A peroxisomal cinnamate:CoA ligase-dependent phytohormone metabolic cascade in submerged rice germination

The mechanism underlying the ability of rice to germinate underwater is a largely enigmatic but key research question highly relevant to rice cultivation. Moreover, although rice is known to accumulate salicylic acid (SA), SA biosynthesis is poorly defined, and its role in underwater germination is...

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Veröffentlicht in:Developmental cell 2024-06, Vol.59 (11), p.1363-1378.e4
Hauptverfasser: Wang, Yukang, Jin, Gaochen, Song, Shuyan, Jin, Yijun, Wang, Xiaowen, Yang, Shuaiqi, Shen, Xingxing, Gan, Yinbo, Wang, Yuexing, Li, Ran, Liu, Jian-Xiang, Hu, Jianping, Pan, Ronghui
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container_end_page 1378.e4
container_issue 11
container_start_page 1363
container_title Developmental cell
container_volume 59
creator Wang, Yukang
Jin, Gaochen
Song, Shuyan
Jin, Yijun
Wang, Xiaowen
Yang, Shuaiqi
Shen, Xingxing
Gan, Yinbo
Wang, Yuexing
Li, Ran
Liu, Jian-Xiang
Hu, Jianping
Pan, Ronghui
description The mechanism underlying the ability of rice to germinate underwater is a largely enigmatic but key research question highly relevant to rice cultivation. Moreover, although rice is known to accumulate salicylic acid (SA), SA biosynthesis is poorly defined, and its role in underwater germination is unknown. It is also unclear whether peroxisomes, organelles essential to oilseed germination and rice SA accumulation, play a role in rice germination. Here, we show that submerged imbibition of rice seeds induces SA accumulation to promote germination in submergence. Two submergence-induced peroxisomal Oryza sativa cinnamate:CoA ligases (OsCNLs) are required for this SA accumulation. SA exerts this germination-promoting function by inducing indole-acetic acid (IAA) catabolism through the IAA-amino acid conjugating enzyme GH3. The metabolic cascade we identified may potentially be adopted in agriculture to improve the underwater germination of submergence-intolerant rice varieties. SA pretreatment is also a promising strategy to improve submerged rice germination in the field. [Display omitted] •OsCNLs are induced in rice submerged imbibition to synthesize salicylic acid (SA)•Peroxisomal OsCNLs are key enzymes in the SA biosynthetic pathway in rice•SA promotes submerged germination via OsGH3-mediated indole-acetic acid catabolism•SA pretreatment is a cost-effective strategy to improve rice submerged germination Wang et al. demonstrated a peroxisomal cinnamate:CoA ligase (CNL)-dependent phytohormone metabolic cascade in rice. Submerged imbibition-induced salicylic acid (SA) biosynthesis promotes anaerobic germination by inducing OsGH3-mediated indole-acetic acid (IAA)-amino acid conjugation, thus releasing IAA’s inhibition of germination under water submergence conditions.
doi_str_mv 10.1016/j.devcel.2024.03.023
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Moreover, although rice is known to accumulate salicylic acid (SA), SA biosynthesis is poorly defined, and its role in underwater germination is unknown. It is also unclear whether peroxisomes, organelles essential to oilseed germination and rice SA accumulation, play a role in rice germination. Here, we show that submerged imbibition of rice seeds induces SA accumulation to promote germination in submergence. Two submergence-induced peroxisomal Oryza sativa cinnamate:CoA ligases (OsCNLs) are required for this SA accumulation. SA exerts this germination-promoting function by inducing indole-acetic acid (IAA) catabolism through the IAA-amino acid conjugating enzyme GH3. The metabolic cascade we identified may potentially be adopted in agriculture to improve the underwater germination of submergence-intolerant rice varieties. SA pretreatment is also a promising strategy to improve submerged rice germination in the field. [Display omitted] •OsCNLs are induced in rice submerged imbibition to synthesize salicylic acid (SA)•Peroxisomal OsCNLs are key enzymes in the SA biosynthetic pathway in rice•SA promotes submerged germination via OsGH3-mediated indole-acetic acid catabolism•SA pretreatment is a cost-effective strategy to improve rice submerged germination Wang et al. demonstrated a peroxisomal cinnamate:CoA ligase (CNL)-dependent phytohormone metabolic cascade in rice. Submerged imbibition-induced salicylic acid (SA) biosynthesis promotes anaerobic germination by inducing OsGH3-mediated indole-acetic acid (IAA)-amino acid conjugation, thus releasing IAA’s inhibition of germination under water submergence conditions.</description><identifier>ISSN: 1534-5807</identifier><identifier>EISSN: 1878-1551</identifier><identifier>DOI: 10.1016/j.devcel.2024.03.023</identifier><identifier>PMID: 38579719</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>cinnamate:CoA ligase ; CNL ; GH3 ; Gretchen Hagen 3 ; IAA ; indole-3-acetic acid ; PAL ; peroxisome ; rice direct seeding ; salicylic acid ; submerged germination ; submerged imbibition ; the phenylalanine ammonia-lyase pathway</subject><ispartof>Developmental cell, 2024-06, Vol.59 (11), p.1363-1378.e4</ispartof><rights>2024 Elsevier Inc.</rights><rights>Copyright © 2024 Elsevier Inc. 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Moreover, although rice is known to accumulate salicylic acid (SA), SA biosynthesis is poorly defined, and its role in underwater germination is unknown. It is also unclear whether peroxisomes, organelles essential to oilseed germination and rice SA accumulation, play a role in rice germination. Here, we show that submerged imbibition of rice seeds induces SA accumulation to promote germination in submergence. Two submergence-induced peroxisomal Oryza sativa cinnamate:CoA ligases (OsCNLs) are required for this SA accumulation. SA exerts this germination-promoting function by inducing indole-acetic acid (IAA) catabolism through the IAA-amino acid conjugating enzyme GH3. The metabolic cascade we identified may potentially be adopted in agriculture to improve the underwater germination of submergence-intolerant rice varieties. SA pretreatment is also a promising strategy to improve submerged rice germination in the field. [Display omitted] •OsCNLs are induced in rice submerged imbibition to synthesize salicylic acid (SA)•Peroxisomal OsCNLs are key enzymes in the SA biosynthetic pathway in rice•SA promotes submerged germination via OsGH3-mediated indole-acetic acid catabolism•SA pretreatment is a cost-effective strategy to improve rice submerged germination Wang et al. demonstrated a peroxisomal cinnamate:CoA ligase (CNL)-dependent phytohormone metabolic cascade in rice. Submerged imbibition-induced salicylic acid (SA) biosynthesis promotes anaerobic germination by inducing OsGH3-mediated indole-acetic acid (IAA)-amino acid conjugation, thus releasing IAA’s inhibition of germination under water submergence conditions.</description><subject>cinnamate:CoA ligase</subject><subject>CNL</subject><subject>GH3</subject><subject>Gretchen Hagen 3</subject><subject>IAA</subject><subject>indole-3-acetic acid</subject><subject>PAL</subject><subject>peroxisome</subject><subject>rice direct seeding</subject><subject>salicylic acid</subject><subject>submerged germination</subject><subject>submerged imbibition</subject><subject>the phenylalanine ammonia-lyase pathway</subject><issn>1534-5807</issn><issn>1878-1551</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><recordid>eNp9kEtPHDEQhK0IBAT4B1HkI5eZtB_zWA5Iq1VeElIucLY8dnvxasae2LMI_n28WsKRU9ehqlr1EfKFQc2Atd92tcVng2PNgcsaRA1cfCIXrO_6ijUNOym6EbJqeujOyeecd1BirIczci76plt1bHVB_JrOmOKLz3HSIzU-BD3pBW83cU1Hv9UZK4szBothofPT6xKfYppiQDrhooc4ekONzkZbpD7QvB8mTFu0NHmDdItp8kEvPoYrcur0mPH67V6Sxx_fHza_qvs_P39v1veVES1fqqas4S3olePgJJcMXCeFBRx0L4ciBsGROSm467vGCW2HhgsHMLhWttKIS3Jz7J1T_LvHvKjJ58Jp1AHjPisBotT2UspilUerSTHnhE7NyU86vSoG6gBZ7dQRsjpAViBUgVxiX98-HMba99B_qsVwdzRg2fnsMalsPAaD1ic0i7LRf_zhH2aEkJc</recordid><startdate>20240603</startdate><enddate>20240603</enddate><creator>Wang, Yukang</creator><creator>Jin, Gaochen</creator><creator>Song, Shuyan</creator><creator>Jin, Yijun</creator><creator>Wang, Xiaowen</creator><creator>Yang, Shuaiqi</creator><creator>Shen, Xingxing</creator><creator>Gan, Yinbo</creator><creator>Wang, Yuexing</creator><creator>Li, Ran</creator><creator>Liu, Jian-Xiang</creator><creator>Hu, Jianping</creator><creator>Pan, Ronghui</creator><general>Elsevier Inc</general><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0002-4264-5566</orcidid></search><sort><creationdate>20240603</creationdate><title>A peroxisomal cinnamate:CoA ligase-dependent phytohormone metabolic cascade in submerged rice germination</title><author>Wang, Yukang ; Jin, Gaochen ; Song, Shuyan ; Jin, Yijun ; Wang, Xiaowen ; Yang, Shuaiqi ; Shen, Xingxing ; Gan, Yinbo ; Wang, Yuexing ; Li, Ran ; Liu, Jian-Xiang ; Hu, Jianping ; Pan, Ronghui</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c362t-5024260a9f20f42410f743d0eba84b3d0b32e1f432f875f3adb523f00bf6464c3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>cinnamate:CoA ligase</topic><topic>CNL</topic><topic>GH3</topic><topic>Gretchen Hagen 3</topic><topic>IAA</topic><topic>indole-3-acetic acid</topic><topic>PAL</topic><topic>peroxisome</topic><topic>rice direct seeding</topic><topic>salicylic acid</topic><topic>submerged germination</topic><topic>submerged imbibition</topic><topic>the phenylalanine ammonia-lyase pathway</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Wang, Yukang</creatorcontrib><creatorcontrib>Jin, Gaochen</creatorcontrib><creatorcontrib>Song, Shuyan</creatorcontrib><creatorcontrib>Jin, Yijun</creatorcontrib><creatorcontrib>Wang, Xiaowen</creatorcontrib><creatorcontrib>Yang, Shuaiqi</creatorcontrib><creatorcontrib>Shen, Xingxing</creatorcontrib><creatorcontrib>Gan, Yinbo</creatorcontrib><creatorcontrib>Wang, Yuexing</creatorcontrib><creatorcontrib>Li, Ran</creatorcontrib><creatorcontrib>Liu, Jian-Xiang</creatorcontrib><creatorcontrib>Hu, Jianping</creatorcontrib><creatorcontrib>Pan, Ronghui</creatorcontrib><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><jtitle>Developmental cell</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Wang, Yukang</au><au>Jin, Gaochen</au><au>Song, Shuyan</au><au>Jin, Yijun</au><au>Wang, Xiaowen</au><au>Yang, Shuaiqi</au><au>Shen, Xingxing</au><au>Gan, Yinbo</au><au>Wang, Yuexing</au><au>Li, Ran</au><au>Liu, Jian-Xiang</au><au>Hu, Jianping</au><au>Pan, Ronghui</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>A peroxisomal cinnamate:CoA ligase-dependent phytohormone metabolic cascade in submerged rice germination</atitle><jtitle>Developmental cell</jtitle><addtitle>Dev Cell</addtitle><date>2024-06-03</date><risdate>2024</risdate><volume>59</volume><issue>11</issue><spage>1363</spage><epage>1378.e4</epage><pages>1363-1378.e4</pages><issn>1534-5807</issn><eissn>1878-1551</eissn><abstract>The mechanism underlying the ability of rice to germinate underwater is a largely enigmatic but key research question highly relevant to rice cultivation. Moreover, although rice is known to accumulate salicylic acid (SA), SA biosynthesis is poorly defined, and its role in underwater germination is unknown. It is also unclear whether peroxisomes, organelles essential to oilseed germination and rice SA accumulation, play a role in rice germination. Here, we show that submerged imbibition of rice seeds induces SA accumulation to promote germination in submergence. Two submergence-induced peroxisomal Oryza sativa cinnamate:CoA ligases (OsCNLs) are required for this SA accumulation. SA exerts this germination-promoting function by inducing indole-acetic acid (IAA) catabolism through the IAA-amino acid conjugating enzyme GH3. The metabolic cascade we identified may potentially be adopted in agriculture to improve the underwater germination of submergence-intolerant rice varieties. SA pretreatment is also a promising strategy to improve submerged rice germination in the field. [Display omitted] •OsCNLs are induced in rice submerged imbibition to synthesize salicylic acid (SA)•Peroxisomal OsCNLs are key enzymes in the SA biosynthetic pathway in rice•SA promotes submerged germination via OsGH3-mediated indole-acetic acid catabolism•SA pretreatment is a cost-effective strategy to improve rice submerged germination Wang et al. demonstrated a peroxisomal cinnamate:CoA ligase (CNL)-dependent phytohormone metabolic cascade in rice. Submerged imbibition-induced salicylic acid (SA) biosynthesis promotes anaerobic germination by inducing OsGH3-mediated indole-acetic acid (IAA)-amino acid conjugation, thus releasing IAA’s inhibition of germination under water submergence conditions.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>38579719</pmid><doi>10.1016/j.devcel.2024.03.023</doi><orcidid>https://orcid.org/0000-0002-4264-5566</orcidid></addata></record>
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source Elsevier ScienceDirect Journals
subjects cinnamate:CoA ligase
CNL
GH3
Gretchen Hagen 3
IAA
indole-3-acetic acid
PAL
peroxisome
rice direct seeding
salicylic acid
submerged germination
submerged imbibition
the phenylalanine ammonia-lyase pathway
title A peroxisomal cinnamate:CoA ligase-dependent phytohormone metabolic cascade in submerged rice germination
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