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Title: MicroRNAs Suppress NB Domain Genes in Tomato That Confer Resistance to Fusarium oxysporum

Abstract

MicroRNAs (miRNAs) suppress the transcriptional and post-transcriptional expression of genes in plants. Several miRNA families target genes encoding nucleotide-binding site–leucine-rich repeat (NB-LRR) plant innate immune receptors. The fungus Fusarium oxysporum f. sp. lycopersici causes vascular wilt disease in tomato. Here, we explored a role for miRNAs in tomato defense against F. oxysporum using comparative miRNA profiling of susceptible (Moneymaker) and resistant (Motelle) tomato cultivars. slmiR482f and slmiR5300 were repressed during infection of Motelle with F. oxysporum. Two predicted mRNA targets each of slmiR482f and slmiR5300 exhibited increased expression in Motelle and the ability of these four targets to be regulated by the miRNAs was confirmed by co-expression in Nicotiana benthamiana. Silencing of the targets in the resistant Motelle cultivar revealed a role in fungal resistance for all four genes. All four targets encode proteins with full or partial nucleotide-binding (NB) domains. One slmiR5300 target corresponds to tm-2, a susceptible allele of the Tomato Mosaic Virus resistance gene, supporting functions in immunity to a fungal pathogen. The observation that none of the targets correspond to I-2, the only known resistance (R) gene for F. oxysporum in tomato, supports roles for additional R genes in the immune response. In conclusion, taken together,more » our findings suggest that Moneymaker is highly susceptible because its potential resistance is insufficiently expressed due to the action of miRNAs.« less

Authors:
 [1];  [1];  [1];  [2];  [1];  [1];  [1]
  1. Univ. of California, Riverside, CA (United States). Inst. for Integrative Genome Biology
  2. Los Alamos National Lab. (LANL), Los Alamos, NM (United States). Bioscience Division
Publication Date:
Research Org.:
Los Alamos National Laboratory (LANL), Los Alamos, NM (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1263545
Resource Type:
Accepted Manuscript
Journal Name:
PLoS Pathogens
Additional Journal Information:
Journal Volume: 10; Journal Issue: 10; Journal ID: ISSN 1553-7374
Publisher:
Public Library of Science
Country of Publication:
United States
Language:
English
Subject:
60 APPLIED LIFE SCIENCES; MicroRNAs; Fusarium oxysporum; Tomato; Protein domains; Gene expression; Messenger RNA; Infectious disease control

Citation Formats

Ouyang, Shouqiang, Park, Gyungsoon, Atamian, Hagop S., Han, Cliff S., Stajich, Jason E., Kaloshian, Isgouhi, and Borkovich, Katherine A. MicroRNAs Suppress NB Domain Genes in Tomato That Confer Resistance to Fusarium oxysporum. United States: N. p., 2014. Web. doi:10.1371/journal.ppat.1004464.
Ouyang, Shouqiang, Park, Gyungsoon, Atamian, Hagop S., Han, Cliff S., Stajich, Jason E., Kaloshian, Isgouhi, & Borkovich, Katherine A. MicroRNAs Suppress NB Domain Genes in Tomato That Confer Resistance to Fusarium oxysporum. United States. https://doi.org/10.1371/journal.ppat.1004464
Ouyang, Shouqiang, Park, Gyungsoon, Atamian, Hagop S., Han, Cliff S., Stajich, Jason E., Kaloshian, Isgouhi, and Borkovich, Katherine A. Thu . "MicroRNAs Suppress NB Domain Genes in Tomato That Confer Resistance to Fusarium oxysporum". United States. https://doi.org/10.1371/journal.ppat.1004464. https://www.osti.gov/servlets/purl/1263545.
@article{osti_1263545,
title = {MicroRNAs Suppress NB Domain Genes in Tomato That Confer Resistance to Fusarium oxysporum},
author = {Ouyang, Shouqiang and Park, Gyungsoon and Atamian, Hagop S. and Han, Cliff S. and Stajich, Jason E. and Kaloshian, Isgouhi and Borkovich, Katherine A.},
abstractNote = {MicroRNAs (miRNAs) suppress the transcriptional and post-transcriptional expression of genes in plants. Several miRNA families target genes encoding nucleotide-binding site–leucine-rich repeat (NB-LRR) plant innate immune receptors. The fungus Fusarium oxysporum f. sp. lycopersici causes vascular wilt disease in tomato. Here, we explored a role for miRNAs in tomato defense against F. oxysporum using comparative miRNA profiling of susceptible (Moneymaker) and resistant (Motelle) tomato cultivars. slmiR482f and slmiR5300 were repressed during infection of Motelle with F. oxysporum. Two predicted mRNA targets each of slmiR482f and slmiR5300 exhibited increased expression in Motelle and the ability of these four targets to be regulated by the miRNAs was confirmed by co-expression in Nicotiana benthamiana. Silencing of the targets in the resistant Motelle cultivar revealed a role in fungal resistance for all four genes. All four targets encode proteins with full or partial nucleotide-binding (NB) domains. One slmiR5300 target corresponds to tm-2, a susceptible allele of the Tomato Mosaic Virus resistance gene, supporting functions in immunity to a fungal pathogen. The observation that none of the targets correspond to I-2, the only known resistance (R) gene for F. oxysporum in tomato, supports roles for additional R genes in the immune response. In conclusion, taken together, our findings suggest that Moneymaker is highly susceptible because its potential resistance is insufficiently expressed due to the action of miRNAs.},
doi = {10.1371/journal.ppat.1004464},
journal = {PLoS Pathogens},
number = 10,
volume = 10,
place = {United States},
year = {Thu Oct 16 00:00:00 EDT 2014},
month = {Thu Oct 16 00:00:00 EDT 2014}
}

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journal, February 2018

  • Islam, Waqar; Noman, Ali; Qasim, Muhammad
  • International Journal of Molecular Sciences, Vol. 19, Issue 2
  • DOI: 10.3390/ijms19020515

Evolution of Disease Defense Genes and Their Regulators in Plants
journal, January 2019

  • Zhang, Rongzhi; Zheng, Fengya; Wei, Shugen
  • International Journal of Molecular Sciences, Vol. 20, Issue 2
  • DOI: 10.3390/ijms20020335

Lineage-Specific Evolved MicroRNAs Regulating NB-LRR Defense Genes in Triticeae
journal, June 2019

  • Zhang, Rongzhi; Zhang, Shujuan; Hao, Weiwei
  • International Journal of Molecular Sciences, Vol. 20, Issue 13, p. 3128
  • DOI: 10.3390/ijms20133128

Roles of Small RNAs in Virus-Plant Interactions
journal, September 2019

  • Zhang, Baogang; Li, Wenji; Zhang, Jialin
  • Viruses, Vol. 11, Issue 9
  • DOI: 10.3390/v11090827

Function identification of miR482b, a negative regulator during tomato resistance to Phytophthora infestans
journal, March 2018


Small RNAs, emerging regulators critical for the development of horticultural traits
journal, September 2018


Functional genomics of tomato for the study of plant immunity: Table 1
journal, March 2015

  • Rosli, Hernan G.; Martin, Gregory B.
  • Briefings in Functional Genomics, Vol. 14, Issue 4
  • DOI: 10.1093/bfgp/elv007

MiRNA160 is associated with local defense and systemic acquired resistance against Phytophthora infestans infection in potato
journal, January 2018

  • Natarajan, Bhavani; Kalsi, Harpreet S.; Godbole, Prajakta
  • Journal of Experimental Botany, Vol. 69, Issue 8
  • DOI: 10.1093/jxb/ery025

Expression profiling across wild and cultivated tomatoes supports the relevance of early miR482/2118 suppression for Phytophthora resistance
journal, February 2018

  • de Vries, Sophie; Kukuk, Andreas; von Dahlen, Janina K.
  • Proceedings of the Royal Society B: Biological Sciences, Vol. 285, Issue 1873
  • DOI: 10.1098/rspb.2017.2560

Salicylic acid perturbs sRNA-gibberellin regulatory network in immune response of potato to Potato virus Y infection
journal, October 2017

  • Kriznik, Maja; Petek, Marko; Dobnik, David
  • Frontiers in Plant Science
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Origin and evolution of the plant immune system
journal, January 2019


A novel fungal effector from Puccinia graminis suppressing RNA silencing and plant defense responses
journal, February 2019

  • Yin, Chuntao; Ramachandran, Sowmya R.; Zhai, Ying
  • New Phytologist, Vol. 222, Issue 3
  • DOI: 10.1111/nph.15676

Small RNA profiling of Cavendish banana roots inoculated with Fusarium oxysporum f. sp. cubense race 1 and tropical race 4
journal, June 2019

  • Fei, Shulang; Czislowski, Elizabeth; Fletcher, Stephen
  • Phytopathology Research, Vol. 1, Issue 1
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Metabolic Impacts of Using Nitrogen and Copper-Regulated Promoters to Regulate Gene Expression in Neurospora crassa
journal, September 2015

  • Ouyang, Shouqiang; Beecher, Consuelo N.; Wang, Kang
  • G3 Genes|Genomes|Genetics, Vol. 5, Issue 9
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Enhanced resistance to bacterial and oomycete pathogens by short tandem target mimic RNAs in tomato
text, January 2019

  • Baulcombe, David; Canto Pastor, Alex; Santos, Bacm
  • Apollo - University of Cambridge Repository
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Function of miR825 and miR825* as Negative Regulators in Bacillus cereus AR156-elicited Systemic Resistance to Botrytis cinerea in Arabidopsis thaliana
journal, October 2019

  • Nie, Pingping; Chen, Chen; Yin, Qian
  • International Journal of Molecular Sciences, Vol. 20, Issue 20
  • DOI: 10.3390/ijms20205032

Enhanced resistance to bacterial and oomycete pathogens by short tandem target mimic RNAs in tomato
journal, August 2018

  • Canto-Pastor, Alex; Santos, Bruno AMC.; Valli, Adrian A.
  • Proceedings of the National Academy of Sciences
  • DOI: 10.1101/396564

The function of small RNAs in plant biotic stress response: Small RNAs and biotic stress
journal, February 2016

  • Huang, Juan; Yang, Meiling; Zhang, Xiaoming
  • Journal of Integrative Plant Biology, Vol. 58, Issue 4
  • DOI: 10.1111/jipb.12463

Nanotechnology based approaches for detection and delivery of microRNA in healthcare and crop protection
journal, April 2018

  • Chaudhary, Vrantika; Jangra, Sumit; Yadav, Neelam R.
  • Journal of Nanobiotechnology, Vol. 16, Issue 1
  • DOI: 10.1186/s12951-018-0368-8

Enhanced resistance to bacterial and oomycete pathogens by short tandem target mimic RNAs in tomato
journal, January 2019

  • Canto-Pastor, Alex; Santos, Bruno A. M. C.; Valli, Adrian A.
  • Proceedings of the National Academy of Sciences, Vol. 116, Issue 7
  • DOI: 10.1073/pnas.1814380116

Osa-miR169 Negatively Regulates Rice Immunity against the Blast Fungus Magnaporthe oryzae
journal, January 2017


Salicylic Acid Perturbs sRNA-Gibberellin Regulatory Network in Immune Response of Potato to Potato virus Y Infection
journal, December 2017


Cryptochrome 2 extensively regulates transcription of the chloroplast genome in tomato
journal, March 2017


Effects of cultivation ages and modes on microbial diversity in the rhizosphere soil of Panax ginseng
journal, January 2016


Function identification of miR482b, a negative regulator during tomato resistance to Phytophthora infestans
journal, March 2018


New insights into tomato microRNAs
journal, October 2018

  • Cardoso, Thaís Cunha de Sousa; Alves, Tamires Caixeta; Caneschi, Carolina Milagres
  • Scientific Reports, Vol. 8, Issue 1
  • DOI: 10.1038/s41598-018-34202-3

Integrated miRNA and mRNA expression profiling reveals the response regulators of a susceptible tomato cultivar to early blight disease
journal, March 2017

  • Sarkar, Deepti; Maji, Ranjan Kumar; Dey, Sayani
  • DNA Research, Vol. 24, Issue 3
  • DOI: 10.1093/dnares/dsx003

MiRNA160 is associated with local defense and systemic acquired resistance against Phytophthora infestans infection in potato
journal, January 2018

  • Natarajan, Bhavani; Kalsi, Harpreet S.; Godbole, Prajakta
  • Journal of Experimental Botany, Vol. 69, Issue 8
  • DOI: 10.1093/jxb/ery025

Expression profiling across wild and cultivated tomatoes supports the relevance of early miR482/2118 suppression for Phytophthora resistance
journal, February 2018

  • de Vries, Sophie; Kukuk, Andreas; von Dahlen, Janina K.
  • Proceedings of the Royal Society B: Biological Sciences, Vol. 285, Issue 1873
  • DOI: 10.1098/rspb.2017.2560

Nanotechnology based approaches for detection and delivery of microRNA in healthcare and crop protection
journal, April 2018

  • Chaudhary, Vrantika; Jangra, Sumit; Yadav, Neelam R.
  • Journal of Nanobiotechnology, Vol. 16, Issue 1
  • DOI: 10.1186/s12951-018-0368-8

A role for small RNA in regulating innate immunity during plant growth
journal, January 2018


MicroRNA-Mediated Gene Silencing in Plant Defense and Viral Counter-Defense
journal, September 2017


Osa-miR169 Negatively Regulates Rice Immunity against the Blast Fungus Magnaporthe oryzae
journal, January 2017


Functional Roles of microRNAs in Agronomically Important Plants—Potential as Targets for Crop Improvement and Protection
journal, March 2017

  • Djami-Tchatchou, Arnaud T.; Sanan-Mishra, Neeti; Ntushelo, Khayalethu
  • Frontiers in Plant Science, Vol. 8
  • DOI: 10.3389/fpls.2017.00378

Comparative Transcriptome Profiles of Near-Isogenic Hexaploid Wheat Lines Differing for Effective Alleles at the 2DL FHB Resistance QTL
journal, January 2018

  • Biselli, Chiara; Bagnaresi, Paolo; Faccioli, Primetta
  • Frontiers in Plant Science, Vol. 9
  • DOI: 10.3389/fpls.2018.00037

RNA Interference: A Natural Immune System of Plants to Counteract Biotic Stressors
journal, January 2019


Evolution of Disease Defense Genes and Their Regulators in Plants
journal, January 2019

  • Zhang, Rongzhi; Zheng, Fengya; Wei, Shugen
  • International Journal of Molecular Sciences, Vol. 20, Issue 2
  • DOI: 10.3390/ijms20020335

Lineage-Specific Evolved MicroRNAs Regulating NB-LRR Defense Genes in Triticeae
journal, June 2019

  • Zhang, Rongzhi; Zhang, Shujuan; Hao, Weiwei
  • International Journal of Molecular Sciences, Vol. 20, Issue 13, p. 3128
  • DOI: 10.3390/ijms20133128

Function of miR825 and miR825* as Negative Regulators in Bacillus cereus AR156-elicited Systemic Resistance to Botrytis cinerea in Arabidopsis thaliana
journal, October 2019

  • Nie, Pingping; Chen, Chen; Yin, Qian
  • International Journal of Molecular Sciences, Vol. 20, Issue 20
  • DOI: 10.3390/ijms20205032

From Nucleotides to Satellite Imagery: Approaches to Identify and Manage the Invasive Pathogen Xylella fastidiosa and Its Insect Vectors in Europe
journal, June 2020

  • Raffini, Francesca; Bertorelle, Giorgio; Biello, Roberto
  • Sustainability, Vol. 12, Issue 11
  • DOI: 10.3390/su12114508

Roles of Small RNAs in Virus-Plant Interactions
journal, September 2019

  • Zhang, Baogang; Li, Wenji; Zhang, Jialin
  • Viruses, Vol. 11, Issue 9
  • DOI: 10.3390/v11090827