Cotton miR319b-Targeted TCP4-Like Enhances Plant Defense Against Verticillium dahliae by Activating GhICS1 Transcription Expression

Teosinte branched1/Cincinnata/proliferating cell factor (TCP) transcription factors play important roles in plant growth and defense. However, the molecular mechanisms of TCPs participating in plant defense remain unclear. Here, we characterized a cotton TCP4-like fine-tuned by miR319b, which could...

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Main Authors: Pei Jia, Ye Tang, Guang Hu, Yonggang Quan, Aimin Chen, Naiqin Zhong, Qingzhong Peng, Jiahe Wu
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-05-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2022.870882/full
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author Pei Jia
Pei Jia
Ye Tang
Ye Tang
Guang Hu
Yonggang Quan
Aimin Chen
Naiqin Zhong
Qingzhong Peng
Jiahe Wu
Jiahe Wu
author_facet Pei Jia
Pei Jia
Ye Tang
Ye Tang
Guang Hu
Yonggang Quan
Aimin Chen
Naiqin Zhong
Qingzhong Peng
Jiahe Wu
Jiahe Wu
author_sort Pei Jia
collection DOAJ
description Teosinte branched1/Cincinnata/proliferating cell factor (TCP) transcription factors play important roles in plant growth and defense. However, the molecular mechanisms of TCPs participating in plant defense remain unclear. Here, we characterized a cotton TCP4-like fine-tuned by miR319b, which could interact with NON-EXPRESSER OF PATHOGEN-RELATED GENES 1 (NPR1) to directly activate isochorismate synthase 1 (ICS1) expression, facilitating plant resistance against Verticillium dahliae. mRNA degradome data and GUS-fused assay showed that GhTCP4-like mRNA was directedly cleaved by ghr-miR319b. Knockdown of ghr-miR319b increased plant resistance to V. dahliae, whereas silencing GhTCP4-like increased plant susceptibility by the virus-induced gene silencing (VIGS) method, suggesting that GhTCP4-like is a positive regulator of plant defense. According to the electrophoretic mobility shift assay and GUS reporter analysis, GhTCP4-like could transcriptionally activate GhICS1 expression, resulting in increased salicylic acid (SA) accumulation. Yeast two-hybrid and luciferase complementation image analyses demonstrated that GhTCP4-like interacts with GhNPR1, which can promote GhTCP4-like transcriptional activation in GhICS1 expression according to the GUS reporter assay. Together, these results revealed that GhTCP4-like interacts with GhNPR1 to promote GhICS1 expression through fine-tuning of ghr-miR319b, leading to SA accumulation, which is percepted by NPR1 to increase plant defense against V. dahliae. Therefore, GhTCP4-like participates in a positive feedback regulation loop of SA biosynthesis via NPR1, increasing plant defenses against fungal infection.
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spelling doaj.art-a65355724efa45ee905f994d593f31ba2022-12-22T03:27:11ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2022-05-011310.3389/fpls.2022.870882870882Cotton miR319b-Targeted TCP4-Like Enhances Plant Defense Against Verticillium dahliae by Activating GhICS1 Transcription ExpressionPei Jia0Pei Jia1Ye Tang2Ye Tang3Guang Hu4Yonggang Quan5Aimin Chen6Naiqin Zhong7Qingzhong Peng8Jiahe Wu9Jiahe Wu10Hunan Provincial Key Laboratory of Plant Resources Conservation and Utilization, College of Biology and Environmental Sciences, Jishou University, Jishou, ChinaState Key Laboratory of Plant Genomics, Institute of Microbiology, Chinese Academy of Sciences, Beijing, ChinaHunan Provincial Key Laboratory of Plant Resources Conservation and Utilization, College of Biology and Environmental Sciences, Jishou University, Jishou, ChinaState Key Laboratory of Plant Genomics, Institute of Microbiology, Chinese Academy of Sciences, Beijing, ChinaState Key Laboratory of Plant Genomics, Institute of Microbiology, Chinese Academy of Sciences, Beijing, ChinaThe Key Laboratory for the Creation of Cotton Varieties in the Northwest, Ministry of Agriculture, Join Hope Seeds Co. Ltd., Changji, ChinaThe Key Laboratory for the Creation of Cotton Varieties in the Northwest, Ministry of Agriculture, Join Hope Seeds Co. Ltd., Changji, ChinaState Key Laboratory of Plant Genomics, Institute of Microbiology, Chinese Academy of Sciences, Beijing, ChinaHunan Provincial Key Laboratory of Plant Resources Conservation and Utilization, College of Biology and Environmental Sciences, Jishou University, Jishou, ChinaHunan Provincial Key Laboratory of Plant Resources Conservation and Utilization, College of Biology and Environmental Sciences, Jishou University, Jishou, ChinaState Key Laboratory of Plant Genomics, Institute of Microbiology, Chinese Academy of Sciences, Beijing, ChinaTeosinte branched1/Cincinnata/proliferating cell factor (TCP) transcription factors play important roles in plant growth and defense. However, the molecular mechanisms of TCPs participating in plant defense remain unclear. Here, we characterized a cotton TCP4-like fine-tuned by miR319b, which could interact with NON-EXPRESSER OF PATHOGEN-RELATED GENES 1 (NPR1) to directly activate isochorismate synthase 1 (ICS1) expression, facilitating plant resistance against Verticillium dahliae. mRNA degradome data and GUS-fused assay showed that GhTCP4-like mRNA was directedly cleaved by ghr-miR319b. Knockdown of ghr-miR319b increased plant resistance to V. dahliae, whereas silencing GhTCP4-like increased plant susceptibility by the virus-induced gene silencing (VIGS) method, suggesting that GhTCP4-like is a positive regulator of plant defense. According to the electrophoretic mobility shift assay and GUS reporter analysis, GhTCP4-like could transcriptionally activate GhICS1 expression, resulting in increased salicylic acid (SA) accumulation. Yeast two-hybrid and luciferase complementation image analyses demonstrated that GhTCP4-like interacts with GhNPR1, which can promote GhTCP4-like transcriptional activation in GhICS1 expression according to the GUS reporter assay. Together, these results revealed that GhTCP4-like interacts with GhNPR1 to promote GhICS1 expression through fine-tuning of ghr-miR319b, leading to SA accumulation, which is percepted by NPR1 to increase plant defense against V. dahliae. Therefore, GhTCP4-like participates in a positive feedback regulation loop of SA biosynthesis via NPR1, increasing plant defenses against fungal infection.https://www.frontiersin.org/articles/10.3389/fpls.2022.870882/fullGossypium hirsutumVerticillium dahliaGhTCP4-likeGhICS1ghr-miR319b
spellingShingle Pei Jia
Pei Jia
Ye Tang
Ye Tang
Guang Hu
Yonggang Quan
Aimin Chen
Naiqin Zhong
Qingzhong Peng
Jiahe Wu
Jiahe Wu
Cotton miR319b-Targeted TCP4-Like Enhances Plant Defense Against Verticillium dahliae by Activating GhICS1 Transcription Expression
Frontiers in Plant Science
Gossypium hirsutum
Verticillium dahlia
GhTCP4-like
GhICS1
ghr-miR319b
title Cotton miR319b-Targeted TCP4-Like Enhances Plant Defense Against Verticillium dahliae by Activating GhICS1 Transcription Expression
title_full Cotton miR319b-Targeted TCP4-Like Enhances Plant Defense Against Verticillium dahliae by Activating GhICS1 Transcription Expression
title_fullStr Cotton miR319b-Targeted TCP4-Like Enhances Plant Defense Against Verticillium dahliae by Activating GhICS1 Transcription Expression
title_full_unstemmed Cotton miR319b-Targeted TCP4-Like Enhances Plant Defense Against Verticillium dahliae by Activating GhICS1 Transcription Expression
title_short Cotton miR319b-Targeted TCP4-Like Enhances Plant Defense Against Verticillium dahliae by Activating GhICS1 Transcription Expression
title_sort cotton mir319b targeted tcp4 like enhances plant defense against verticillium dahliae by activating ghics1 transcription expression
topic Gossypium hirsutum
Verticillium dahlia
GhTCP4-like
GhICS1
ghr-miR319b
url https://www.frontiersin.org/articles/10.3389/fpls.2022.870882/full
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