Tomato-Pseudomonas syringae interactions under elevated CO2 concentration: the role of stomata

X, Li; Sun, Zaoyi; Shao, Shujun; Zhang, Shuai; Ahammed, Golam Jalal; Zhang, Guanqun; Jiang, Yuping; Zhou, Jie; Xia, Xiaojian; Zhou, Yanhong; Yu, Jingquan; Shi, Kai

doi:10.1093/jxb/eru420

Cited by 37 publications

(34 citation statements)

References 45 publications

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“…CAs are important enzymes in CO 2 metabolism and we addressed whether they play a role in atmospheric CO 2affected plant disease resistance. Previous reports have shown that elevated CO 2 increased the disease resistance of tomato plants against Pst (Li et al 2014;Zhang et al 2015). In contrast, we found enhanced disease susceptibility to P. syringae and increased resistance against B. cinerea in Arabidopsis plants grown at increasing CO 2 levels ( Fig.…”

Section: Discussioncontrasting

confidence: 45%

Carbonic anhydrases CA1 and CA4 function in atmospheric CO2-modulated disease resistance

Zhou

Vroegop-Vos

Dijken

et al. 2020

Planta

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Main conclusion Carbonic anhydrases CA1 and CA4 attenuate plant immunity and can contribute to altered disease resistance levels in response to changing atmospheric CO 2 conditions. Abstract β-Carbonic anhydrases (CAs) play an important role in CO 2 metabolism and plant development, but have also been implicated in plant immunity. Here we show that the bacterial pathogen Pseudomonas syringae and application of the microbe-associated molecular pattern (MAMP) flg22 repress CA1 and CA4 gene expression in Arabidopsis thaliana. Using the CA double-mutant ca1ca4, we provide evidence that CA1 and CA4 play an attenuating role in pathogen-and flg22triggered immune responses. In line with this, ca1ca4 plants exhibited enhanced resistance against P. syringae, which was accompanied by an increased expression of the defense-related genes FRK1 and ICS1. Under low atmospheric CO 2 conditions (150 ppm), when CA activity is typically low, the levels of CA1 transcription and resistance to P. syringae in wild-type Col-0 were similar to those observed in ca1ca4. However, under ambient (400 ppm) and elevated (800 ppm) atmospheric CO 2 conditions, CA1 transcription was enhanced and resistance to P. syringae reduced. Together, these results suggest that CA1 and CA4 attenuate plant immunity and that differential CA gene expression in response to changing atmospheric CO 2 conditions contribute to altered disease resistance levels. Keywords Arabidopsis • CO 2 metabolism • Defense signaling • Plant immunity • Pseudomonas syringae Abbreviations CA Carbonic anhydrase ET Ethylene JA Jasmonic acid MAMP Microbe-associated molecular pattern Pst Pseudomonas syringae pv. tomato DC3000 Psm Pseudomonas syringae pv. maculicola 4326 PTI Pattern-triggered immunity SA Salicylic acid Electronic supplementary material The online version of this article (

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Section: Discussioncontrasting

confidence: 45%

Carbonic anhydrases CA1 and CA4 function in atmospheric CO2-modulated disease resistance

Zhou

Vroegop-Vos

Dijken

et al. 2020

Planta

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“…This induction of stomatal closure is independent of ABA signaling (Montillet et al ., ). Based on these data and previous findings (Jin et al ., ; Li et al ., ), we conclude that CO 2 acts upstream of JA, and JA signaling is essential for stomatal closure under elevated CO 2 (Figure ).…”

Section: Discussionmentioning

confidence: 60%

Jasmonate‐mediated stomatal closure under elevated CO₂ revealed by time‐resolved metabolomics

et al. 2016

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Foliar stomatal movements are critical for regulating plant water loss and gas exchange. Elevated carbon dioxide (CO ) levels are known to induce stomatal closure. However, the current knowledge on CO signal transduction in stomatal guard cells is limited. Here we report metabolomic responses of Brassica napus guard cells to elevated CO using three hyphenated metabolomics platforms: gas chromatography-mass spectrometry (MS); liquid chromatography (LC)-multiple reaction monitoring-MS; and ultra-high-performance LC-quadrupole time-of-flight-MS. A total of 358 metabolites from guard cells were quantified in a time-course response to elevated CO level. Most metabolites increased under elevated CO , showing the most significant differences at 10 min. In addition, reactive oxygen species production increased and stomatal aperture decreased with time. Major alterations in flavonoid, organic acid, sugar, fatty acid, phenylpropanoid and amino acid metabolic pathways indicated changes in both primary and specialized metabolic pathways in guard cells. Most interestingly, the jasmonic acid (JA) biosynthesis pathway was significantly altered in the course of elevated CO treatment. Together with results obtained from JA biosynthesis and signaling mutants as well as CO signaling mutants, we discovered that CO -induced stomatal closure is mediated by JA signaling.

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“…The accumulation of H 2 O 2 in guard cells under elevated CO 2 was accompanied by an increase in NO accumulation in guard cells as well as upregulation of OST1 , NR and SLAC1 transcripts at both leaf and guard cell levels (Figs 2, 4, 5). As observed in a previous study (Li et al ., ), silencing NR abolished the elevated CO 2 ‐induced accumulation of NO in guard cells and stomatal closure. In this study, elevated CO 2 ‐induced stomatal closure could be blocked by either tungstate (an inhibitor of NR) or the NO scavenger cPTIO but not by L‐NAME/L‐NNA application (specific inhibitors of NO synthase) (Fig.…”

Section: Discussionmentioning

confidence: 91%

“…S3). These results together indicated that the NR was primarily responsible for the NO production in guard cells under elevated CO 2 conditions as observed in our earlier study (Li et al ., ). Interestingly, the elevated CO 2 ‐induced NO accumulation in guard cells seems to acts downstream of H 2 O 2 induction, as silencing of RBOH1 almost completely blocked elevated CO 2 ‐induced NR activation and NO induction (Figs ).…”

Section: Discussionmentioning

confidence: 97%

Guard cell hydrogen peroxide and nitric oxide mediate elevated CO₂‐induced stomatal movement in tomato

Shi

Zhang

et al. 2015

New Phytologist

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SummaryClimate change as a consequence of increasing atmospheric CO 2 influences plant photosynthesis and transpiration. Although the involvement of stomata in plant responses to elevated CO 2 has been well established, the underlying mechanism of elevated CO 2 -induced stomatal movement remains largely unknown.We used diverse techniques, including laser scanning confocal microscopy, transmission electron microscopy, biochemical methodologies and gene silencing to investigate the signaling pathway for elevated CO 2 -induced stomatal movement in tomato (Solanum lycopersicum).Elevated CO 2 -induced stomatal closure was dependent on the production of RESPIRATORY BURST OXIDASE 1 (RBOH1)-mediated hydrogen peroxide (H 2 O 2 ) and NITRATE REDUCTASE (NR)-mediated nitric oxide (NO) in guard cells in an abscisic acid (ABA)-independent manner. Silencing of OPEN STOMATA 1 (OST1) compromised the elevated CO 2 -induced accumulation of H 2 O 2 and NO, upregulation of SLOW ANION CHANNEL ASSOCIATED 1 (SLAC1) gene expression and reduction of stomatal aperture, whereas silencing of RBOH1 or NR had no effects on the expression of OST1.Our results demonstrate that as critical signaling molecules, RBOH1-dependent H 2 O 2 and NR-dependent NO act downstream of OST1 that regulate SLAC1 expression and elevated CO 2 -induced stomatal movement. This information is crucial to deepen the understanding of CO 2 signaling pathway in guard cells.

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Tomato-Pseudomonas syringae interactions under elevated CO2 concentration: the role of stomata

Abstract: SummaryElevated CO2 enhanced defence against Pseudomonas syringae in tomato plants, not only by reducing stomata-mediated entry of P. syringae but also by invoking a stomata-independent pathway to counteract P. syringae.

Cited by 37 publications

References 45 publications

Carbonic anhydrases CA1 and CA4 function in atmospheric CO2-modulated disease resistance

Carbonic anhydrases CA1 and CA4 function in atmospheric CO2-modulated disease resistance

Jasmonate‐mediated stomatal closure under elevated CO₂ revealed by time‐resolved metabolomics

Guard cell hydrogen peroxide and nitric oxide mediate elevated CO₂‐induced stomatal movement in tomato

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Tomato-Pseudomonas syringae interactions under elevated CO2 concentration: the role of stomata

Abstract: SummaryElevated CO2 enhanced defence against Pseudomonas syringae in tomato plants, not only by reducing stomata-mediated entry of P. syringae but also by invoking a stomata-independent pathway to counteract P. syringae.

Cited by 37 publications

References 45 publications

Carbonic anhydrases CA1 and CA4 function in atmospheric CO2-modulated disease resistance

Carbonic anhydrases CA1 and CA4 function in atmospheric CO2-modulated disease resistance

Jasmonate‐mediated stomatal closure under elevated CO2 revealed by time‐resolved metabolomics

Guard cell hydrogen peroxide and nitric oxide mediate elevated CO2‐induced stomatal movement in tomato

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Product

Resources

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Jasmonate‐mediated stomatal closure under elevated CO₂ revealed by time‐resolved metabolomics

Guard cell hydrogen peroxide and nitric oxide mediate elevated CO₂‐induced stomatal movement in tomato