Resistance to Powdery Mildew in Qingke Involves the Accumulation of Aromatic Phenolamides Through Jasmonate-Mediated Activation of Defense-Related Genes
Powdery mildew (PM) leads to severe yield reduction in qingke (Hordeum vulgare L. var. nudum). Although studies have focused on identifying PM-related resistance genes, mechanistic insights into the metabolic regulation networks of resistance against PM have rarely been explored in qingke. Here, we...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2022-06-01
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| Series: | Frontiers in Plant Science |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fpls.2022.900345/full |
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| author | Congping Xu Congping Xu Congping Xu Congping Xu Chuansong Zhan Chuansong Zhan Sishu Huang Sishu Huang Qijun Xu Qijun Xu Tang Tang Yulin Wang Jie Luo Jie Luo Xingquan Zeng Xingquan Zeng Xingquan Zeng |
| author_facet | Congping Xu Congping Xu Congping Xu Congping Xu Chuansong Zhan Chuansong Zhan Sishu Huang Sishu Huang Qijun Xu Qijun Xu Tang Tang Yulin Wang Jie Luo Jie Luo Xingquan Zeng Xingquan Zeng Xingquan Zeng |
| author_sort | Congping Xu |
| collection | DOAJ |
| description | Powdery mildew (PM) leads to severe yield reduction in qingke (Hordeum vulgare L. var. nudum). Although studies have focused on identifying PM-related resistance genes, mechanistic insights into the metabolic regulation networks of resistance against PM have rarely been explored in qingke. Here, we integrated transcriptomic, proteomic and metabolomic data using PM-susceptible (G72) and PM-resistant (K69) accessions to systemically explore the mechanisms of PM resistance. The integrated results show that a rapidly transduction of jasmonic acid (JA) and (+)-7-iso-jasmonoyl-L-isoleucine (JA-Ile), and importantly, a inducing accumulation of aromatic PAs conferred qingke-specific resistance for PM stress. Functional analysis revealed that the four BAHD N-acyltransferase genes were responsible for the synthesis of aliphatic and aromatic PAs. The expression of the four genes are induced by methyl jasmonate (MeJA) and PM treatment. Co-expression network analysis shows that a histone lysine demethylase, JMJ705 gene, also induced by MeJA and PM treatment, had highly correlation with PAs biosynthesis. Chromatin immunoprecipitation (ChIP)-seq assays revealed that the level of trimethylated histone H3 lysine 27 (H3K27me3) of the four genes in MeJA and PM-treated plants was significantly reduced. Overall, our results suggest that a novel strategy for jasmonic acid signal-mediated demethylation controlling the accumulation of aromatic PAs to enhance plant immune resistance through removal of H3K27me3 and activating defense-related gene expression. |
| first_indexed | 2024-04-12T12:25:58Z |
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| id | doaj.art-eb97f99294d840e4a2f6aff2ab02d0f1 |
| institution | Directory Open Access Journal |
| issn | 1664-462X |
| language | English |
| last_indexed | 2024-04-12T12:25:58Z |
| publishDate | 2022-06-01 |
| publisher | Frontiers Media S.A. |
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| series | Frontiers in Plant Science |
| spelling | doaj.art-eb97f99294d840e4a2f6aff2ab02d0f12022-12-22T03:33:10ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2022-06-011310.3389/fpls.2022.900345900345Resistance to Powdery Mildew in Qingke Involves the Accumulation of Aromatic Phenolamides Through Jasmonate-Mediated Activation of Defense-Related GenesCongping Xu0Congping Xu1Congping Xu2Congping Xu3Chuansong Zhan4Chuansong Zhan5Sishu Huang6Sishu Huang7Qijun Xu8Qijun Xu9Tang Tang10Yulin Wang11Jie Luo12Jie Luo13Xingquan Zeng14Xingquan Zeng15Xingquan Zeng16State Key Laboratory of Hulless Barley and Yak Germplasm Resources and Genetic Improvement, Lhasa, ChinaTibet Academy of Agricultural and Animal Husbandry Sciences Lhasa, Tibet, ChinaCollege of Tropical Crops, Hainan University, Haikou, ChinaSanya Nanfan Research Institute of Hainan University, Hainan Yazhou Bay Seed Laboratory, Sanya, ChinaCollege of Tropical Crops, Hainan University, Haikou, ChinaSanya Nanfan Research Institute of Hainan University, Hainan Yazhou Bay Seed Laboratory, Sanya, ChinaCollege of Tropical Crops, Hainan University, Haikou, ChinaSanya Nanfan Research Institute of Hainan University, Hainan Yazhou Bay Seed Laboratory, Sanya, ChinaState Key Laboratory of Hulless Barley and Yak Germplasm Resources and Genetic Improvement, Lhasa, ChinaTibet Academy of Agricultural and Animal Husbandry Sciences Lhasa, Tibet, ChinaWuhan Metware Biotechnology Co., Ltd., Wuhan, ChinaState Key Laboratory of Hulless Barley and Yak Germplasm Resources and Genetic Improvement, Lhasa, ChinaCollege of Tropical Crops, Hainan University, Haikou, ChinaSanya Nanfan Research Institute of Hainan University, Hainan Yazhou Bay Seed Laboratory, Sanya, ChinaState Key Laboratory of Hulless Barley and Yak Germplasm Resources and Genetic Improvement, Lhasa, ChinaTibet Academy of Agricultural and Animal Husbandry Sciences Lhasa, Tibet, ChinaPlant Sciences College, Tibet Agriculture and Animal Husbandry University, Tibet, ChinaPowdery mildew (PM) leads to severe yield reduction in qingke (Hordeum vulgare L. var. nudum). Although studies have focused on identifying PM-related resistance genes, mechanistic insights into the metabolic regulation networks of resistance against PM have rarely been explored in qingke. Here, we integrated transcriptomic, proteomic and metabolomic data using PM-susceptible (G72) and PM-resistant (K69) accessions to systemically explore the mechanisms of PM resistance. The integrated results show that a rapidly transduction of jasmonic acid (JA) and (+)-7-iso-jasmonoyl-L-isoleucine (JA-Ile), and importantly, a inducing accumulation of aromatic PAs conferred qingke-specific resistance for PM stress. Functional analysis revealed that the four BAHD N-acyltransferase genes were responsible for the synthesis of aliphatic and aromatic PAs. The expression of the four genes are induced by methyl jasmonate (MeJA) and PM treatment. Co-expression network analysis shows that a histone lysine demethylase, JMJ705 gene, also induced by MeJA and PM treatment, had highly correlation with PAs biosynthesis. Chromatin immunoprecipitation (ChIP)-seq assays revealed that the level of trimethylated histone H3 lysine 27 (H3K27me3) of the four genes in MeJA and PM-treated plants was significantly reduced. Overall, our results suggest that a novel strategy for jasmonic acid signal-mediated demethylation controlling the accumulation of aromatic PAs to enhance plant immune resistance through removal of H3K27me3 and activating defense-related gene expression.https://www.frontiersin.org/articles/10.3389/fpls.2022.900345/fullpowdery mildew (Blumeria graminis f. sp. hordei)metabolomicstranscriptomeproteomejasmonic acidH3K27me3 |
| spellingShingle | Congping Xu Congping Xu Congping Xu Congping Xu Chuansong Zhan Chuansong Zhan Sishu Huang Sishu Huang Qijun Xu Qijun Xu Tang Tang Yulin Wang Jie Luo Jie Luo Xingquan Zeng Xingquan Zeng Xingquan Zeng Resistance to Powdery Mildew in Qingke Involves the Accumulation of Aromatic Phenolamides Through Jasmonate-Mediated Activation of Defense-Related Genes Frontiers in Plant Science powdery mildew (Blumeria graminis f. sp. hordei) metabolomics transcriptome proteome jasmonic acid H3K27me3 |
| title | Resistance to Powdery Mildew in Qingke Involves the Accumulation of Aromatic Phenolamides Through Jasmonate-Mediated Activation of Defense-Related Genes |
| title_full | Resistance to Powdery Mildew in Qingke Involves the Accumulation of Aromatic Phenolamides Through Jasmonate-Mediated Activation of Defense-Related Genes |
| title_fullStr | Resistance to Powdery Mildew in Qingke Involves the Accumulation of Aromatic Phenolamides Through Jasmonate-Mediated Activation of Defense-Related Genes |
| title_full_unstemmed | Resistance to Powdery Mildew in Qingke Involves the Accumulation of Aromatic Phenolamides Through Jasmonate-Mediated Activation of Defense-Related Genes |
| title_short | Resistance to Powdery Mildew in Qingke Involves the Accumulation of Aromatic Phenolamides Through Jasmonate-Mediated Activation of Defense-Related Genes |
| title_sort | resistance to powdery mildew in qingke involves the accumulation of aromatic phenolamides through jasmonate mediated activation of defense related genes |
| topic | powdery mildew (Blumeria graminis f. sp. hordei) metabolomics transcriptome proteome jasmonic acid H3K27me3 |
| url | https://www.frontiersin.org/articles/10.3389/fpls.2022.900345/full |
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