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Title: Temporal Dynamics of Growth and Photosynthesis Suppression in Response to Jasmonate Signaling

Abstract

Biotic stress constrains plant productivity in natural and agricultural ecosystems. Repression of photosynthetic genes is a conserved plant response to biotic attack, but how this transcriptional reprogramming is linked to changes in photosynthesis and the transition from growth- to defense-oriented metabolism is poorly understood. Here, we used a combination of noninvasive chlorophyll fluorescence imaging technology and RNA sequencing to determine the effect of the defense hormone jasmonate (JA) on the growth, photosynthetic efficiency, and gene expression of Arabidopsis (Arabidopsis thaliana) rosette leaves. High temporal resolution was achieved through treatment with coronatine (COR), a high-affinity agonist of the JA receptor. We show that leaf growth is rapidly arrested after COR treatment and that this effect is tightly correlated with changes in the expression of genes involved in growth, photosynthesis, and defense. Rapid COR-induced expression of defense genes occurred concomitantly with the repression of photosynthetic genes but was not associated with a reduced quantum efficiency of photosystem II. These findings support the view that photosynthetic capacity is maintained during the period in which stress-induced JA signaling redirects metabolism from growth to defense. Chlorophyll fluorescence images captured in a multiscale time series, however, revealed a transient COR-induced decrease in quantum efficiency of photosystemmore » II at dawn of the day after treatment. Physiological studies suggest that this response results from delayed stomatal opening at the nightday transition. These collective results establish a high-resolution temporal view of how a major stress response pathway modulates plant growth and photosynthesis and highlight the utility of chlorophyll fluorescence imaging for revealing transient stress-induced perturbations in photosynthetic performance.« less

Authors:
 [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1]
  1. Michigan State Univ., East Lansing, MI (United States)
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)
OSTI Identifier:
1602540
Grant/Contract Number:  
FG02-91ER20021
Resource Type:
Accepted Manuscript
Journal Name:
Plant Physiology (Bethesda)
Additional Journal Information:
Journal Name: Plant Physiology (Bethesda); Journal Volume: 165; Journal Issue: 3; 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

Attaran, Elham, Major, Ian T., Cruz, Jeffrey A., Rosa, Bruce A., Koo, Abraham J. K., Chen, Jin, Kramer, David M., He, Sheng Yang, and Howe, Gregg A. Temporal Dynamics of Growth and Photosynthesis Suppression in Response to Jasmonate Signaling. United States: N. p., 2014. Web. doi:10.1104/pp.114.239004.
Attaran, Elham, Major, Ian T., Cruz, Jeffrey A., Rosa, Bruce A., Koo, Abraham J. K., Chen, Jin, Kramer, David M., He, Sheng Yang, & Howe, Gregg A. Temporal Dynamics of Growth and Photosynthesis Suppression in Response to Jasmonate Signaling. United States. https://doi.org/10.1104/pp.114.239004
Attaran, Elham, Major, Ian T., Cruz, Jeffrey A., Rosa, Bruce A., Koo, Abraham J. K., Chen, Jin, Kramer, David M., He, Sheng Yang, and Howe, Gregg A. Mon . "Temporal Dynamics of Growth and Photosynthesis Suppression in Response to Jasmonate Signaling". United States. https://doi.org/10.1104/pp.114.239004. https://www.osti.gov/servlets/purl/1602540.
@article{osti_1602540,
title = {Temporal Dynamics of Growth and Photosynthesis Suppression in Response to Jasmonate Signaling},
author = {Attaran, Elham and Major, Ian T. and Cruz, Jeffrey A. and Rosa, Bruce A. and Koo, Abraham J. K. and Chen, Jin and Kramer, David M. and He, Sheng Yang and Howe, Gregg A.},
abstractNote = {Biotic stress constrains plant productivity in natural and agricultural ecosystems. Repression of photosynthetic genes is a conserved plant response to biotic attack, but how this transcriptional reprogramming is linked to changes in photosynthesis and the transition from growth- to defense-oriented metabolism is poorly understood. Here, we used a combination of noninvasive chlorophyll fluorescence imaging technology and RNA sequencing to determine the effect of the defense hormone jasmonate (JA) on the growth, photosynthetic efficiency, and gene expression of Arabidopsis (Arabidopsis thaliana) rosette leaves. High temporal resolution was achieved through treatment with coronatine (COR), a high-affinity agonist of the JA receptor. We show that leaf growth is rapidly arrested after COR treatment and that this effect is tightly correlated with changes in the expression of genes involved in growth, photosynthesis, and defense. Rapid COR-induced expression of defense genes occurred concomitantly with the repression of photosynthetic genes but was not associated with a reduced quantum efficiency of photosystem II. These findings support the view that photosynthetic capacity is maintained during the period in which stress-induced JA signaling redirects metabolism from growth to defense. Chlorophyll fluorescence images captured in a multiscale time series, however, revealed a transient COR-induced decrease in quantum efficiency of photosystem II at dawn of the day after treatment. Physiological studies suggest that this response results from delayed stomatal opening at the nightday transition. These collective results establish a high-resolution temporal view of how a major stress response pathway modulates plant growth and photosynthesis and highlight the utility of chlorophyll fluorescence imaging for revealing transient stress-induced perturbations in photosynthetic performance.},
doi = {10.1104/pp.114.239004},
journal = {Plant Physiology (Bethesda)},
number = 3,
volume = 165,
place = {United States},
year = {Mon May 12 00:00:00 EDT 2014},
month = {Mon May 12 00:00:00 EDT 2014}
}

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Rapid defense responses in maize leaves induced by Spodoptera exigua caterpillar feeding
journal, July 2017

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  • Journal of Experimental Botany, Vol. 68, Issue 16
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Architecture and dynamics of the jasmonic acid gene regulatory network
journal, December 2016

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  • The Plant Cell
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Combining Digital Imaging and Genome Wide Association Mapping to Dissect Uncharacterized Traits in Plant/Pathogen Interactions
posted_content, April 2018

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Cytokinin levels and signaling respond to wounding and the perception of herbivore elicitors in Nicotiana attenuata
journal, August 2014

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AtRTP5 negatively regulates plant resistance to Phytophthora pathogens by modulating the biosynthesis of endogenous jasmonic acid and salicylic acid
journal, November 2019

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A plant's balance of growth and defense - revisited
journal, August 2017


Effects of sugarcane aphid herbivory on transcriptional responses of resistant and susceptible sorghum
journal, October 2018


Specific pools of endogenous peptides are present in gametophore, protonema, and protoplast cells of the moss Physcomitrella patens
journal, January 2015

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Development of a visible marker trait based on leaf sheath–specific anthocyanin pigmentation applicable to various genotypes in rice
journal, January 2019

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Methyl Jasmonate Regulates Antioxidant Defense and Suppresses Arsenic Uptake in Brassica napus L.
journal, April 2016

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Identification of Two bZIP Transcription Factors Interacting with the Promoter of Soybean Rubisco Activase Gene (GmRCAα)
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Limitation of Grassland Productivity by Low Temperature and Seasonality of Growth
journal, July 2016


The Role of Light–Dark Regulation of the Chloroplast ATP Synthase
journal, July 2017

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Current Understanding of the Interplay between Phytohormones and Photosynthesis under Environmental Stress
journal, August 2015

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Chloroplasts at the Crossroad of Photosynthesis, Pathogen Infection and Plant Defense
journal, December 2018

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Evaluation of Disease Severity and Global Transcriptome Response Induced by Citrus bark cracking viroid, Hop latent viroid, and Their Co-Infection in Hop (Humulus lupulus L.)
journal, June 2019

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Role of Stomatal Conductance in Modifying the Dose Response of Stress-Volatile Emissions in Methyl Jasmonate Treated Leaves of Cucumber (Cucumis Sativa)
journal, February 2020

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