Unraveling the tripartite interaction of volatile compounds of Streptomyces rochei with grain mold pathogens infecting sorghum

Sorghum is a major grain crop used in traditional meals and health drinks, and as an efficient fuel. However, its productivity, value, germination, and usability are affected by grain mold, which is a severe problem in sorghum production systems, which reduces the yield of harvested grains for consu...

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Main Authors: A. Sudha, D. Durgadevi, S. Archana, A. Muthukumar, T. Suthin Raj, S. Nakkeeran, Peter Poczai, Omaima Nasif, Mohammad Javed Ansari, R. Z. Sayyed
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-07-01
Series:Frontiers in Microbiology
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Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2022.923360/full
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author A. Sudha
D. Durgadevi
S. Archana
A. Muthukumar
T. Suthin Raj
S. Nakkeeran
Peter Poczai
Omaima Nasif
Mohammad Javed Ansari
R. Z. Sayyed
author_facet A. Sudha
D. Durgadevi
S. Archana
A. Muthukumar
T. Suthin Raj
S. Nakkeeran
Peter Poczai
Omaima Nasif
Mohammad Javed Ansari
R. Z. Sayyed
author_sort A. Sudha
collection DOAJ
description Sorghum is a major grain crop used in traditional meals and health drinks, and as an efficient fuel. However, its productivity, value, germination, and usability are affected by grain mold, which is a severe problem in sorghum production systems, which reduces the yield of harvested grains for consumer use. The organic approach to the management of the disease is essential and will increase consumer demand. Bioactive molecules like mVOC (volatile organic compound) identification are used to unravel the molecules responsible for antifungal activity. The Streptomyces rochei strain (ASH) has been reported to be a potential antagonist to many pathogens, with high levels of VOCs. The present study aimed to study the inhibitory effect of S. rochei on sorghum grain mold pathogens using a dual culture technique and via the production of microbial volatile organic compounds (mVOCs). mVOCs inhibited the mycelial growth of Fusarium moniliforme by 63.75 and Curvularia lunata by 68.52%. mVOCs suppressed mycelial growth and inhibited the production of spores by altering the structure of mycelia in tripartite plate assay. About 45 mVOCs were profiled when Streptomyces rochei interacted with these two pathogens. In the present study, several compounds were upregulated or downregulated by S. rochei, including 2-methyl-1-butanol, methanoazulene, and cedrene. S. rochei emitted novel terpenoid compounds with peak areas, such as myrcene (1.14%), cymene (6.41%), and ç-terpinene (7.32%) upon interaction with F. moniliforme and C. lunata. The peak area of some of the compounds, including furan 2-methyl (0.70%), benzene (1.84%), 1-butanol, 2-methyl-(8.25%), and myrcene (1.12)%, was increased during tripartite interaction with F. moniliforme and C. lunata, which resulted in furan 2-methyl (6.60%), benzene (4.43%), butanol, 2-methyl (18.67%), and myrcene (1.14%). These metabolites were implicated in the sesquiterpenoid and alkane biosynthetic pathways and the oxalic acid degradation pathway. The present study shows how S. rochei exhibits hyperparasitism, competition, and antibiosis via mVOCs. In addition to their antimicrobial functions, these metabolites could also enhance plant growth.
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spelling doaj.art-d3c2c938c0f14c87b635ffec948636632022-12-22T02:50:05ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2022-07-011310.3389/fmicb.2022.923360923360Unraveling the tripartite interaction of volatile compounds of Streptomyces rochei with grain mold pathogens infecting sorghumA. Sudha0D. Durgadevi1S. Archana2A. Muthukumar3T. Suthin Raj4S. Nakkeeran5Peter Poczai6Omaima Nasif7Mohammad Javed Ansari8R. Z. Sayyed9Department of Plant Pathology, Tamil Nadu Agricultural University, Coimbatore, IndiaDepartment of Plant Pathology, Tamil Nadu Agricultural University, Coimbatore, IndiaDepartment of Plant Pathology, Tamil Nadu Agricultural University, Coimbatore, IndiaDepartment of Plant Pathology, Faculty of Agriculture, Annamalai University, Chidambaram, IndiaDepartment of Plant Pathology, Faculty of Agriculture, Annamalai University, Chidambaram, IndiaDepartment of Biotechnology, Tamil Nadu Agricultural University, Coimbatore, IndiaFinnish Museum of Natural History, University of Helsinki, Helsinki, FinlandDepartment of Physiology, College of Medicine, King Khalid University Hospital, King Saud University, Riyadh, Saudi ArabiaDepartment of Botany, Hindu College, (Mahatma Jyotiba Phule Rohilkhand University, Bareilly), Moradabad, IndiaDepartment of Microbiology, PSGVP Mandal’s S. I. Patil Arts, G. B. Patel Science, and STKV Sangh Commerce College, Shahada, IndiaSorghum is a major grain crop used in traditional meals and health drinks, and as an efficient fuel. However, its productivity, value, germination, and usability are affected by grain mold, which is a severe problem in sorghum production systems, which reduces the yield of harvested grains for consumer use. The organic approach to the management of the disease is essential and will increase consumer demand. Bioactive molecules like mVOC (volatile organic compound) identification are used to unravel the molecules responsible for antifungal activity. The Streptomyces rochei strain (ASH) has been reported to be a potential antagonist to many pathogens, with high levels of VOCs. The present study aimed to study the inhibitory effect of S. rochei on sorghum grain mold pathogens using a dual culture technique and via the production of microbial volatile organic compounds (mVOCs). mVOCs inhibited the mycelial growth of Fusarium moniliforme by 63.75 and Curvularia lunata by 68.52%. mVOCs suppressed mycelial growth and inhibited the production of spores by altering the structure of mycelia in tripartite plate assay. About 45 mVOCs were profiled when Streptomyces rochei interacted with these two pathogens. In the present study, several compounds were upregulated or downregulated by S. rochei, including 2-methyl-1-butanol, methanoazulene, and cedrene. S. rochei emitted novel terpenoid compounds with peak areas, such as myrcene (1.14%), cymene (6.41%), and ç-terpinene (7.32%) upon interaction with F. moniliforme and C. lunata. The peak area of some of the compounds, including furan 2-methyl (0.70%), benzene (1.84%), 1-butanol, 2-methyl-(8.25%), and myrcene (1.12)%, was increased during tripartite interaction with F. moniliforme and C. lunata, which resulted in furan 2-methyl (6.60%), benzene (4.43%), butanol, 2-methyl (18.67%), and myrcene (1.14%). These metabolites were implicated in the sesquiterpenoid and alkane biosynthetic pathways and the oxalic acid degradation pathway. The present study shows how S. rochei exhibits hyperparasitism, competition, and antibiosis via mVOCs. In addition to their antimicrobial functions, these metabolites could also enhance plant growth.https://www.frontiersin.org/articles/10.3389/fmicb.2022.923360/fullantifungalgrain moldinteractionmVOCssorghumS. rochei
spellingShingle A. Sudha
D. Durgadevi
S. Archana
A. Muthukumar
T. Suthin Raj
S. Nakkeeran
Peter Poczai
Omaima Nasif
Mohammad Javed Ansari
R. Z. Sayyed
Unraveling the tripartite interaction of volatile compounds of Streptomyces rochei with grain mold pathogens infecting sorghum
Frontiers in Microbiology
antifungal
grain mold
interaction
mVOCs
sorghum
S. rochei
title Unraveling the tripartite interaction of volatile compounds of Streptomyces rochei with grain mold pathogens infecting sorghum
title_full Unraveling the tripartite interaction of volatile compounds of Streptomyces rochei with grain mold pathogens infecting sorghum
title_fullStr Unraveling the tripartite interaction of volatile compounds of Streptomyces rochei with grain mold pathogens infecting sorghum
title_full_unstemmed Unraveling the tripartite interaction of volatile compounds of Streptomyces rochei with grain mold pathogens infecting sorghum
title_short Unraveling the tripartite interaction of volatile compounds of Streptomyces rochei with grain mold pathogens infecting sorghum
title_sort unraveling the tripartite interaction of volatile compounds of streptomyces rochei with grain mold pathogens infecting sorghum
topic antifungal
grain mold
interaction
mVOCs
sorghum
S. rochei
url https://www.frontiersin.org/articles/10.3389/fmicb.2022.923360/full
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