Biosynthesis and Emission of Stress-Induced Volatile Terpenes in Roots and Leaves of Switchgrass (Panicum virgatum L.)
Abstract
Switchgrass (Panicum virgatum L.), a perennial C4 grass, represents an important species in natural and anthropogenic grasslands of North America. Its resilience to abiotic and biotic stress has made switchgrass a preferred bioenergy crop. However, little is known about the mechanisms of resistance of switchgrass against pathogens and herbivores. Volatile compounds such as terpenes have important activities in plant direct and indirect defense. Here, we show that switchgrass leaves emit blends of monoterpenes and sesquiterpenes upon feeding by the generalist insect herbivore Spodoptera frugiperda (fall armyworm) and in a systemic response to the treatment of roots with defense hormones. Belowground application of methyl jasmonate also induced the release of volatile terpenes from roots. To correlate the emission of terpenes with the expression and activity of their corresponding biosynthetic genes, we identified a gene family of 44 monoterpene and sesquiterpene synthases (mono- and sesqui-TPSs) of the type-a, type-b, type-g, and type-e subfamilies, of which 32 TPSs were found to be functionally active in vitro. The TPS genes are distributed over the K and N subgenomes with clusters occurring on several chromosomes. Synteny analysis revealed syntenic networks for approximately 30–40% of the switchgrass TPS genes in the genomes of Panicum hallii, Setariamore », and Sorghum bicolor, suggesting shared TPS ancestry in the common progenitor of these grass lineages. Eighteen switchgrass TPS genes were substantially induced upon insect and hormone treatment and the enzymatic products of nine of these genes correlated with compounds of the induced volatile blends. In accordance with the emission of volatiles, TPS gene expression was induced systemically in response to belowground treatment, whereas this response was not observed upon aboveground feeding of S. frugiperda. Our results demonstrate complex above and belowground responses of induced volatile terpene metabolism in switchgrass and provide a framework for more detailed investigations of the function of terpenes in stress resistance in this monocot crop
- Authors:
-
- Virginia Polytechnic Inst. and State Univ. (Virginia Tech), Blacksburg, VA (United States). Dept. of Biological Sciences
- Univ. of Tennessee, Knoxville, TN (United States). Dept. of Plant Sciences
- Hudson Alpha Institute for Biotechnology, Huntsville, AL (United States). Genome Sequencing Ctr.
- Max Planck Institute for Chemical Ecology, Jena (Germany). Dept. of Biochemistry
- Univ. of California, Davis, CA (United States). Dept. of Plant Biology
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC)
- OSTI Identifier:
- 1628296
- Grant/Contract Number:
- AC02-05CH11231
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Frontiers in Plant Science
- Additional Journal Information:
- Journal Volume: 10; Journal ID: ISSN 1664-462X
- Publisher:
- Frontiers Research Foundation
- Country of Publication:
- United States
- Language:
- English
- Subject:
- Plant Sciences
Citation Formats
Muchlinski, Andrew, Chen, Xinlu, Lovell, John T., Köllner, Tobias G., Pelot, Kyle A., Zerbe, Philipp, Ruggiero, Meredith, Callaway, LeMar, Laliberte, Suzanne, Chen, Feng, and Tholl, Dorothea. Biosynthesis and Emission of Stress-Induced Volatile Terpenes in Roots and Leaves of Switchgrass (Panicum virgatum L.). United States: N. p., 2019.
Web. doi:10.3389/fpls.2019.01144.
Muchlinski, Andrew, Chen, Xinlu, Lovell, John T., Köllner, Tobias G., Pelot, Kyle A., Zerbe, Philipp, Ruggiero, Meredith, Callaway, LeMar, Laliberte, Suzanne, Chen, Feng, & Tholl, Dorothea. Biosynthesis and Emission of Stress-Induced Volatile Terpenes in Roots and Leaves of Switchgrass (Panicum virgatum L.). United States. https://doi.org/10.3389/fpls.2019.01144
Muchlinski, Andrew, Chen, Xinlu, Lovell, John T., Köllner, Tobias G., Pelot, Kyle A., Zerbe, Philipp, Ruggiero, Meredith, Callaway, LeMar, Laliberte, Suzanne, Chen, Feng, and Tholl, Dorothea. Thu .
"Biosynthesis and Emission of Stress-Induced Volatile Terpenes in Roots and Leaves of Switchgrass (Panicum virgatum L.)". United States. https://doi.org/10.3389/fpls.2019.01144. https://www.osti.gov/servlets/purl/1628296.
@article{osti_1628296,
title = {Biosynthesis and Emission of Stress-Induced Volatile Terpenes in Roots and Leaves of Switchgrass (Panicum virgatum L.)},
author = {Muchlinski, Andrew and Chen, Xinlu and Lovell, John T. and Köllner, Tobias G. and Pelot, Kyle A. and Zerbe, Philipp and Ruggiero, Meredith and Callaway, LeMar and Laliberte, Suzanne and Chen, Feng and Tholl, Dorothea},
abstractNote = {Switchgrass (Panicum virgatum L.), a perennial C4 grass, represents an important species in natural and anthropogenic grasslands of North America. Its resilience to abiotic and biotic stress has made switchgrass a preferred bioenergy crop. However, little is known about the mechanisms of resistance of switchgrass against pathogens and herbivores. Volatile compounds such as terpenes have important activities in plant direct and indirect defense. Here, we show that switchgrass leaves emit blends of monoterpenes and sesquiterpenes upon feeding by the generalist insect herbivore Spodoptera frugiperda (fall armyworm) and in a systemic response to the treatment of roots with defense hormones. Belowground application of methyl jasmonate also induced the release of volatile terpenes from roots. To correlate the emission of terpenes with the expression and activity of their corresponding biosynthetic genes, we identified a gene family of 44 monoterpene and sesquiterpene synthases (mono- and sesqui-TPSs) of the type-a, type-b, type-g, and type-e subfamilies, of which 32 TPSs were found to be functionally active in vitro. The TPS genes are distributed over the K and N subgenomes with clusters occurring on several chromosomes. Synteny analysis revealed syntenic networks for approximately 30–40% of the switchgrass TPS genes in the genomes of Panicum hallii, Setaria italica, and Sorghum bicolor, suggesting shared TPS ancestry in the common progenitor of these grass lineages. Eighteen switchgrass TPS genes were substantially induced upon insect and hormone treatment and the enzymatic products of nine of these genes correlated with compounds of the induced volatile blends. In accordance with the emission of volatiles, TPS gene expression was induced systemically in response to belowground treatment, whereas this response was not observed upon aboveground feeding of S. frugiperda. Our results demonstrate complex above and belowground responses of induced volatile terpene metabolism in switchgrass and provide a framework for more detailed investigations of the function of terpenes in stress resistance in this monocot crop},
doi = {10.3389/fpls.2019.01144},
journal = {Frontiers in Plant Science},
number = ,
volume = 10,
place = {United States},
year = {Thu Sep 19 00:00:00 EDT 2019},
month = {Thu Sep 19 00:00:00 EDT 2019}
}
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Supplementary Table 1: Normalized emission of volatile compounds from switchgrass plants (cv. Alamo) treated with fall armyworms (FAW), methyl jasmonate (MeJA), salicylic acid (SA) or mock control. Results from non-treated controls were the same as mock controls. Values were obtained in biological triplicate and are reported as mean peak areamore »
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Indole is an essential herbivore-induced volatile priming signal in maize
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- Nature Genetics, Vol. 50, Issue 9
Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.