MicroRNA400-Guided Cleavage of Pentatricopeptide Repeat Protein mRNAs Renders Arabidopsis thaliana More Susceptible to Pathogenic Bacteria and Fungi

Park, Young Ju; Lee, Hwa Jung; Kwak, Kyung Jin; Lee, Kwanuk; Hong, Suk Whan; Kang, Hunseung

doi:10.1093/pcp/pcu096

Cited by 94 publications

(70 citation statements)

References 53 publications

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“…Distinct miRNAs have been linked to the genetic programs involved in plant defense, although little is known about the molecular mechanisms underlying their role in those processes155051. Even less is known about these mechanisms of defense against fungal pathogens as most studies carried out in Arabidopsis so far have focused on the role of miRNAs in immunity against the bacterial pathogen Pseudomonas syringae 12155152.…”

Section: Discussionmentioning

confidence: 99%

The Arabidopsis miR396 mediates pathogen-associated molecular pattern-triggered immune responses against fungal pathogens

Soto-Suárez

Baldrich

Weigel

et al. 2017

Sci Rep

115

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MicroRNAs (miRNAs) play a pivotal role in regulating gene expression during plant development. Although a substantial fraction of plant miRNAs has proven responsive to pathogen infection, their role in disease resistance remains largely unknown, especially during fungal infections. In this study, we screened Arabidopsis thaliana lines in which miRNA activity has been reduced using artificial miRNA target mimics (MIM lines) for their response to fungal pathogens. Reduced activity of miR396 (MIM396 plants) was found to confer broad resistance to necrotrophic and hemibiotrophic fungal pathogens. MiR396 levels gradually decreased during fungal infection, thus, enabling its GRF (GROWTH-REGULATING FACTOR) transcription factor target genes to trigger host reprogramming. Pathogen resistance in MIM396 plants is based on a superactivation of defense responses consistent with a priming event during pathogen infection. Notably, low levels of miR396 are not translated in developmental defects in absence of pathogen challenge. Our findings support a role of miR396 in regulating plant immunity, and broaden our knowledge about the molecular players and processes that sustain defense priming. That miR396 modulates innate immunity without growth costs also suggests fine-tuning of miR396 levels as an effective biotechnological means for protection against pathogen infection.

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Section: Discussionmentioning

confidence: 99%

The Arabidopsis miR396 mediates pathogen-associated molecular pattern-triggered immune responses against fungal pathogens

Soto-Suárez

Baldrich

Weigel

et al. 2017

Sci Rep

115

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“…It is defined that the PPR proteins have tandem repeats of 35 amino acid motifs which form an extended binding surface that can recognize RNA sequences and mediate protein-protein interaction (Barkan and Small 2014). In Arabidopsis, cleavage of a PPR protein mRNA made the plant more susceptible to bacteria and fungi (Park et al 2014). Based on the protein analysis, there was only one deleterious SNP identified which would affect the protein function and potentially may impact on the biological function of this protein.…”

Section: Discussionmentioning

confidence: 99%

Genetic mapping and haplotype analysis of a locus for quantitative resistance to Fusarium graminearum in soybean accession PI 567516C

et al. 2017

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A major novel quantitative disease resistance locus, qRfg_Gm06, for Fusarium graminearum was genetically mapped to chromosome 6. Genomic-assisted haplotype analysis within this region identified three putative candidate genes. Fusarium graminearum causes seed, root rot, and seedling damping-off in soybean which contributes to reduced stands and yield. A cultivar Magellan and PI 567516C were identified with low and high levels of partial resistance to F. graminearum, respectively. Quantitative disease resistance loci (QDRL) were mapped with 241 F recombinant inbred lines (RILs) derived from a cross of Magellan × PI 567516C. Phenotypic evaluation for resistance to F. graminearum used the rolled towel assay in a randomized incomplete block design. The genetic map was constructed from 927 polymorphic single nucleotide polymorphism (SNP) and simple sequence repeat (SSR) markers. One major QDRL qRfg_Gm06 was detected and mapped to chromosome 6 with a LOD score of 20.3 explaining 40.2% of the total phenotypic variation. This QDRL was mapped to a ~400 kb genomic region of the Williams 82 reference genome. Genome mining of this region identified 14 putative candidate disease resistance genes. Haplotype analysis of this locus using whole genome re-sequencing (WGRS) of 106 diverse soybean lines narrowed the list to three genes. A SNP genotyping Kompetitive allele-specific PCR (KASP) assay was designed for one of the genes and was validated in a subset of the RILs and all 106 diverse lines.

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“…miR400-directed cleavage of PPR genes rendered Arabidopsis plants more susceptible to the bacterium Pseudomonas syringae pv. tomato DC3000 and the fungus Botrytis cinerea (Park et al, 2014b). By contrast, differential gene expression analysis pointed to the implication of several rice miRNAs in immunity against the blast fungus Magnaporthe oryzae (Li et al, 2014).…”

Section: Introductionmentioning

confidence: 97%

Arabidopsis miR827 mediates post‐transcriptional gene silencing of its ubiquitin E3 ligase target gene in the syncytium of the cyst nematode Heterodera schachtii to enhance susceptibility

Hewezi

Piya

et al. 2016

The Plant Journal

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MicroRNAs (miRNAs) are a major class of small non-coding RNAs with emerging functions in biotic and abiotic interactions. Here, we report on a new functional role of Arabidopsis miR827 and its NITROGEN LIMITATION ADAPTATION (NLA) target gene in mediating plant susceptibility to the beet cyst nematode Heterodera schachtii. Cyst nematodes are sedentary endoparasites that induce the formation of multinucleated feeding structures termed syncytia in the roots of host plants. Using promoter:GUS fusion assays we established that miR827 was activated in the initial feeding cells and this activation was maintained in the syncytium during all sedentary stages of nematode development. Meanwhile, the NLA target gene, which encodes an ubiquitin E3 ligase enzyme, was post-transcriptionally silenced in the syncytium to permanently suppress its activity during all nematode parasitic stages. Overexpression of miR827 in Arabidopsis resulted in hyper-susceptibility to H. schachtii. In contrast, inactivation of miR827 activity through target mimicry or by overexpression a miR827-resistant cDNA of NLA produced the opposite phenotype of reduced plant susceptibility to H. schachtii. Gene expression analysis of several pathogenesis-related genes together with Agrobacterium-mediated transient expression in Nicotiana benthamiana provided strong evidence that miR827-mediated downregulation of NLA to suppress basal defense pathways. In addition, using yeast two-hybrid screens we identified several candidates of NLA-interacting proteins that are involved in a wide range of biological processes and molecular functions, including three pathogenesis-related proteins. Taken together, we conclude that nematode-activated miR827 in the syncytium is necessary to suppress immune responses in order to establish infection and cause disease.

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MicroRNA400-Guided Cleavage of Pentatricopeptide Repeat Protein mRNAs Renders Arabidopsis thaliana More Susceptible to Pathogenic Bacteria and Fungi

Cited by 94 publications

References 53 publications

The Arabidopsis miR396 mediates pathogen-associated molecular pattern-triggered immune responses against fungal pathogens

The Arabidopsis miR396 mediates pathogen-associated molecular pattern-triggered immune responses against fungal pathogens

Genetic mapping and haplotype analysis of a locus for quantitative resistance to Fusarium graminearum in soybean accession PI 567516C

Arabidopsis miR827 mediates post‐transcriptional gene silencing of its ubiquitin E3 ligase target gene in the syncytium of the cyst nematode Heterodera schachtii to enhance susceptibility

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