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Genetic and environmental variation impact the cuticular hydrocarbon metabolome on the stigmatic surfaces of maize

BACKGROUND: Simple non-isoprenoid hydrocarbons accumulate in discrete regions of the biosphere, including within bacteria and algae as a carbon and/or energy store, and the cuticles of plants and insects, where they may protect against environmental stresses. The extracellular cuticular surfaces of...

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Autores principales: Dennison, Tesia, Qin, Wenmin, Loneman, Derek M., Condon, Samson G. F., Lauter, Nick, Nikolau, Basil J., Yandeau-Nelson, Marna D.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6796380/
https://www.ncbi.nlm.nih.gov/pubmed/31623561
http://dx.doi.org/10.1186/s12870-019-2040-3
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author Dennison, Tesia
Qin, Wenmin
Loneman, Derek M.
Condon, Samson G. F.
Lauter, Nick
Nikolau, Basil J.
Yandeau-Nelson, Marna D.
author_facet Dennison, Tesia
Qin, Wenmin
Loneman, Derek M.
Condon, Samson G. F.
Lauter, Nick
Nikolau, Basil J.
Yandeau-Nelson, Marna D.
author_sort Dennison, Tesia
collection PubMed
description BACKGROUND: Simple non-isoprenoid hydrocarbons accumulate in discrete regions of the biosphere, including within bacteria and algae as a carbon and/or energy store, and the cuticles of plants and insects, where they may protect against environmental stresses. The extracellular cuticular surfaces of the stigmatic silks of maize are rich in linear hydrocarbons and therefore provide a convenient system to study the biological origins and functions of these unique metabolites. RESULTS: To test the hypotheses that genetics and environment influence the accumulation of surface hydrocarbons on silks and to examine the breadth of metabolome compositions across diverse germplasm, cuticular hydrocarbons were analyzed on husk-encased silks and silks that emerged from the husk leaves from 32 genetically diverse maize inbred lines, most of which are commonly utilized in genetics experiments. Total hydrocarbon accumulation varied ~ 10-fold among inbred lines, and up to 5-fold between emerged and husk-encased silks. Alkenes accounted for 5-60% of the total hydrocarbon metabolome, and the majority of alkenes were monoenes with a double bond at either the 7th or 9th carbon atom of the alkyl chain. Total hydrocarbon accumulation was impacted to similar degrees by genotype and husk encasement status, whereas genotype predominantly impacted alkene composition. Only minor differences in the metabolome were observed on silks that were emerged into the external environment for 3- versus 6-days. The environmental influence on the metabolome was further investigated by growing inbred lines in 2 years, one of which was warmer and wetter. Inbred lines grown in the drier year accumulated up to 2-fold more hydrocarbons and up to a 22% higher relative abundance of alkenes. In summary, the surface hydrocarbon metabolome of silks is primarily governed by genotype and husk encasement status, with smaller impacts of environment and genotype-by-environment interactions. CONCLUSIONS: This study reveals that the composition of the cuticular hydrocarbon metabolome on silks is affected significantly by genetic factors, and is therefore amenable to dissection using quantitative genetic approaches. Such studies will clarify the genetic mechanisms responsible for the accumulation of these metabolites, enabling detailed functional investigations of the diverse and complex protective roles of silk surface lipids against environmental stresses.
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spelling pubmed-67963802019-10-21 Genetic and environmental variation impact the cuticular hydrocarbon metabolome on the stigmatic surfaces of maize Dennison, Tesia Qin, Wenmin Loneman, Derek M. Condon, Samson G. F. Lauter, Nick Nikolau, Basil J. Yandeau-Nelson, Marna D. BMC Plant Biol Research Article BACKGROUND: Simple non-isoprenoid hydrocarbons accumulate in discrete regions of the biosphere, including within bacteria and algae as a carbon and/or energy store, and the cuticles of plants and insects, where they may protect against environmental stresses. The extracellular cuticular surfaces of the stigmatic silks of maize are rich in linear hydrocarbons and therefore provide a convenient system to study the biological origins and functions of these unique metabolites. RESULTS: To test the hypotheses that genetics and environment influence the accumulation of surface hydrocarbons on silks and to examine the breadth of metabolome compositions across diverse germplasm, cuticular hydrocarbons were analyzed on husk-encased silks and silks that emerged from the husk leaves from 32 genetically diverse maize inbred lines, most of which are commonly utilized in genetics experiments. Total hydrocarbon accumulation varied ~ 10-fold among inbred lines, and up to 5-fold between emerged and husk-encased silks. Alkenes accounted for 5-60% of the total hydrocarbon metabolome, and the majority of alkenes were monoenes with a double bond at either the 7th or 9th carbon atom of the alkyl chain. Total hydrocarbon accumulation was impacted to similar degrees by genotype and husk encasement status, whereas genotype predominantly impacted alkene composition. Only minor differences in the metabolome were observed on silks that were emerged into the external environment for 3- versus 6-days. The environmental influence on the metabolome was further investigated by growing inbred lines in 2 years, one of which was warmer and wetter. Inbred lines grown in the drier year accumulated up to 2-fold more hydrocarbons and up to a 22% higher relative abundance of alkenes. In summary, the surface hydrocarbon metabolome of silks is primarily governed by genotype and husk encasement status, with smaller impacts of environment and genotype-by-environment interactions. CONCLUSIONS: This study reveals that the composition of the cuticular hydrocarbon metabolome on silks is affected significantly by genetic factors, and is therefore amenable to dissection using quantitative genetic approaches. Such studies will clarify the genetic mechanisms responsible for the accumulation of these metabolites, enabling detailed functional investigations of the diverse and complex protective roles of silk surface lipids against environmental stresses. BioMed Central 2019-10-17 /pmc/articles/PMC6796380/ /pubmed/31623561 http://dx.doi.org/10.1186/s12870-019-2040-3 Text en © The Author(s). 2019 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Dennison, Tesia
Qin, Wenmin
Loneman, Derek M.
Condon, Samson G. F.
Lauter, Nick
Nikolau, Basil J.
Yandeau-Nelson, Marna D.
Genetic and environmental variation impact the cuticular hydrocarbon metabolome on the stigmatic surfaces of maize
title Genetic and environmental variation impact the cuticular hydrocarbon metabolome on the stigmatic surfaces of maize
title_full Genetic and environmental variation impact the cuticular hydrocarbon metabolome on the stigmatic surfaces of maize
title_fullStr Genetic and environmental variation impact the cuticular hydrocarbon metabolome on the stigmatic surfaces of maize
title_full_unstemmed Genetic and environmental variation impact the cuticular hydrocarbon metabolome on the stigmatic surfaces of maize
title_short Genetic and environmental variation impact the cuticular hydrocarbon metabolome on the stigmatic surfaces of maize
title_sort genetic and environmental variation impact the cuticular hydrocarbon metabolome on the stigmatic surfaces of maize
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6796380/
https://www.ncbi.nlm.nih.gov/pubmed/31623561
http://dx.doi.org/10.1186/s12870-019-2040-3
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