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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Published in | PLoS biology Vol. 18; no. 3; p. e3000671 |
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Main Authors | , , , , , , , , , , , , , , , , |
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23.03.2020
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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. |
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AbstractList | 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. 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 C ucumis s ativus I rregular V asculature P atterning ( 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. The novel vascular patterning regulator CsIVP functions to integrate the programming of organ morphogenesis and salicylic acid-mediated resistance to downy mildew in cucumber. |
Author | Zhang, Xiaolan Lucas, William John Yan, Shuangshuang Ning, Kang Cheng, Zhihua Yan, Liying Li, Xuexian Lv, Qingyang Zhong, Yanting Ding, Lian Zi, Hailing Luo, Laixin Liu, Renyi Wang, Zhongyi Zhou, Zhaoyang Liu, Xiaofeng Shan, Hongyan |
AuthorAffiliation | 2 Key Laboratory of Biology and Genetic Improvement of Horticultural Crops (South China), Ministry of Agriculture and Rural Affairs, College of Horticulture, South China Agricultural University, Guangzhou, China 3 Department of Plant Nutrition, the Key Laboratory of Plant-Soil Interactions, China Agricultural University, Beijing, China 4 Shanghai Center for Plant Stress Biology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai, China Cornell University, UNITED STATES 7 College of Horticulture, and FAFU-UCR Joint Center for Horticultural Biology and Metabolomics, Haixia Institute of Science and Technology, Fujian Agriculture and Forestry University, Fuzhou, China 1 State Key Laboratories of Agrobiotechnology, Beijing Key Laboratory of Growth and Developmental Regulation for Protected Vegetable Crops, MOE Joint Laboratory for International Cooperation in Crop Molecular Breeding, China Agricultural University, Beijing, China 8 College of Horticulture Science an |
AuthorAffiliation_xml | – name: 5 State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Beijing, China – name: Cornell University, UNITED STATES – name: 2 Key Laboratory of Biology and Genetic Improvement of Horticultural Crops (South China), Ministry of Agriculture and Rural Affairs, College of Horticulture, South China Agricultural University, Guangzhou, China – name: 3 Department of Plant Nutrition, the Key Laboratory of Plant-Soil Interactions, China Agricultural University, Beijing, China – name: 6 Department of Plant Pathology, China Agricultural University, Beijing, China – name: 7 College of Horticulture, and FAFU-UCR Joint Center for Horticultural Biology and Metabolomics, Haixia Institute of Science and Technology, Fujian Agriculture and Forestry University, Fuzhou, China – name: 9 Department of Plant Biology, University of California, Davis, California, United States of America – name: 8 College of Horticulture Science and Technology, Hebei Normal University of Science & Technology, Qinhuangdao, China – name: 4 Shanghai Center for Plant Stress Biology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai, China – name: 1 State Key Laboratories of Agrobiotechnology, Beijing Key Laboratory of Growth and Developmental Regulation for Protected Vegetable Crops, MOE Joint Laboratory for International Cooperation in Crop Molecular Breeding, China Agricultural University, Beijing, China |
Author_xml | – sequence: 1 givenname: Shuangshuang surname: Yan fullname: Yan, Shuangshuang organization: Key Laboratory of Biology and Genetic Improvement of Horticultural Crops (South China), Ministry of Agriculture and Rural Affairs, College of Horticulture, South China Agricultural University, Guangzhou, China – sequence: 2 givenname: Kang surname: Ning fullname: Ning, Kang organization: State Key Laboratories of Agrobiotechnology, Beijing Key Laboratory of Growth and Developmental Regulation for Protected Vegetable Crops, MOE Joint Laboratory for International Cooperation in Crop Molecular Breeding, China Agricultural University, Beijing, China – sequence: 3 givenname: Zhongyi surname: Wang fullname: Wang, Zhongyi organization: State Key Laboratories of Agrobiotechnology, Beijing Key Laboratory of Growth and Developmental Regulation for Protected Vegetable Crops, MOE Joint Laboratory for International Cooperation in Crop Molecular Breeding, China Agricultural University, Beijing, China – sequence: 4 givenname: Xiaofeng surname: Liu fullname: Liu, Xiaofeng organization: State Key Laboratories of Agrobiotechnology, Beijing Key Laboratory of Growth and Developmental Regulation for Protected Vegetable Crops, MOE Joint Laboratory for International Cooperation in Crop Molecular Breeding, China Agricultural University, Beijing, China – sequence: 5 givenname: Yanting surname: Zhong fullname: Zhong, Yanting organization: Department of Plant Nutrition, the Key Laboratory of Plant-Soil Interactions, China Agricultural University, Beijing, China – sequence: 6 givenname: Lian orcidid: 0000-0002-8432-2220 surname: Ding fullname: Ding, Lian organization: State Key Laboratories of Agrobiotechnology, Beijing Key Laboratory of Growth and Developmental Regulation for Protected Vegetable Crops, MOE Joint Laboratory for International Cooperation in Crop Molecular Breeding, China Agricultural University, Beijing, China – sequence: 7 givenname: Hailing surname: Zi fullname: Zi, Hailing organization: Shanghai Center for Plant Stress Biology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai, China – sequence: 8 givenname: Zhihua surname: Cheng fullname: Cheng, Zhihua organization: State Key Laboratories of Agrobiotechnology, Beijing Key Laboratory of Growth and Developmental Regulation for Protected Vegetable Crops, MOE Joint Laboratory for International Cooperation in Crop Molecular Breeding, China Agricultural University, Beijing, China – sequence: 9 givenname: Xuexian surname: Li fullname: Li, Xuexian organization: Department of Plant Nutrition, the Key Laboratory of Plant-Soil Interactions, China Agricultural University, Beijing, China – sequence: 10 givenname: Hongyan surname: Shan fullname: Shan, Hongyan organization: State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Beijing, China – sequence: 11 givenname: Qingyang surname: Lv fullname: Lv, Qingyang organization: Department of Plant Pathology, China Agricultural University, Beijing, China – sequence: 12 givenname: Laixin surname: Luo fullname: Luo, Laixin organization: Department of Plant Pathology, China Agricultural University, Beijing, China – sequence: 13 givenname: Renyi orcidid: 0000-0002-2534-4171 surname: Liu fullname: Liu, Renyi organization: College of Horticulture, and FAFU-UCR Joint Center for Horticultural Biology and Metabolomics, Haixia Institute of Science and Technology, Fujian Agriculture and Forestry University, Fuzhou, China – sequence: 14 givenname: Liying surname: Yan fullname: Yan, Liying organization: College of Horticulture Science and Technology, Hebei Normal University of Science & Technology, Qinhuangdao, China – sequence: 15 givenname: Zhaoyang surname: Zhou fullname: Zhou, Zhaoyang organization: State Key Laboratories of Agrobiotechnology, Beijing Key Laboratory of Growth and Developmental Regulation for Protected Vegetable Crops, MOE Joint Laboratory for International Cooperation in Crop Molecular Breeding, China Agricultural University, Beijing, China – sequence: 16 givenname: William John surname: Lucas fullname: Lucas, William John organization: Department of Plant Biology, University of California, Davis, California, United States of America – sequence: 17 givenname: Xiaolan orcidid: 0000-0002-6343-3116 surname: Zhang fullname: Zhang, Xiaolan organization: State Key Laboratories of Agrobiotechnology, Beijing Key Laboratory of Growth and Developmental Regulation for Protected Vegetable Crops, MOE Joint Laboratory for International Cooperation in Crop Molecular Breeding, China Agricultural University, Beijing, China |
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Copyright | 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. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. 2020 Yan et al 2020 Yan et al |
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SubjectTerms | Agriculture Airborne microorganisms Biology Biology and Life Sciences Crop diseases Crop yield Crops Disease resistance Domestication Downy mildew 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-mediated interference Salicylic acid Signal transduction Transcription factors Vascular tissue |
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Title | CsIVP functions in vasculature development and downy mildew resistance in cucumber |
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