Lipid Signaling Requires ROS Production to Elicit Actin Cytoskeleton Remodeling during Plant Innate Immunity
In terrestrial plants a basal innate immune system, pattern-triggered immunity (PTI), has evolved to limit infection by diverse microbes. The remodeling of actin cytoskeletal arrays is now recognized as a key hallmark event during the rapid host cellular responses to pathogen attack. Several actin b...
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| Format: | Article |
| Language: | English |
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MDPI AG
2022-02-01
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| Series: | International Journal of Molecular Sciences |
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| Online Access: | https://www.mdpi.com/1422-0067/23/5/2447 |
| _version_ | 1797474996185989120 |
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| author | Lingyan Cao Wenyi Wang Weiwei Zhang Christopher J. Staiger |
| author_facet | Lingyan Cao Wenyi Wang Weiwei Zhang Christopher J. Staiger |
| author_sort | Lingyan Cao |
| collection | DOAJ |
| description | In terrestrial plants a basal innate immune system, pattern-triggered immunity (PTI), has evolved to limit infection by diverse microbes. The remodeling of actin cytoskeletal arrays is now recognized as a key hallmark event during the rapid host cellular responses to pathogen attack. Several actin binding proteins have been demonstrated to fine tune the dynamics of actin filaments during this process. However, the upstream signals that stimulate actin remodeling during PTI signaling remain poorly characterized. Two second messengers, reactive oxygen species (ROS) and phosphatidic acid (PA), are elevated following pathogen perception or microbe-associated molecular pattern (MAMP) treatment, and the timing of signaling fluxes roughly correlates with actin cytoskeletal rearrangements. Here, we combined genetic analysis, chemical complementation experiments, and quantitative live-cell imaging experiments to test the role of these second messengers in actin remodeling and to order the signaling events during plant immunity. We demonstrated that PHOSPHOLIPASE Dβ (PLDβ) isoforms are necessary to elicit actin accumulation in response to flg22-associated PTI. Further, bacterial growth experiments and MAMP-induced apoplastic ROS production measurements revealed that PLDβ-generated PA acts upstream of ROS signaling to trigger actin remodeling through inhibition of CAPPING PROTEIN (CP) activity. Collectively, our results provide compelling evidence that PLDβ/PA functions upstream of RBOHD-mediated ROS production to elicit actin rearrangements during the innate immune response in <i>Arabidopsis</i>. |
| first_indexed | 2024-03-09T20:38:52Z |
| format | Article |
| id | doaj.art-65cc2ae6cf1540ba9438c8bef7414045 |
| institution | Directory Open Access Journal |
| issn | 1661-6596 1422-0067 |
| language | English |
| last_indexed | 2024-03-09T20:38:52Z |
| publishDate | 2022-02-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | International Journal of Molecular Sciences |
| spelling | doaj.art-65cc2ae6cf1540ba9438c8bef74140452023-11-23T23:04:07ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672022-02-01235244710.3390/ijms23052447Lipid Signaling Requires ROS Production to Elicit Actin Cytoskeleton Remodeling during Plant Innate ImmunityLingyan Cao0Wenyi Wang1Weiwei Zhang2Christopher J. Staiger3Department of Biological Sciences, Purdue University, West Lafayette, IN 47907, USADepartment of Botany and Plant Pathology, Purdue University, West Lafayette, IN 47907, USADepartment of Biological Sciences, Purdue University, West Lafayette, IN 47907, USADepartment of Biological Sciences, Purdue University, West Lafayette, IN 47907, USAIn terrestrial plants a basal innate immune system, pattern-triggered immunity (PTI), has evolved to limit infection by diverse microbes. The remodeling of actin cytoskeletal arrays is now recognized as a key hallmark event during the rapid host cellular responses to pathogen attack. Several actin binding proteins have been demonstrated to fine tune the dynamics of actin filaments during this process. However, the upstream signals that stimulate actin remodeling during PTI signaling remain poorly characterized. Two second messengers, reactive oxygen species (ROS) and phosphatidic acid (PA), are elevated following pathogen perception or microbe-associated molecular pattern (MAMP) treatment, and the timing of signaling fluxes roughly correlates with actin cytoskeletal rearrangements. Here, we combined genetic analysis, chemical complementation experiments, and quantitative live-cell imaging experiments to test the role of these second messengers in actin remodeling and to order the signaling events during plant immunity. We demonstrated that PHOSPHOLIPASE Dβ (PLDβ) isoforms are necessary to elicit actin accumulation in response to flg22-associated PTI. Further, bacterial growth experiments and MAMP-induced apoplastic ROS production measurements revealed that PLDβ-generated PA acts upstream of ROS signaling to trigger actin remodeling through inhibition of CAPPING PROTEIN (CP) activity. Collectively, our results provide compelling evidence that PLDβ/PA functions upstream of RBOHD-mediated ROS production to elicit actin rearrangements during the innate immune response in <i>Arabidopsis</i>.https://www.mdpi.com/1422-0067/23/5/2447actin cytoskeletonpattern-triggered immunity (PTI)phospholipase D (PLD)phosphatidic acid (PA)reactive oxygen species (ROS) |
| spellingShingle | Lingyan Cao Wenyi Wang Weiwei Zhang Christopher J. Staiger Lipid Signaling Requires ROS Production to Elicit Actin Cytoskeleton Remodeling during Plant Innate Immunity International Journal of Molecular Sciences actin cytoskeleton pattern-triggered immunity (PTI) phospholipase D (PLD) phosphatidic acid (PA) reactive oxygen species (ROS) |
| title | Lipid Signaling Requires ROS Production to Elicit Actin Cytoskeleton Remodeling during Plant Innate Immunity |
| title_full | Lipid Signaling Requires ROS Production to Elicit Actin Cytoskeleton Remodeling during Plant Innate Immunity |
| title_fullStr | Lipid Signaling Requires ROS Production to Elicit Actin Cytoskeleton Remodeling during Plant Innate Immunity |
| title_full_unstemmed | Lipid Signaling Requires ROS Production to Elicit Actin Cytoskeleton Remodeling during Plant Innate Immunity |
| title_short | Lipid Signaling Requires ROS Production to Elicit Actin Cytoskeleton Remodeling during Plant Innate Immunity |
| title_sort | lipid signaling requires ros production to elicit actin cytoskeleton remodeling during plant innate immunity |
| topic | actin cytoskeleton pattern-triggered immunity (PTI) phospholipase D (PLD) phosphatidic acid (PA) reactive oxygen species (ROS) |
| url | https://www.mdpi.com/1422-0067/23/5/2447 |
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