Salicylic Acid Is Required for Broad-Spectrum Disease Resistance in Rice

Rice plants contain high basal levels of salicylic acid (SA), but some of their functions remain elusive. To elucidate the importance of SA homeostasis in rice immunity, we characterized four rice SA hydroxylase genes (<i>OsSAHs</i>) and verified their roles in SA metabolism and disease...

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Main Authors: Bingbing Liang, Han Wang, Ce Yang, Luyao Wang, Linlu Qi, Zejian Guo, Xujun Chen
Format: Article
Language:English
Published: MDPI AG 2022-01-01
Series:International Journal of Molecular Sciences
Subjects:
Online Access:https://www.mdpi.com/1422-0067/23/3/1354
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author Bingbing Liang
Han Wang
Ce Yang
Luyao Wang
Linlu Qi
Zejian Guo
Xujun Chen
author_facet Bingbing Liang
Han Wang
Ce Yang
Luyao Wang
Linlu Qi
Zejian Guo
Xujun Chen
author_sort Bingbing Liang
collection DOAJ
description Rice plants contain high basal levels of salicylic acid (SA), but some of their functions remain elusive. To elucidate the importance of SA homeostasis in rice immunity, we characterized four rice SA hydroxylase genes (<i>OsSAHs</i>) and verified their roles in SA metabolism and disease resistance. Recombinant OsSAH proteins catalyzed SA in vitro, while OsSAH3 protein showed only SA 5-hydroxylase (SA5H) activity, which was remarkably higher than that of other OsSAHs that presented both SA3H and SA5H activities. Amino acid substitutions revealed that three amino acids in the binding pocket affected SAH enzyme activity and/or specificity. Knockout <i>OsSAH</i><i>2</i> and <i>OsSAH3</i> (<i>sah</i>KO) genes conferred enhanced resistance to both hemibiotrophic and necrotrophic pathogens, whereas overexpression of each <i>OsSAH</i> gene increased susceptibility to the pathogens. <i>sah</i>KO mutants showed increased SA and jasmonate levels compared to those of the wild type and <i>OsSAH</i>-overexpressing plants. Analysis of the <i>OsSAH3</i> promoter indicated that its induction was mainly restricted around <i>Magnaporthe oryzae</i> infection sites. Taken together, our findings indicate that SA plays a vital role in immune signaling. Moreover, fine-tuning SA homeostasis through suppression of SA metabolism is an effective approach in studying broad-spectrum disease resistance in rice.
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spelling doaj.art-c3d88618e37e40278f4f9268820b4a7f2023-11-23T16:39:04ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672022-01-01233135410.3390/ijms23031354Salicylic Acid Is Required for Broad-Spectrum Disease Resistance in RiceBingbing Liang0Han Wang1Ce Yang2Luyao Wang3Linlu Qi4Zejian Guo5Xujun Chen6Key Laboratory of Pest Monitoring and Green Management, MOA, Joint Laboratory for International Cooperation in Crop Molecular Breeding, Department of Plant Pathology, China Agricultural University, Beijing 100193, ChinaKey Laboratory of Pest Monitoring and Green Management, MOA, Joint Laboratory for International Cooperation in Crop Molecular Breeding, Department of Plant Pathology, China Agricultural University, Beijing 100193, ChinaKey Laboratory of Pest Monitoring and Green Management, MOA, Joint Laboratory for International Cooperation in Crop Molecular Breeding, Department of Plant Pathology, China Agricultural University, Beijing 100193, ChinaKey Laboratory of Pest Monitoring and Green Management, MOA, Joint Laboratory for International Cooperation in Crop Molecular Breeding, Department of Plant Pathology, China Agricultural University, Beijing 100193, ChinaKey Laboratory of Pest Monitoring and Green Management, MOA, Joint Laboratory for International Cooperation in Crop Molecular Breeding, Department of Plant Pathology, China Agricultural University, Beijing 100193, ChinaKey Laboratory of Pest Monitoring and Green Management, MOA, Joint Laboratory for International Cooperation in Crop Molecular Breeding, Department of Plant Pathology, China Agricultural University, Beijing 100193, ChinaKey Laboratory of Pest Monitoring and Green Management, MOA, Joint Laboratory for International Cooperation in Crop Molecular Breeding, Department of Plant Pathology, China Agricultural University, Beijing 100193, ChinaRice plants contain high basal levels of salicylic acid (SA), but some of their functions remain elusive. To elucidate the importance of SA homeostasis in rice immunity, we characterized four rice SA hydroxylase genes (<i>OsSAHs</i>) and verified their roles in SA metabolism and disease resistance. Recombinant OsSAH proteins catalyzed SA in vitro, while OsSAH3 protein showed only SA 5-hydroxylase (SA5H) activity, which was remarkably higher than that of other OsSAHs that presented both SA3H and SA5H activities. Amino acid substitutions revealed that three amino acids in the binding pocket affected SAH enzyme activity and/or specificity. Knockout <i>OsSAH</i><i>2</i> and <i>OsSAH3</i> (<i>sah</i>KO) genes conferred enhanced resistance to both hemibiotrophic and necrotrophic pathogens, whereas overexpression of each <i>OsSAH</i> gene increased susceptibility to the pathogens. <i>sah</i>KO mutants showed increased SA and jasmonate levels compared to those of the wild type and <i>OsSAH</i>-overexpressing plants. Analysis of the <i>OsSAH3</i> promoter indicated that its induction was mainly restricted around <i>Magnaporthe oryzae</i> infection sites. Taken together, our findings indicate that SA plays a vital role in immune signaling. Moreover, fine-tuning SA homeostasis through suppression of SA metabolism is an effective approach in studying broad-spectrum disease resistance in rice.https://www.mdpi.com/1422-0067/23/3/1354immunitydioxygenasehydroxylationjasmonic acid<i>Oryza sativa</i>salicylic acid
spellingShingle Bingbing Liang
Han Wang
Ce Yang
Luyao Wang
Linlu Qi
Zejian Guo
Xujun Chen
Salicylic Acid Is Required for Broad-Spectrum Disease Resistance in Rice
International Journal of Molecular Sciences
immunity
dioxygenase
hydroxylation
jasmonic acid
<i>Oryza sativa</i>
salicylic acid
title Salicylic Acid Is Required for Broad-Spectrum Disease Resistance in Rice
title_full Salicylic Acid Is Required for Broad-Spectrum Disease Resistance in Rice
title_fullStr Salicylic Acid Is Required for Broad-Spectrum Disease Resistance in Rice
title_full_unstemmed Salicylic Acid Is Required for Broad-Spectrum Disease Resistance in Rice
title_short Salicylic Acid Is Required for Broad-Spectrum Disease Resistance in Rice
title_sort salicylic acid is required for broad spectrum disease resistance in rice
topic immunity
dioxygenase
hydroxylation
jasmonic acid
<i>Oryza sativa</i>
salicylic acid
url https://www.mdpi.com/1422-0067/23/3/1354
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AT ceyang salicylicacidisrequiredforbroadspectrumdiseaseresistanceinrice
AT luyaowang salicylicacidisrequiredforbroadspectrumdiseaseresistanceinrice
AT linluqi salicylicacidisrequiredforbroadspectrumdiseaseresistanceinrice
AT zejianguo salicylicacidisrequiredforbroadspectrumdiseaseresistanceinrice
AT xujunchen salicylicacidisrequiredforbroadspectrumdiseaseresistanceinrice