitao, Sun, Yan, Surowiec, Kazimierz, Zhang, Jin-Lin, Paré, Paul W.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4824779/
https://www.ncbi.nlm.nih.gov/pubmed/27092166
http://dx.doi.org/10.3389/fpls.2016.00458
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author Aziz, Mina
Nadipalli, Ranjith K.
Xie, Xitao
Sun, Yan
Surowiec, Kazimierz
Zhang, Jin-Lin
Paré, Paul W.
author_facet Aziz, Mina
Nadipalli, Ranjith K.
Xie, Xitao
Sun, Yan
Surowiec, Kazimierz
Zhang, Jin-Lin
Paré, Paul W.
author_sort Aziz, Mina
collection PubMed
description Sulfur is an element necessary for the life cycle of higher plants. Its assimilation and reduction into essential biomolecules are pivotal factors determining a plant’s growth and vigor as well as resistance to environmental stress. While certain soil microbes can enhance ion solubility via chelating agents or oxidation, microbial regulation of plant-sulfur assimilation has not been reported. With an increasing understanding that soil microbes can activate growth and stress tolerance in plants via chemical signaling, the question arises as to whether such beneficial bacteria also regulate sulfur assimilation. Here we report a previously unidentified mechanism by which the growth-promoting rhizobacterium Bacillus amyloliquefaciens (GB03) transcriptionally activates genes responsible for sulfur assimilation, increasing sulfur uptake and accumulation in Arabidopsis. Transcripts encoding for sulfur-rich aliphatic and indolic glucosinolates are also GB03 induced. As a result, GB03-exposed plants with elevated glucosinolates exhibit greater protection against the generalist herbivore, Spodoptera exigua (beet armyworm, BAW). In contrast, a previously characterized glucosinolate mutant compromised in the production of both aliphatic and indolic glucosinolates is also compromised in terms of GB03-induced protection against insect herbivory. As with in vitro studies, soil-grown plants show enhanced glucosinolate accumulation and protection against BAW feeding with GB03 exposure. These results demonstrate the potential of microbes to enhance plant sulfur assimilation and emphasize the sophisticated integration of microbial signaling in plant defense.
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spelling pubmed-48247792016-04-18 Augmenting Sulfur Metabolism and Herbivore Defense in Arabidopsis by Bacterial Volatile Signaling Aziz, Mina Nadipalli, Ranjith K. Xie, Xitao Sun, Yan Surowiec, Kazimierz Zhang, Jin-Lin Paré, Paul W. Front Plant Sci Plant Science Sulfur is an element necessary for the life cycle of higher plants. Its assimilation and reduction into essential biomolecules are pivotal factors determining a plant’s growth and vigor as well as resistance to environmental stress. While certain soil microbes can enhance ion solubility via chelating agents or oxidation, microbial regulation of plant-sulfur assimilation has not been reported. With an increasing understanding that soil microbes can activate growth and stress tolerance in plants via chemical signaling, the question arises as to whether such beneficial bacteria also regulate sulfur assimilation. Here we report a previously unidentified mechanism by which the growth-promoting rhizobacterium Bacillus amyloliquefaciens (GB03) transcriptionally activates genes responsible for sulfur assimilation, increasing sulfur uptake and accumulation in Arabidopsis. Transcripts encoding for sulfur-rich aliphatic and indolic glucosinolates are also GB03 induced. As a result, GB03-exposed plants with elevated glucosinolates exhibit greater protection against the generalist herbivore, Spodoptera exigua (beet armyworm, BAW). In contrast, a previously characterized glucosinolate mutant compromised in the production of both aliphatic and indolic glucosinolates is also compromised in terms of GB03-induced protection against insect herbivory. As with in vitro studies, soil-grown plants show enhanced glucosinolate accumulation and protection against BAW feeding with GB03 exposure. These results demonstrate the potential of microbes to enhance plant sulfur assimilation and emphasize the sophisticated integration of microbial signaling in plant defense. Frontiers Media S.A. 2016-04-08 /pmc/articles/PMC4824779/ /pubmed/27092166 http://dx.doi.org/10.3389/fpls.2016.00458 Text en Copyright © 2016 Aziz, Nadipalli, Xie, Sun, Surowiec, Zhang and Paré. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Plant Science
Aziz, Mina
Nadipalli, Ranjith K.
Xie, Xitao
Sun, Yan
Surowiec, Kazimierz
Zhang, Jin-Lin
Paré, Paul W.
Augmenting Sulfur Metabolism and Herbivore Defense in Arabidopsis by Bacterial Volatile Signaling
title Augmenting Sulfur Metabolism and Herbivore Defense in Arabidopsis by Bacterial Volatile Signaling
title_full Augmenting Sulfur Metabolism and Herbivore Defense in Arabidopsis by Bacterial Volatile Signaling
title_fullStr Augmenting Sulfur Metabolism and Herbivore Defense in Arabidopsis by Bacterial Volatile Signaling
title_full_unstemmed Augmenting Sulfur Metabolism and Herbivore Defense in Arabidopsis by Bacterial Volatile Signaling
title_short Augmenting Sulfur Metabolism and Herbivore Defense in Arabidopsis by Bacterial Volatile Signaling
title_sort augmenting sulfur metabolism and herbivore defense in arabidopsis by bacterial volatile signaling
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4824779/
https://www.ncbi.nlm.nih.gov/pubmed/27092166
http://dx.doi.org/10.3389/fpls.2016.00458
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