Broad-spectrum resistance gene RPW8.1 balances immunity and growth via feedback regulation of WRKYs
© 2023 The Authors. Plant Biotechnology Journal published by Society for Experimental Biology and The Association of Applied Biologists and John Wiley & Sons Ltd..
Arabidopsis RESISTANCE TO POWDERY MILDEW 8.1 (RPW8.1) is an important tool for engineering broad-spectrum disease resistance against multiple pathogens. Ectopic expression of RPW8.1 leads to enhanced disease resistance with cell death at leaves and compromised plant growth, implying a regulatory mechanism balancing RPW8.1-mediated resistance and growth. Here, we show that RPW8.1 constitutively enhances the expression of transcription factor WRKY51 and activates salicylic acid and ethylene signalling pathways; WRKY51 in turn suppresses RPW8.1 expression, forming a feedback regulation loop. RPW8.1 and WRKY51 are both induced by pathogen infection and pathogen-/microbe-associated molecular patterns. In ectopic expression of RPW8.1 background (R1Y4), overexpression of WRKY51 not only rescues the growth suppression and cell death caused by RPW8.1, but also suppresses RPW8.1-mediated broad-spectrum disease resistance and pattern-triggered immunity. Mechanistically, WRKY51 directly binds to and represses RPW8.1 promoter, thus limiting the expression amplitude of RPW8.1. Moreover, WRKY6, WRKY28 and WRKY41 play a role redundant to WRKY51 in the suppression of RPW8.1 expression and are constitutively upregulated in R1Y4 plants with WRKY51 being knocked out (wrky51 R1Y4) plants. Notably, WRKY51 has no significant effects on disease resistance or plant growth in wild type without RPW8.1, indicating a specific role in RPW8.1-mediated disease resistance. Altogether, our results reveal a regulatory circuit controlling the accumulation of RPW8.1 to an appropriate level to precisely balance growth and disease resistance during pathogen invasion.
| Medienart: |
E-Artikel |
|---|
| Erscheinungsjahr: |
2024 |
|---|---|
| Erschienen: |
2024 |
| Enthalten in: |
Zur Gesamtaufnahme - volume:22 |
|---|---|
| Enthalten in: |
Plant biotechnology journal - 22(2024), 1 vom: 26. Jan., Seite 116-130 |
| Sprache: |
Englisch |
|---|
| Beteiligte Personen: |
Yang, Xue-Mei [VerfasserIn] |
|---|
| Links: |
|---|
| Themen: |
Arabidopsis Proteins |
|---|
| Anmerkungen: |
Date Completed 29.12.2023 Date Revised 30.12.2023 published: Print-Electronic Citation Status MEDLINE |
|---|
| doi: |
10.1111/pbi.14172 |
|---|
| funding: |
|
|---|---|
| Förderinstitution / Projekttitel: |
|
| PPN (Katalog-ID): |
NLM362489556 |
|---|
| LEADER | 01000caa a22002652 4500 | ||
|---|---|---|---|
| 001 | NLM362489556 | ||
| 003 | DE-627 | ||
| 005 | 20240108140204.0 | ||
| 007 | cr uuu---uuuuu | ||
| 008 | 231226s2024 xx |||||o 00| ||eng c | ||
| 024 | 7 | |a 10.1111/pbi.14172 |2 doi | |
| 028 | 5 | 2 | |a pubmed24n1243.xml |
| 035 | |a (DE-627)NLM362489556 | ||
| 035 | |a (NLM)37752622 | ||
| 040 | |a DE-627 |b ger |c DE-627 |e rakwb | ||
| 041 | |a eng | ||
| 100 | 1 | |a Yang, Xue-Mei |e verfasserin |4 aut | |
| 245 | 1 | 0 | |a Broad-spectrum resistance gene RPW8.1 balances immunity and growth via feedback regulation of WRKYs |
| 264 | 1 | |c 2024 | |
| 336 | |a Text |b txt |2 rdacontent | ||
| 337 | |a ƒaComputermedien |b c |2 rdamedia | ||
| 338 | |a ƒa Online-Ressource |b cr |2 rdacarrier | ||
| 500 | |a Date Completed 29.12.2023 | ||
| 500 | |a Date Revised 30.12.2023 | ||
| 500 | |a published: Print-Electronic | ||
| 500 | |a Citation Status MEDLINE | ||
| 520 | |a © 2023 The Authors. Plant Biotechnology Journal published by Society for Experimental Biology and The Association of Applied Biologists and John Wiley & Sons Ltd. | ||
| 520 | |a Arabidopsis RESISTANCE TO POWDERY MILDEW 8.1 (RPW8.1) is an important tool for engineering broad-spectrum disease resistance against multiple pathogens. Ectopic expression of RPW8.1 leads to enhanced disease resistance with cell death at leaves and compromised plant growth, implying a regulatory mechanism balancing RPW8.1-mediated resistance and growth. Here, we show that RPW8.1 constitutively enhances the expression of transcription factor WRKY51 and activates salicylic acid and ethylene signalling pathways; WRKY51 in turn suppresses RPW8.1 expression, forming a feedback regulation loop. RPW8.1 and WRKY51 are both induced by pathogen infection and pathogen-/microbe-associated molecular patterns. In ectopic expression of RPW8.1 background (R1Y4), overexpression of WRKY51 not only rescues the growth suppression and cell death caused by RPW8.1, but also suppresses RPW8.1-mediated broad-spectrum disease resistance and pattern-triggered immunity. Mechanistically, WRKY51 directly binds to and represses RPW8.1 promoter, thus limiting the expression amplitude of RPW8.1. Moreover, WRKY6, WRKY28 and WRKY41 play a role redundant to WRKY51 in the suppression of RPW8.1 expression and are constitutively upregulated in R1Y4 plants with WRKY51 being knocked out (wrky51 R1Y4) plants. Notably, WRKY51 has no significant effects on disease resistance or plant growth in wild type without RPW8.1, indicating a specific role in RPW8.1-mediated disease resistance. Altogether, our results reveal a regulatory circuit controlling the accumulation of RPW8.1 to an appropriate level to precisely balance growth and disease resistance during pathogen invasion | ||
| 650 | 4 | |a Journal Article | |
| 650 | 4 | |a RPW8.1 | |
| 650 | 4 | |a WRKY51 | |
| 650 | 4 | |a balance | |
| 650 | 4 | |a growth | |
| 650 | 4 | |a immunity | |
| 650 | 7 | |a Arabidopsis Proteins |2 NLM | |
| 700 | 1 | |a Zhao, Jing-Hao |e verfasserin |4 aut | |
| 700 | 1 | |a Xiong, Xiao-Yu |e verfasserin |4 aut | |
| 700 | 1 | |a Hu, Zhang-Wei |e verfasserin |4 aut | |
| 700 | 1 | |a Sun, Ji-Fen |e verfasserin |4 aut | |
| 700 | 1 | |a Su, Hao |e verfasserin |4 aut | |
| 700 | 1 | |a Liu, Yan-Jing |e verfasserin |4 aut | |
| 700 | 1 | |a Xiang, Ling |e verfasserin |4 aut | |
| 700 | 1 | |a Zhu, Yong |e verfasserin |4 aut | |
| 700 | 1 | |a Li, Jin-Lu |e verfasserin |4 aut | |
| 700 | 1 | |a Bhutto, Sadam Hussain |e verfasserin |4 aut | |
| 700 | 1 | |a Li, Guo-Bang |e verfasserin |4 aut | |
| 700 | 1 | |a Zhou, Shi-Xin |e verfasserin |4 aut | |
| 700 | 1 | |a Li, Chi |e verfasserin |4 aut | |
| 700 | 1 | |a Pu, Mei |e verfasserin |4 aut | |
| 700 | 1 | |a Wang, He |e verfasserin |4 aut | |
| 700 | 1 | |a Zhao, Zhi-Xue |e verfasserin |4 aut | |
| 700 | 1 | |a Zhang, Ji-Wei |e verfasserin |4 aut | |
| 700 | 1 | |a Huang, Yan-Yan |e verfasserin |4 aut | |
| 700 | 1 | |a Fan, Jing |e verfasserin |4 aut | |
| 700 | 1 | |a Wang, Wen-Ming |e verfasserin |4 aut | |
| 700 | 1 | |a Li, Yan |e verfasserin |4 aut | |
| 773 | 0 | 8 | |i Enthalten in |t Plant biotechnology journal |d 2003 |g 22(2024), 1 vom: 26. Jan., Seite 116-130 |w (DE-627)NLM16681718X |x 1467-7652 |7 nnns |
| 773 | 1 | 8 | |g volume:22 |g year:2024 |g number:1 |g day:26 |g month:01 |g pages:116-130 |
| 856 | 4 | 0 | |u http://dx.doi.org/10.1111/pbi.14172 |3 Volltext |
| 912 | |a GBV_USEFLAG_A | ||
| 912 | |a GBV_NLM | ||
| 951 | |a AR | ||
| 952 | |d 22 |j 2024 |e 1 |b 26 |c 01 |h 116-130 | ||