Cotton miR393-TIR1 Module Regulates Plant Defense Against <i>Verticillium dahliae</i> via Auxin Perception and Signaling

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Abstract

Plant auxin is essential in plant growth and development. However, the molecular mechanisms of auxin involvement in plant immunity are unclear. Here, we addressed the function of the cotton ( Gossypium hirsutum) miR393-TIR1 module in plant defense against Verticillium dahliae infection via auxin perception and signaling. GhTIR1 was directedly cleaved by ghr-miR393 according to mRNA degradome data, 5′-RACE analysis, and a GUS reporter assay. Ghr-miR393 knockdown significantly increased plant susceptibility to V. dahliae compared to the control, while ghr-miR393 overexpression and GhTIR1 knockdown significantly increased plant resistance. External indole-3-acetic acid (IAA) application significantly enhanced susceptibility to V. dahliae in ghr-miR393 knockdown and control plants compared to mock treatment, and only slightly increased susceptibility in overexpressing ghr-miR393 and GhTIR1-silenced plants. Application of external PEO-IAA (an auxin antagonist) had a contrary trend with IAA application. Based on yeast two-hybrid and bimolecular fluorescence complementation assays, GhTIR1 interacted with GhIAA14 in the nucleus, and GhIAA14 knockdown reduced plant resistance to V. dahliae infection. The results suggested that the ghr-miR393-GhTIR1 module regulates plant defense via auxin perception and signaling. Additionally, simultaneous knockdown of GhTIR1 and GhICS1 significantly increased plant susceptibility to V. dahliae compared to the control, indicating that salicylic acid (SA) accumulation is vital for the ghr-miR393-GhTIR1 module to regulates plant resistance. Transcriptome data also demonstrated that GhTIR1 knockdown significantly downregulated expression of auxin-related genes and upregulated expression of SA-related genes. Overall, the ghr-miR393-GhTIR1 module participates in plant response to V. dahliae infection via IAA perception and signaling partially depending on the SA defense pathway.

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Most cited references 46

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MicroRNAs (miRNAs) and short interfering RNAs (siRNAs) are small noncoding RNAs that have recently emerged as important regulators of mRNA degradation, translational repression, and chromatin modification. In Arabidopsis thaliana, 43 miRNAs comprising 15 families have been reported thus far. In an attempt to identify novel and abiotic stress regulated miRNAs and siRNAs, we constructed a library of small RNAs from Arabidopsis seedlings exposed to dehydration, salinity, or cold stress or to the plant stress hormone abscisic acid. Sequencing of the library and subsequent analysis revealed 26 new miRNAs from 34 loci, forming 15 new families. Two of the new miRNAs from three loci are members of previously reported miR171 and miR319 families. Some of the miRNAs are preferentially expressed in specific tissues, and several are either upregulated or downregulated by abiotic stresses. Ten of the miRNAs are highly conserved in other plant species. Fifty-one potential targets with diverse function were predicted for the newly identified miRNAs based on sequence complementarity. In addition to miRNAs, we identified 102 other novel endogenous small RNAs in Arabidopsis. These findings suggest that a large number of miRNAs and other small regulatory RNAs are encoded by the Arabidopsis genome and that some of them may play important roles in plant responses to environmental stresses as well as in development and genome maintenance.

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GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants.

R A Jefferson, T. Kavanagh, M W Bevan (1987)

We have used the Escherichia coli beta-glucuronidase gene (GUS) as a gene fusion marker for analysis of gene expression in transformed plants. Higher plants tested lack intrinsic beta-glucuronidase activity, thus enhancing the sensitivity with which measurements can be made. We have constructed gene fusions using the cauliflower mosaic virus (CaMV) 35S promoter or the promoter from a gene encoding the small subunit of ribulose bisphosphate carboxylase (rbcS) to direct the expression of beta-glucuronidase in transformed plants. Expression of GUS can be measured accurately using fluorometric assays of very small amounts of transformed plant tissue. Plants expressing GUS are normal, healthy and fertile. GUS is very stable, and tissue extracts continue to show high levels of GUS activity after prolonged storage. Histochemical analysis has been used to demonstrate the localization of gene activity in cells and tissues of transformed plants.

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Auxin and plant-microbe interactions.

Stijn Spaepen, Jos Vanderleyden (2011)

Microbial synthesis of the phytohormone auxin has been known for a long time. This property is best documented for bacteria that interact with plants because bacterial auxin can cause interference with the many plant developmental processes regulated by auxin. Auxin biosynthesis in bacteria can occur via multiple pathways as has been observed in plants. There is also increasing evidence that indole-3-acetic acid (IAA), the major naturally occurring auxin, is a signaling molecule in microorganisms because IAA affects gene expression in some microorganisms. Therefore, IAA can act as a reciprocal signaling molecule in microbe-plant interactions. Interest in microbial synthesis of auxin is also increasing in yet another recently discovered property of auxin in Arabidopsis. Down-regulation of auxin signaling is part of the plant defense system against phytopathogenic bacteria. Exogenous application of auxin, e.g., produced by the pathogen, enhances susceptibility to the bacterial pathogen.

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Author and article information

Contributors

Peng Wang: URI : http://loop.frontiersin.org/people/472578/overview

Jingjing Zhan: URI : http://loop.frontiersin.org/people/812200/overview

Ge Zhao: URI : http://loop.frontiersin.org/people/466117/overview

Fuguang Li: URI : http://loop.frontiersin.org/people/1237481/overview

Xiaoyang Ge: URI : http://loop.frontiersin.org/people/753525/overview

Jiahe Wu: URI : http://loop.frontiersin.org/people/232084/overview

Journal

Journal ID (nlm-ta): Front Plant Sci

Journal ID (iso-abbrev): Front Plant Sci

Journal ID (publisher-id): Front. Plant Sci.

Title: Frontiers in Plant Science

Publisher: Frontiers Media S.A.

ISSN (Electronic): 1664-462X

Publication date (Electronic): 03 May 2022

Publication date Collection: 2022

Volume: 13

Electronic Location Identifier: 888703

Affiliations

[1] ¹Zhengzhou Research Base, State Key Laboratory of Cotton Biology, School of Agricultural Sciences, Zhengzhou University , Zhengzhou, China

[2] ²State Key Laboratory of Cotton Biology, Institute of Cotton Research of Chinese Academy of Agricultural Sciences , Anyang, China

[3] ³The State Key Laboratory of Plant Genomics, Institute of Microbiology, Chinese Academy of Sciences , Beijing, China

Author notes

Edited by: Wen-Ming Wang, Sichuan Agricultural University, China

Reviewed by: Xing Fen Wang, Hebei Agricultural University, China; Yan Li, Sichuan Agricultural University, China

*Correspondence: Xiaoyang Ge, gexiaoyang@ 123456caas.cn

Jiahe Wu, wujiahe@ 123456im.ac.cn

^†These authors have contributed equally to this work

This article was submitted to Plant Pathogen Interactions, a section of the journal Frontiers in Plant Science

Article

DOI: 10.3389/fpls.2022.888703

PMC ID: 9111529

PubMed ID: 35592575

SO-VID: 4807da9e-b072-4c01-9f29-228d490540cf

License:

This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

History

Date received : 03 March 2022

Date accepted : 24 March 2022

Page count

Figures: 12, Tables: 0, Equations: 0, References: 46, Pages: 16, Words: 8990

Funding

Funded by: National Natural Science Foundation of China, doi 10.13039/501100001809;

Cotton miR393-TIR1 Module Regulates Plant Defense Against Verticillium dahliae via Auxin Perception and Signaling

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Abstract

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Plant MYBs

Most cited references 46

Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis.

GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants.

Auxin and plant-microbe interactions.

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