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Title: Isoprene Acts as a Signaling Molecule in Gene Networks Important for Stress Responses and Plant Growth

Abstract

Isoprene synthase converts dimethylallyl diphosphate to isoprene and appears to be necessary and sufficient to allow plants to emit isoprene at significant rates. Isoprene can protect plants from abiotic stress but is not produced naturally by all plants; for example, Arabidopsis (Arabidopsis thaliana) and tobacco (Nicotiana tabacum) do not produce isoprene. It is typically present at very low concentrations, suggesting a role as a signaling molecule; however, its exact physiological role and mechanism of action are not fully understood. We transformed Arabidopsis with a Eucalyptus globulus isoprene synthase. The regulatory mechanisms of photosynthesis and isoprene emission were similar to those of native emitters, indicating that regulation of isoprene emission is not specific to isoprene-emitting species. Leaf chlorophyll and carotenoid contents were enhanced by isoprene, which also had a marked positive effect on hypocotyl, cotyledon, leaf, and inflorescence growth in Arabidopsis. By contrast, leaf and stem growth was reduced in tobacco engineered to emit isoprene. Expression of genes belonging to signaling networks or associated with specific growth regulators (e.g. gibberellic acid that promotes growth and jasmonic acid that promotes defense) and genes that lead to stress tolerance was altered by isoprene emission. Isoprene likely executes its effects on growth and stressmore » tolerance through direct regulation of gene expression. Enhancement of jasmonic acid-mediated defense signaling by isoprene may trigger a growth-defense tradeoff leading to variations in the growth response. Our data support a role for isoprene as a signaling molecule.« less

Authors:
ORCiD logo [1]; ORCiD logo [2];  [3];  [3];  [4]; ORCiD logo [5];  [5]; ORCiD logo [6]
  1. School of Forestry and Biotechnology, Zhejiang Agriculture and Forestry University, Lin’an 311300, China; Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, Michigan 48824
  2. MSU-DOE Plant Research Laboratory, Michigan State University, East Lansing, Michigan 48824; Plant Resilience Institute, Michigan State University, East Lansing, Michigan 48824
  3. Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, Michigan 48824
  4. MSU-DOE Plant Research Laboratory, Michigan State University, East Lansing, Michigan 48824
  5. Department of Plant Biology, Michigan State University, East Lansing, Michigan 48824
  6. Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, Michigan 48824; MSU-DOE Plant Research Laboratory, Michigan State University, East Lansing, Michigan 48824; Plant Resilience Institute, Michigan State University, East Lansing, Michigan 48824
Publication Date:
Research Org.:
Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Laboratory
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences, and Biosciences Division
OSTI Identifier:
1494767
Alternate Identifier(s):
OSTI ID: 1607926
Grant/Contract Number:  
FG02-91ER 20021; FG02-91ER20021
Resource Type:
Published Article
Journal Name:
Plant Physiology (Bethesda)
Additional Journal Information:
Journal Name: Plant Physiology (Bethesda) Journal Volume: 180 Journal Issue: 1; Journal ID: ISSN 0032-0889
Publisher:
American Society of Plant Biologists
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Zuo, Zhaojiang, Weraduwage, Sarathi M., Lantz, Alexandra T., Sanchez, Lydia M., Weise, Sean E., Wang, Jie, Childs, Kevin L., and Sharkey, Thomas D. Isoprene Acts as a Signaling Molecule in Gene Networks Important for Stress Responses and Plant Growth. United States: N. p., 2019. Web. doi:10.1104/pp.18.01391.
Zuo, Zhaojiang, Weraduwage, Sarathi M., Lantz, Alexandra T., Sanchez, Lydia M., Weise, Sean E., Wang, Jie, Childs, Kevin L., & Sharkey, Thomas D. Isoprene Acts as a Signaling Molecule in Gene Networks Important for Stress Responses and Plant Growth. United States. https://doi.org/10.1104/pp.18.01391
Zuo, Zhaojiang, Weraduwage, Sarathi M., Lantz, Alexandra T., Sanchez, Lydia M., Weise, Sean E., Wang, Jie, Childs, Kevin L., and Sharkey, Thomas D. Wed . "Isoprene Acts as a Signaling Molecule in Gene Networks Important for Stress Responses and Plant Growth". United States. https://doi.org/10.1104/pp.18.01391.
@article{osti_1494767,
title = {Isoprene Acts as a Signaling Molecule in Gene Networks Important for Stress Responses and Plant Growth},
author = {Zuo, Zhaojiang and Weraduwage, Sarathi M. and Lantz, Alexandra T. and Sanchez, Lydia M. and Weise, Sean E. and Wang, Jie and Childs, Kevin L. and Sharkey, Thomas D.},
abstractNote = {Isoprene synthase converts dimethylallyl diphosphate to isoprene and appears to be necessary and sufficient to allow plants to emit isoprene at significant rates. Isoprene can protect plants from abiotic stress but is not produced naturally by all plants; for example, Arabidopsis (Arabidopsis thaliana) and tobacco (Nicotiana tabacum) do not produce isoprene. It is typically present at very low concentrations, suggesting a role as a signaling molecule; however, its exact physiological role and mechanism of action are not fully understood. We transformed Arabidopsis with a Eucalyptus globulus isoprene synthase. The regulatory mechanisms of photosynthesis and isoprene emission were similar to those of native emitters, indicating that regulation of isoprene emission is not specific to isoprene-emitting species. Leaf chlorophyll and carotenoid contents were enhanced by isoprene, which also had a marked positive effect on hypocotyl, cotyledon, leaf, and inflorescence growth in Arabidopsis. By contrast, leaf and stem growth was reduced in tobacco engineered to emit isoprene. Expression of genes belonging to signaling networks or associated with specific growth regulators (e.g. gibberellic acid that promotes growth and jasmonic acid that promotes defense) and genes that lead to stress tolerance was altered by isoprene emission. Isoprene likely executes its effects on growth and stress tolerance through direct regulation of gene expression. Enhancement of jasmonic acid-mediated defense signaling by isoprene may trigger a growth-defense tradeoff leading to variations in the growth response. Our data support a role for isoprene as a signaling molecule.},
doi = {10.1104/pp.18.01391},
journal = {Plant Physiology (Bethesda)},
number = 1,
volume = 180,
place = {United States},
year = {Wed Feb 13 00:00:00 EST 2019},
month = {Wed Feb 13 00:00:00 EST 2019}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1104/pp.18.01391

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