Abstract
Microbial volatile compounds (mVCs) may cause stomatal closure to limit pathogen invasion as part of plant innate immune response. However, the mechanisms of mVC-induced stomatal closure remain unclear. In this study, we co-cultured Enterobacter aerogenes with Arabidopsis (Arabidopsis thaliana) seedlings without direct contact to initiate stomatal closure. Experiments using the reactive oxygen species (ROS)-sensitive fluorescent dye, H2DCF-DA, showed that mVCs from E. aerogenes enhanced ROS production in guard cells of wild-type plants. The involvement of ROS in stomatal closure was then demonstrated in an ROS production mutant (rbohD). In addition, we identified two stages of signal transduction during E. aerogenes VC-induced stomatal closure by comparing the response of wild-type Arabidopsis with a panel of mutants. In the early stage (3 h exposure), E. aerogenes VCs induced stomatal closure in wild-type and receptor-like kinase THESEUS1 mutant (the1-1) but not in rbohD, plant hormone-related mutants (nced3, erf4, jar1-1), or MAPK kinase mutants (mkk1 and mkk3). However, in the late stage (24 h exposure), E. aerogenes VCs induced stomatal closure in wild-type and rbohD but not in nced3, erf4, jar1-1, the1-1, mkk1 or mkk3. Taken together, our results suggest that E. aerogenes mVC-induced plant immune responses modulate stomatal closure in Arabidopsis by a multi-phase mechanism.
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Abbreviations
- ABA:
-
Abscisic acid
- COR:
-
Phytotoxin coronatine
- CWI:
-
Cell wall integrity
- EaVCs:
-
E. aerogenes Volatile compounds
- ERF4:
-
Ethylene-responsive factor 4
- ETI:
-
Effector-triggered immunity
- H2DCF-DA:
-
2,7-Dichlorofluorescein diacetate
- JAR1:
-
Jasmonic acid resistant1
- MAPKs:
-
Mitogen-activated protein kinases
- MKK1/MKK3:
-
MAPK kinases MKK1/MKK3
- mVCs:
-
Microbial volatile compounds
- NCED3:
-
9-Cis-epoxycarotenoid dioxygenase 3
- OST1:
-
OPEN STOMATA 1
- PAMPs/MAMPs:
-
Pathogen/microbe-associated molecular patterns
- PP2C:
-
Protein phosphatase 2C
- PRRs:
-
Pattern recognition receptors
- PstDC3000:
-
Pseudomonas syringae Pv. Tomato DC3000
- PTI:
-
Pattern-triggered immunity
- RBOH:
-
Respiratory burst oxidase homolog
- RLKs:
-
Receptor-like protein kinases
- ROS:
-
Reactive oxygen species
- THE1:
-
Receptor-like kinase THESEUS1
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Acknowledgements
We are grateful to Dr. Hsu-Liang Hsieh for the gift of jar1-1 seeds, and Dr. Heribert Hirt for the gift of mkk1 and mkk3 seeds. We also thank Dr. Marcus Calkins for English editing.
Funding
This work was supported by the Ministry of Science and Technology, Taiwan (MOST-110-2321-B-006-007-, MOST-109-2621-B-006-002-, MOST-109-2313-B-006-008-, MOST-108-2313-B-006-002-); Higher Education Sprout Project from Ministry of Education of the Headquarters of University Advancement at National Cheng Kung University (NCKU); NCKU Distinguished International Student Scholarship for Graduate Students; Shanghai scholarship, Taiwan; NCKU Butterfly-ASEAN Scholarship which supplied by Chen-Yung Memorial Foundation, Inc.; and Sinopac bank scholarship, Taiwan.
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TTTT (first author) performed experiments, analyzed data and wrote the first draft of the manuscript; CCC wrote and revised the manuscript; JYC and PYS performed experiments; TM, RHL, NNT, CHC and TPN provided ideas to revise the manuscript; HJH (corresponding author) conceived, organized and oversaw the entire work.
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Truong, TT.T., Chiu, CC., Chen, JY. et al. Uncovering molecular mechanisms involved in microbial volatile compounds-induced stomatal closure in Arabidopsis thaliana. Plant Mol Biol 113, 143–155 (2023). https://doi.org/10.1007/s11103-023-01379-9
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DOI: https://doi.org/10.1007/s11103-023-01379-9