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Volatile Organic Compounds Emitted by the Biocontrol Agent Pythium oligandrum Contribute to Ginger Plant Growth and Disease Resistance

The oomycete Pythium oligandrum is a potential biocontrol agent to control a wide range of fungal and oomycete-caused diseases, such as Pythium myriotylum-caused rhizome rot in ginger, leading to reduced yields and compromised quality. Previously, P. oligandrum has been studied for its plant growth-...

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Autores principales: Sheikh, Taha Majid Mahmood, Zhou, Dongmei, Ali, Haider, Hussain, Sarfraz, Wang, Nan, Chen, Siqiao, Zhao, Yishen, Wen, Xian, Wang, Xiaoyu, Zhang, Jinfeng, Wang, Lunji, Deng, Sheng, Feng, Hui, Raza, Waseem, Fu, Pengxiao, Peng, Hao, Wei, Lihui, Daly, Paul
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10433877/
https://www.ncbi.nlm.nih.gov/pubmed/37534988
http://dx.doi.org/10.1128/spectrum.01510-23
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author Sheikh, Taha Majid Mahmood
Zhou, Dongmei
Ali, Haider
Hussain, Sarfraz
Wang, Nan
Chen, Siqiao
Zhao, Yishen
Wen, Xian
Wang, Xiaoyu
Zhang, Jinfeng
Wang, Lunji
Deng, Sheng
Feng, Hui
Raza, Waseem
Fu, Pengxiao
Peng, Hao
Wei, Lihui
Daly, Paul
author_facet Sheikh, Taha Majid Mahmood
Zhou, Dongmei
Ali, Haider
Hussain, Sarfraz
Wang, Nan
Chen, Siqiao
Zhao, Yishen
Wen, Xian
Wang, Xiaoyu
Zhang, Jinfeng
Wang, Lunji
Deng, Sheng
Feng, Hui
Raza, Waseem
Fu, Pengxiao
Peng, Hao
Wei, Lihui
Daly, Paul
author_sort Sheikh, Taha Majid Mahmood
collection PubMed
description The oomycete Pythium oligandrum is a potential biocontrol agent to control a wide range of fungal and oomycete-caused diseases, such as Pythium myriotylum-caused rhizome rot in ginger, leading to reduced yields and compromised quality. Previously, P. oligandrum has been studied for its plant growth-promoting potential by auxin production and induction of disease resistance by elicitors such as oligandrin. Volatile organic compounds (VOCs) play beneficial roles in sustainable agriculture by enhancing plant growth and resistance. We investigated the contribution of P. oligandrum-produced VOCs on plant growth and disease suppression by initially using Nicotiana benthamiana plants for screening. P. oligandrum VOCs significantly enhanced tobacco seedling and plant biomass contents. Screening of the individual VOCs showed that 3-octanone and hexadecane promoted the growth of tobacco seedlings. The total VOCs from P. oligandrum also enhanced the shoot and root growth of ginger plants. Transcriptomic analysis showed a higher expression of genes related to plant growth hormones and stress responses in the leaves of ginger plants exposed to P. oligandrum VOCs. The concentrations of plant growth hormones such as auxin, zeatin, and gibberellic acid were higher in the leaves of ginger plants exposed to P. oligandrum VOCs. In a ginger disease biocontrol assay, the VOC-exposed ginger plants infected with P. myriotylum had lower levels of disease severity. We conclude that this study contributes to understanding the growth-promoting mechanisms of P. oligandrum on ginger and tobacco, priming of ginger plants against various stresses, and the mechanisms of action of P. oligandrum as a biocontrol agent. IMPORTANCE Plant growth promotion plays a vital role in enhancing production of agricultural crops, and Pythium oligandrum is known for its plant growth-promoting potential through production of auxins and induction of resistance by elicitors. This study highlights the significance of P. oligandrum-produced VOCs in plant growth promotion and disease resistance. Transcriptomic analyses of leaves of ginger plants exposed to P. oligandrum VOCs revealed the upregulation of genes involved in plant growth hormone signaling and stress responses. Moreover, the concentration of growth hormones significantly increased in P. oligandrum VOC-exposed ginger plants. Additionally, the disease severity was reduced in P. myriotylum-infected ginger plants exposed to P. oligandrum VOCs. In ginger, P. myriotylum-caused rhizome rot disease results in severe losses, and biocontrol has a role as part of an integrated pest management strategy for rhizome rot disease. Overall, growth enhancement and disease reduction in plants exposed to P. oligandrum-produced VOCs contribute to its role as a biocontrol agent.
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spelling pubmed-104338772023-08-18 Volatile Organic Compounds Emitted by the Biocontrol Agent Pythium oligandrum Contribute to Ginger Plant Growth and Disease Resistance Sheikh, Taha Majid Mahmood Zhou, Dongmei Ali, Haider Hussain, Sarfraz Wang, Nan Chen, Siqiao Zhao, Yishen Wen, Xian Wang, Xiaoyu Zhang, Jinfeng Wang, Lunji Deng, Sheng Feng, Hui Raza, Waseem Fu, Pengxiao Peng, Hao Wei, Lihui Daly, Paul Microbiol Spectr Research Article The oomycete Pythium oligandrum is a potential biocontrol agent to control a wide range of fungal and oomycete-caused diseases, such as Pythium myriotylum-caused rhizome rot in ginger, leading to reduced yields and compromised quality. Previously, P. oligandrum has been studied for its plant growth-promoting potential by auxin production and induction of disease resistance by elicitors such as oligandrin. Volatile organic compounds (VOCs) play beneficial roles in sustainable agriculture by enhancing plant growth and resistance. We investigated the contribution of P. oligandrum-produced VOCs on plant growth and disease suppression by initially using Nicotiana benthamiana plants for screening. P. oligandrum VOCs significantly enhanced tobacco seedling and plant biomass contents. Screening of the individual VOCs showed that 3-octanone and hexadecane promoted the growth of tobacco seedlings. The total VOCs from P. oligandrum also enhanced the shoot and root growth of ginger plants. Transcriptomic analysis showed a higher expression of genes related to plant growth hormones and stress responses in the leaves of ginger plants exposed to P. oligandrum VOCs. The concentrations of plant growth hormones such as auxin, zeatin, and gibberellic acid were higher in the leaves of ginger plants exposed to P. oligandrum VOCs. In a ginger disease biocontrol assay, the VOC-exposed ginger plants infected with P. myriotylum had lower levels of disease severity. We conclude that this study contributes to understanding the growth-promoting mechanisms of P. oligandrum on ginger and tobacco, priming of ginger plants against various stresses, and the mechanisms of action of P. oligandrum as a biocontrol agent. IMPORTANCE Plant growth promotion plays a vital role in enhancing production of agricultural crops, and Pythium oligandrum is known for its plant growth-promoting potential through production of auxins and induction of resistance by elicitors. This study highlights the significance of P. oligandrum-produced VOCs in plant growth promotion and disease resistance. Transcriptomic analyses of leaves of ginger plants exposed to P. oligandrum VOCs revealed the upregulation of genes involved in plant growth hormone signaling and stress responses. Moreover, the concentration of growth hormones significantly increased in P. oligandrum VOC-exposed ginger plants. Additionally, the disease severity was reduced in P. myriotylum-infected ginger plants exposed to P. oligandrum VOCs. In ginger, P. myriotylum-caused rhizome rot disease results in severe losses, and biocontrol has a role as part of an integrated pest management strategy for rhizome rot disease. Overall, growth enhancement and disease reduction in plants exposed to P. oligandrum-produced VOCs contribute to its role as a biocontrol agent. American Society for Microbiology 2023-08-03 /pmc/articles/PMC10433877/ /pubmed/37534988 http://dx.doi.org/10.1128/spectrum.01510-23 Text en Copyright © 2023 Sheikh et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Sheikh, Taha Majid Mahmood
Zhou, Dongmei
Ali, Haider
Hussain, Sarfraz
Wang, Nan
Chen, Siqiao
Zhao, Yishen
Wen, Xian
Wang, Xiaoyu
Zhang, Jinfeng
Wang, Lunji
Deng, Sheng
Feng, Hui
Raza, Waseem
Fu, Pengxiao
Peng, Hao
Wei, Lihui
Daly, Paul
Volatile Organic Compounds Emitted by the Biocontrol Agent Pythium oligandrum Contribute to Ginger Plant Growth and Disease Resistance
title Volatile Organic Compounds Emitted by the Biocontrol Agent Pythium oligandrum Contribute to Ginger Plant Growth and Disease Resistance
title_full Volatile Organic Compounds Emitted by the Biocontrol Agent Pythium oligandrum Contribute to Ginger Plant Growth and Disease Resistance
title_fullStr Volatile Organic Compounds Emitted by the Biocontrol Agent Pythium oligandrum Contribute to Ginger Plant Growth and Disease Resistance
title_full_unstemmed Volatile Organic Compounds Emitted by the Biocontrol Agent Pythium oligandrum Contribute to Ginger Plant Growth and Disease Resistance
title_short Volatile Organic Compounds Emitted by the Biocontrol Agent Pythium oligandrum Contribute to Ginger Plant Growth and Disease Resistance
title_sort volatile organic compounds emitted by the biocontrol agent pythium oligandrum contribute to ginger plant growth and disease resistance
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10433877/
https://www.ncbi.nlm.nih.gov/pubmed/37534988
http://dx.doi.org/10.1128/spectrum.01510-23
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