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Constitutively elevated salicylic acid levels alter photosynthesis and oxidative state but not growth in transgenic populus.

Identifieur interne : 002748 ( Main/Exploration ); précédent : 002747; suivant : 002749

Constitutively elevated salicylic acid levels alter photosynthesis and oxidative state but not growth in transgenic populus.

Auteurs : Liang-Jiao Xue [États-Unis] ; Wenbing Guo ; Yinan Yuan ; Edward O. Anino ; Batbayar Nyamdari ; Mark C. Wilson ; Christopher J. Frost ; Han-Yi Chen ; Benjamin A. Babst ; Scott A. Harding ; Chung-Jui Tsai

Source :

RBID : pubmed:23903318

Descripteurs français

English descriptors

Abstract

Salicylic acid (SA) has long been implicated in plant responses to oxidative stress. SA overproduction in Arabidopsis thaliana leads to dwarfism, making in planta assessment of SA effects difficult in this model system. We report that transgenic Populus tremula × alba expressing a bacterial SA synthase hyperaccumulated SA and SA conjugates without negative growth consequences. In the absence of stress, endogenously elevated SA elicited widespread metabolic and transcriptional changes that resembled those of wild-type plants exposed to oxidative stress-promoting heat treatments. Potential signaling and oxidative stress markers azelaic and gluconic acids as well as antioxidant chlorogenic acids were strongly coregulated with SA, while soluble sugars and other phenylpropanoids were inversely correlated. Photosynthetic responses to heat were attenuated in SA-overproducing plants. Network analysis identified potential drivers of SA-mediated transcriptome rewiring, including receptor-like kinases and WRKY transcription factors. Orthologs of Arabidopsis SA signaling components NON-EXPRESSOR OF PATHOGENESIS-RELATED GENES1 and thioredoxins were not represented. However, all members of the expanded Populus nucleoredoxin-1 family exhibited increased expression and increased network connectivity in SA-overproducing Populus, suggesting a previously undescribed role in SA-mediated redox regulation. The SA response in Populus involved a reprogramming of carbon uptake and partitioning during stress that is compatible with constitutive chemical defense and sustained growth, contrasting with the SA response in Arabidopsis, which is transient and compromises growth if sustained.

DOI: 10.1105/tpc.113.112839
PubMed: 23903318
PubMed Central: PMC3753393


Affiliations:


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Le document en format XML

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<term>Bacterial Proteins (metabolism)</term>
<term>Gene Expression Regulation, Developmental (MeSH)</term>
<term>Gene Expression Regulation, Plant (MeSH)</term>
<term>Gene Ontology (MeSH)</term>
<term>Gene Regulatory Networks (MeSH)</term>
<term>Hot Temperature (MeSH)</term>
<term>Lyases (genetics)</term>
<term>Lyases (metabolism)</term>
<term>Nuclear Proteins (genetics)</term>
<term>Nuclear Proteins (metabolism)</term>
<term>Oligonucleotide Array Sequence Analysis (MeSH)</term>
<term>Oxidation-Reduction (MeSH)</term>
<term>Oxidoreductases (genetics)</term>
<term>Oxidoreductases (metabolism)</term>
<term>Photosynthesis (MeSH)</term>
<term>Plant Leaves (genetics)</term>
<term>Plant Leaves (growth & development)</term>
<term>Plant Leaves (metabolism)</term>
<term>Plant Proteins (genetics)</term>
<term>Plant Proteins (metabolism)</term>
<term>Plants, Genetically Modified (MeSH)</term>
<term>Populus (genetics)</term>
<term>Populus (growth & development)</term>
<term>Populus (metabolism)</term>
<term>Reverse Transcriptase Polymerase Chain Reaction (MeSH)</term>
<term>Salicylic Acid (metabolism)</term>
<term>Signal Transduction (genetics)</term>
<term>Transcriptome (MeSH)</term>
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<term>Acide salicylique (métabolisme)</term>
<term>Feuilles de plante (croissance et développement)</term>
<term>Feuilles de plante (génétique)</term>
<term>Feuilles de plante (métabolisme)</term>
<term>Gene Ontology (MeSH)</term>
<term>Lyases (génétique)</term>
<term>Lyases (métabolisme)</term>
<term>Oxidoreductases (génétique)</term>
<term>Oxidoreductases (métabolisme)</term>
<term>Oxydoréduction (MeSH)</term>
<term>Photosynthèse (MeSH)</term>
<term>Populus (croissance et développement)</term>
<term>Populus (génétique)</term>
<term>Populus (métabolisme)</term>
<term>Protéines bactériennes (génétique)</term>
<term>Protéines bactériennes (métabolisme)</term>
<term>Protéines nucléaires (génétique)</term>
<term>Protéines nucléaires (métabolisme)</term>
<term>Protéines végétales (génétique)</term>
<term>Protéines végétales (métabolisme)</term>
<term>RT-PCR (MeSH)</term>
<term>Régulation de l'expression des gènes au cours du développement (MeSH)</term>
<term>Régulation de l'expression des gènes végétaux (MeSH)</term>
<term>Réseaux de régulation génique (MeSH)</term>
<term>Séquençage par oligonucléotides en batterie (MeSH)</term>
<term>Température élevée (MeSH)</term>
<term>Transcriptome (MeSH)</term>
<term>Transduction du signal (génétique)</term>
<term>Végétaux génétiquement modifiés (MeSH)</term>
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<term>Lyases</term>
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<term>Lyases</term>
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<term>Populus</term>
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<term>Populus</term>
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<term>Populus</term>
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<term>Lyases</term>
<term>Oxidoreductases</term>
<term>Populus</term>
<term>Protéines bactériennes</term>
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<term>Transduction du signal</term>
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<term>Plant Leaves</term>
<term>Populus</term>
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<term>Acide salicylique</term>
<term>Feuilles de plante</term>
<term>Lyases</term>
<term>Oxidoreductases</term>
<term>Populus</term>
<term>Protéines bactériennes</term>
<term>Protéines nucléaires</term>
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<term>Hot Temperature</term>
<term>Oligonucleotide Array Sequence Analysis</term>
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<term>Oxydoréduction</term>
<term>Photosynthèse</term>
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<term>Régulation de l'expression des gènes au cours du développement</term>
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<term>Séquençage par oligonucléotides en batterie</term>
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<div type="abstract" xml:lang="en">Salicylic acid (SA) has long been implicated in plant responses to oxidative stress. SA overproduction in Arabidopsis thaliana leads to dwarfism, making in planta assessment of SA effects difficult in this model system. We report that transgenic Populus tremula × alba expressing a bacterial SA synthase hyperaccumulated SA and SA conjugates without negative growth consequences. In the absence of stress, endogenously elevated SA elicited widespread metabolic and transcriptional changes that resembled those of wild-type plants exposed to oxidative stress-promoting heat treatments. Potential signaling and oxidative stress markers azelaic and gluconic acids as well as antioxidant chlorogenic acids were strongly coregulated with SA, while soluble sugars and other phenylpropanoids were inversely correlated. Photosynthetic responses to heat were attenuated in SA-overproducing plants. Network analysis identified potential drivers of SA-mediated transcriptome rewiring, including receptor-like kinases and WRKY transcription factors. Orthologs of Arabidopsis SA signaling components NON-EXPRESSOR OF PATHOGENESIS-RELATED GENES1 and thioredoxins were not represented. However, all members of the expanded Populus nucleoredoxin-1 family exhibited increased expression and increased network connectivity in SA-overproducing Populus, suggesting a previously undescribed role in SA-mediated redox regulation. The SA response in Populus involved a reprogramming of carbon uptake and partitioning during stress that is compatible with constitutive chemical defense and sustained growth, contrasting with the SA response in Arabidopsis, which is transient and compromises growth if sustained. </div>
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<AbstractText>Salicylic acid (SA) has long been implicated in plant responses to oxidative stress. SA overproduction in Arabidopsis thaliana leads to dwarfism, making in planta assessment of SA effects difficult in this model system. We report that transgenic Populus tremula × alba expressing a bacterial SA synthase hyperaccumulated SA and SA conjugates without negative growth consequences. In the absence of stress, endogenously elevated SA elicited widespread metabolic and transcriptional changes that resembled those of wild-type plants exposed to oxidative stress-promoting heat treatments. Potential signaling and oxidative stress markers azelaic and gluconic acids as well as antioxidant chlorogenic acids were strongly coregulated with SA, while soluble sugars and other phenylpropanoids were inversely correlated. Photosynthetic responses to heat were attenuated in SA-overproducing plants. Network analysis identified potential drivers of SA-mediated transcriptome rewiring, including receptor-like kinases and WRKY transcription factors. Orthologs of Arabidopsis SA signaling components NON-EXPRESSOR OF PATHOGENESIS-RELATED GENES1 and thioredoxins were not represented. However, all members of the expanded Populus nucleoredoxin-1 family exhibited increased expression and increased network connectivity in SA-overproducing Populus, suggesting a previously undescribed role in SA-mediated redox regulation. The SA response in Populus involved a reprogramming of carbon uptake and partitioning during stress that is compatible with constitutive chemical defense and sustained growth, contrasting with the SA response in Arabidopsis, which is transient and compromises growth if sustained. </AbstractText>
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