CsIVP functions in vasculature development and downy mildew resistance in cucumber
Domesticated crops with high yield and quality are frequently susceptible to pathogen attack, whereas enhancement of disease resistance generally compromises crop yield. The underlying mechanisms of how plant development and disease resistance are coordinately programed remain elusive. Here, we show...
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creator | Yan, Shuangshuang Ning, Kang Wang, Zhongyi Liu, Xiaofeng Zhong, Yanting Ding, Lian Zi, Hailing Cheng, Zhihua Li, Xuexian Shan, Hongyan Lv, Qingyang Luo, Laixin Liu, Renyi Yan, Liying Zhou, Zhaoyang Lucas, William John Zhang, Xiaolan |
description | Domesticated crops with high yield and quality are frequently susceptible to pathogen attack, whereas enhancement of disease resistance generally compromises crop yield. The underlying mechanisms of how plant development and disease resistance are coordinately programed remain elusive. Here, we showed that the basic Helix-Loop-Helix (bHLH) transcription factor Cucumis sativus Irregular Vasculature Patterning (CsIVP) was highly expressed in cucumber vascular tissues. Knockdown of CsIVP caused severe vasculature disorganization and abnormal organ morphogenesis. CsIVP directly binds to vascular-related regulators YABBY5 (CsYAB5), BREVIPEDICELLUS (CsBP), and AUXIN/INDOLEACETIC ACIDS4 (CsAUX4) and promotes their expression. Knockdown of CsYAB5 resulted in similar phenotypes as CsIVP-RNA interference (RNAi) plants, including disturbed vascular configuration and abnormal organ morphology. Meanwhile, CsIVP-RNAi plants were more resistant to downy mildew and accumulated more salicylic acid (SA). CsIVP physically interacts with NIM1-INTERACTING1 (CsNIMIN1), a negative regulator in the SA signaling pathway. Thus, CsIVP is a novel vasculature regulator functioning in CsYAB5-mediated organ morphogenesis and SA-mediated downy mildew resistance in cucumber. |
doi_str_mv | 10.1371/journal.pbio.3000671 |
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The underlying mechanisms of how plant development and disease resistance are coordinately programed remain elusive. Here, we showed that the basic Helix-Loop-Helix (bHLH) transcription factor Cucumis sativus Irregular Vasculature Patterning (CsIVP) was highly expressed in cucumber vascular tissues. Knockdown of CsIVP caused severe vasculature disorganization and abnormal organ morphogenesis. CsIVP directly binds to vascular-related regulators YABBY5 (CsYAB5), BREVIPEDICELLUS (CsBP), and AUXIN/INDOLEACETIC ACIDS4 (CsAUX4) and promotes their expression. Knockdown of CsYAB5 resulted in similar phenotypes as CsIVP-RNA interference (RNAi) plants, including disturbed vascular configuration and abnormal organ morphology. Meanwhile, CsIVP-RNAi plants were more resistant to downy mildew and accumulated more salicylic acid (SA). CsIVP physically interacts with NIM1-INTERACTING1 (CsNIMIN1), a negative regulator in the SA signaling pathway. Thus, CsIVP is a novel vasculature regulator functioning in CsYAB5-mediated organ morphogenesis and SA-mediated downy mildew resistance in cucumber.</description><identifier>ISSN: 1545-7885</identifier><identifier>ISSN: 1544-9173</identifier><identifier>EISSN: 1545-7885</identifier><identifier>DOI: 10.1371/journal.pbio.3000671</identifier><identifier>PMID: 32203514</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Agriculture ; Airborne microorganisms ; Biology ; Biology and Life Sciences ; Crop diseases ; Crop yield ; Crop yields ; Crops ; Disease resistance ; Domestication ; Downy mildew ; Drug resistance in microorganisms ; Engineering and Technology ; Flowers & plants ; Funding ; Gene expression ; Helix-loop-helix proteins ; Helix-loop-helix proteins (basic) ; Horticulture ; International cooperation ; Laboratories ; Morphogenesis ; Morphology ; Pathogenesis ; Pathogens ; Phenotypes ; Phylogenetics ; Plant diseases ; Plant pathology ; Plant sciences ; Plant tissues ; Regulators ; RNA ; RNA-mediated interference ; Salicylic acid ; Signal transduction ; Transcription factors ; Vascular tissue</subject><ispartof>PLoS biology, 2020-03, Vol.18 (3), p.e3000671-e3000671</ispartof><rights>COPYRIGHT 2020 Public Library of Science</rights><rights>2020 Yan et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 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The underlying mechanisms of how plant development and disease resistance are coordinately programed remain elusive. Here, we showed that the basic Helix-Loop-Helix (bHLH) transcription factor Cucumis sativus Irregular Vasculature Patterning (CsIVP) was highly expressed in cucumber vascular tissues. Knockdown of CsIVP caused severe vasculature disorganization and abnormal organ morphogenesis. CsIVP directly binds to vascular-related regulators YABBY5 (CsYAB5), BREVIPEDICELLUS (CsBP), and AUXIN/INDOLEACETIC ACIDS4 (CsAUX4) and promotes their expression. Knockdown of CsYAB5 resulted in similar phenotypes as CsIVP-RNA interference (RNAi) plants, including disturbed vascular configuration and abnormal organ morphology. Meanwhile, CsIVP-RNAi plants were more resistant to downy mildew and accumulated more salicylic acid (SA). CsIVP physically interacts with NIM1-INTERACTING1 (CsNIMIN1), a negative regulator in the SA signaling pathway. Thus, CsIVP is a novel vasculature regulator functioning in CsYAB5-mediated organ morphogenesis and SA-mediated downy mildew resistance in cucumber.</description><subject>Agriculture</subject><subject>Airborne microorganisms</subject><subject>Biology</subject><subject>Biology and Life Sciences</subject><subject>Crop diseases</subject><subject>Crop yield</subject><subject>Crop yields</subject><subject>Crops</subject><subject>Disease resistance</subject><subject>Domestication</subject><subject>Downy mildew</subject><subject>Drug resistance in microorganisms</subject><subject>Engineering and Technology</subject><subject>Flowers & plants</subject><subject>Funding</subject><subject>Gene expression</subject><subject>Helix-loop-helix proteins</subject><subject>Helix-loop-helix proteins (basic)</subject><subject>Horticulture</subject><subject>International 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functions in vasculature development and downy mildew resistance in cucumber</title><author>Yan, Shuangshuang ; Ning, Kang ; Wang, Zhongyi ; Liu, Xiaofeng ; Zhong, Yanting ; Ding, Lian ; Zi, Hailing ; Cheng, Zhihua ; Li, Xuexian ; Shan, Hongyan ; Lv, Qingyang ; Luo, Laixin ; Liu, Renyi ; Yan, Liying ; Zhou, Zhaoyang ; Lucas, William John ; Zhang, Xiaolan</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c695t-2348174f1e41b896e2fde49bb9497018c3b6fecc409a262ebc6f32ae4901fefd3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Agriculture</topic><topic>Airborne microorganisms</topic><topic>Biology</topic><topic>Biology and Life Sciences</topic><topic>Crop diseases</topic><topic>Crop yield</topic><topic>Crop yields</topic><topic>Crops</topic><topic>Disease resistance</topic><topic>Domestication</topic><topic>Downy mildew</topic><topic>Drug resistance in microorganisms</topic><topic>Engineering and Technology</topic><topic>Flowers & plants</topic><topic>Funding</topic><topic>Gene expression</topic><topic>Helix-loop-helix proteins</topic><topic>Helix-loop-helix proteins (basic)</topic><topic>Horticulture</topic><topic>International cooperation</topic><topic>Laboratories</topic><topic>Morphogenesis</topic><topic>Morphology</topic><topic>Pathogenesis</topic><topic>Pathogens</topic><topic>Phenotypes</topic><topic>Phylogenetics</topic><topic>Plant diseases</topic><topic>Plant pathology</topic><topic>Plant sciences</topic><topic>Plant tissues</topic><topic>Regulators</topic><topic>RNA</topic><topic>RNA-mediated interference</topic><topic>Salicylic acid</topic><topic>Signal transduction</topic><topic>Transcription factors</topic><topic>Vascular tissue</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Yan, Shuangshuang</creatorcontrib><creatorcontrib>Ning, Kang</creatorcontrib><creatorcontrib>Wang, 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Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Yan, Shuangshuang</au><au>Ning, Kang</au><au>Wang, Zhongyi</au><au>Liu, Xiaofeng</au><au>Zhong, Yanting</au><au>Ding, Lian</au><au>Zi, Hailing</au><au>Cheng, Zhihua</au><au>Li, Xuexian</au><au>Shan, Hongyan</au><au>Lv, Qingyang</au><au>Luo, Laixin</au><au>Liu, Renyi</au><au>Yan, Liying</au><au>Zhou, Zhaoyang</au><au>Lucas, William John</au><au>Zhang, Xiaolan</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>CsIVP functions in vasculature development and downy mildew resistance in cucumber</atitle><jtitle>PLoS biology</jtitle><addtitle>PLoS Biol</addtitle><date>2020-03-23</date><risdate>2020</risdate><volume>18</volume><issue>3</issue><spage>e3000671</spage><epage>e3000671</epage><pages>e3000671-e3000671</pages><issn>1545-7885</issn><issn>1544-9173</issn><eissn>1545-7885</eissn><abstract>Domesticated crops with high yield and quality are frequently susceptible to pathogen attack, whereas enhancement of disease resistance generally compromises crop yield. The underlying mechanisms of how plant development and disease resistance are coordinately programed remain elusive. Here, we showed that the basic Helix-Loop-Helix (bHLH) transcription factor Cucumis sativus Irregular Vasculature Patterning (CsIVP) was highly expressed in cucumber vascular tissues. Knockdown of CsIVP caused severe vasculature disorganization and abnormal organ morphogenesis. CsIVP directly binds to vascular-related regulators YABBY5 (CsYAB5), BREVIPEDICELLUS (CsBP), and AUXIN/INDOLEACETIC ACIDS4 (CsAUX4) and promotes their expression. Knockdown of CsYAB5 resulted in similar phenotypes as CsIVP-RNA interference (RNAi) plants, including disturbed vascular configuration and abnormal organ morphology. Meanwhile, CsIVP-RNAi plants were more resistant to downy mildew and accumulated more salicylic acid (SA). CsIVP physically interacts with NIM1-INTERACTING1 (CsNIMIN1), a negative regulator in the SA signaling pathway. Thus, CsIVP is a novel vasculature regulator functioning in CsYAB5-mediated organ morphogenesis and SA-mediated downy mildew resistance in cucumber.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>32203514</pmid><doi>10.1371/journal.pbio.3000671</doi><orcidid>https://orcid.org/0000-0002-8432-2220</orcidid><orcidid>https://orcid.org/0000-0002-6343-3116</orcidid><orcidid>https://orcid.org/0000-0002-2534-4171</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Agriculture Airborne microorganisms Biology Biology and Life Sciences Crop diseases Crop yield Crop yields Crops Disease resistance Domestication Downy mildew Drug resistance in microorganisms Engineering and Technology Flowers & plants Funding Gene expression Helix-loop-helix proteins Helix-loop-helix proteins (basic) Horticulture International cooperation Laboratories Morphogenesis Morphology Pathogenesis Pathogens Phenotypes Phylogenetics Plant diseases Plant pathology Plant sciences Plant tissues Regulators RNA RNA-mediated interference Salicylic acid Signal transduction Transcription factors Vascular tissue |
title | CsIVP functions in vasculature development and downy mildew resistance in cucumber |
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