Small RNAs regulate plant responses to filamentous pathogens

Kuan, Tung; Zhai, Yi; Ma, Wenbo

doi:10.1016/j.semcdb.2016.05.013

Cited by 16 publications

(11 citation statements)

References 79 publications

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“…In most cases sRNAs function within the organism to regulate gene expression in an endogenous fashion. In plants, defense genes related to both PTI and ETI responses are regulated by micro RNAs (miRNAs) [11, 12]. Several miRNA families are involved in regulating plant responses to pathogen infection [13, 14].…”

Section: Introductionmentioning

confidence: 99%

“…The targets of these miRNAs are involved in both PTI and ETI responses. The PTI-related pathways regulated through miRNAs include hormone signaling, reactive oxygen species evolution, callose deposition, and others [11]. Auxin signaling is carefully controlled during plant development and can be down regulated during pathogen infection such as with miR393 that downregulates auxin F-box receptors during a PTI response to infection [15].…”

Section: Introductionmentioning

confidence: 99%

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Small RNA discovery in the interaction between barley and the powdery mildew pathogen

et al. 2019

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Background Plants encounter pathogenic and non-pathogenic microorganisms on a nearly constant basis. Small RNAs such as siRNAs and miRNAs/milRNAs influence pathogen virulence and host defense responses. We exploited the biotrophic interaction between the powdery mildew fungus, Blumeria graminis f. sp. hordei ( Bgh ), and its diploid host plant, barley ( Hordeum vulgare ) to explore fungal and plant sRNAs expressed during Bgh infection of barley leaf epidermal cells. Results RNA was isolated from four fast-neutron immune-signaling mutants and their progenitor over a time course representing key stages of Bgh infection, including appressorium formation, penetration of epidermal cells, and development of haustorial feeding structures. The Cereal Introduction (CI) 16151 progenitor carries the resistance allele Mla6 , while Bgh isolate 5874 harbors the AVR a6 avirulence effector, resulting in an incompatible interaction. Parallel Analysis of RNA Ends (PARE) was used to verify sRNAs with likely transcript targets in both barley and Bgh. Bgh sRNAs are predicted to regulate effectors, metabolic genes, and translation-related genes. Barley sRNAs are predicted to influence the accumulation of transcripts that encode auxin response factors, NAC transcription factors, homeodomain transcription factors, and several splicing factors. We also identified phasing small interfering RNAs (phasiRNAs) in barley that overlap transcripts that encode receptor-like kinases (RLKs) and nucleotide-binding, leucine-rich domain proteins (NLRs). Conclusions These data suggest that Bgh sRNAs regulate gene expression in metabolism, translation-related, and pathogen effectors. PARE-validated targets of predicted Bgh milRNAs include both EKA (effectors homologous to AVR k1 and AVR a10 ) and CSEP (candidate secreted effector protein) families. We also identified barley phasiRNAs and miRNAs in response to Bgh infection. These include phasiRNA loci that overlap with a significant proportion of receptor-like kinases, suggesting an additional sRNA control mechanism may be active in barley leaves as opposed to predominant R -gene phasiRNA overlap in many eudicots. In addition, we identified conserved miRNAs, novel miRNA candidates, and barley genome mapped sRNAs that have PARE validated transcript targets in barley. The miRNA target transcripts are enriched in transcription factors, signaling-related proteins, and photosynthesis-related proteins. Together these results suggest both barley and ...

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Small RNA discovery in the interaction between barley and the powdery mildew pathogen

et al. 2019

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“…Based on their biogenesis, small RNAs can be broadly classified into two major groups: microRNAs (miRNAs) and small interfering RNAs (siRNAs). MicroRNAs are 21-24 nt sequences encoded by plant microRNA genes (MIR) genes, which operate via posttranscriptional mRNA cleavage or translational inhibition (Kuan et al, 2016). In plants, miRNAs are processed from imperfectly complementary hairpin structures by the Dicer-like 1 (DCL1) endoribonuclease, which are then loaded into an RNA-induced silencing complex (RISC) to regulate expression of corresponding target genes.…”

Section: Introductionmentioning

confidence: 99%

Analysis of miRNAs in Two Wheat Cultivars Infected With Puccinia striiformis f. sp. tritici

et al. 2020

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MicroRNAs are small RNAs that regulate gene expression in eukaryotes. In this study, we analyzed the small RNA profiles of two cultivars that exhibit different reactions to stripe rust infection: one susceptible, the other partially resistant. Using small RNA libraries prepared from the two wheat cultivars infected with stripe rust fungus (Puccinia striiformis f. sp. tritici), we identified 182 previously known miRNAs, 91 variants of known miRNAs, and 163 candidate novel wheat miRNAs. Known miRNA loci were usually copied in all three wheat sub-genomes, whereas novel miRNA loci were often specific to a single subgenome. DESeq2 analysis of differentially expressed microRNAs revealed 23 miRNAs that exhibit cultivar-specific differences. TA078/miR399b showed cultivar-specific differential regulation in response to infection. Using different target prediction algorithms, 145 miRNAs were predicted to target wheat genes, while 69 miRNAs were predicted to target fungal genes. We also confirmed reciprocal expression of TA078/miR399b and tae-miR9664 and their target genes in different treatments, providing evidence for miRNAmediated regulation during infection. Both known and novel miRNAs were predicted to target fungal genes, suggesting trans-kingdom regulation of gene expression. Overall, this study contributes to the current repository of wheat miRNAs and provides novel information on the yet-uncharacterized roles for miRNAs in the wheat-stripe rust pathosystem.

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“…Alterations in the accumulation of a substantial fraction of the miRNAome during pathogen infection is also described in different pathosystems, and for some miRNAs a role in plant immunity has been described ( Shivaprasad et al, 2012 ; Campo et al, 2013 ; Boccara et al, 2014 ; Li et al, 2014 ; Baldrich and San Segundo, 2016 ; Soto-Suárez et al, 2017 ). However, our current knowledge of the biological roles of pathogen-regulated miRNAs in plant immunity is still limited, and most comes from studies in the interaction of Arabidopsis thaliana with the bacterial pathogen Pseudomonas syringae ( Staiger et al, 2013 ; Weiberg et al, 2014 ; Fei et al, 2016 ; Kuan et al, 2016 ).…”

Section: Introductionmentioning

confidence: 99%

The Polycistronic miR166k-166h Positively Regulates Rice Immunity via Post-transcriptional Control of EIN2

2018

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MicroRNAs (miRNAs) are small RNAs acting as regulators of gene expression at the post-transcriptional level. In plants, most miRNAs are generated from independent transcriptional units, and only a few polycistronic miRNAs have been described. miR166 is a conserved miRNA in plants targeting the HD-ZIP III transcription factor genes. Here, we show that a polycistronic miRNA comprising two miR166 family members, miR166k and miR166h, functions as a positive regulator of rice immunity. Rice plants with activated MIR166k-166h expression showed enhanced resistance to infection by the fungal pathogens Magnaporthe oryzae and Fusarium fujikuroi, the causal agents of the rice blast and bakanae disease, respectively. Disease resistance in rice plants with activated MIR166k-166h expression was associated with a stronger expression of defense responses during pathogen infection. Stronger induction of MIR166k-166h expression occurred in resistant but not susceptible rice cultivars. Notably, the ethylene-insensitive 2 (EIN2) gene was identified as a novel target gene for miR166k. The regulatory role of the miR166h-166k polycistron on the newly identified target gene results from the activity of the miR166k-5p specie generated from the miR166k-166h precursor. Collectively, our findings support a role for miR166k-5p in rice immunity by controlling EIN2 expression. Because rice blast is one of the most destructive diseases of cultivated rice worldwide, unraveling miR166k-166h-mediated mechanisms underlying blast resistance could ultimately help in designing appropriate strategies for rice protection.

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Small RNAs regulate plant responses to filamentous pathogens

Cited by 16 publications

References 79 publications

Small RNA discovery in the interaction between barley and the powdery mildew pathogen

Small RNA discovery in the interaction between barley and the powdery mildew pathogen

Analysis of miRNAs in Two Wheat Cultivars Infected With Puccinia striiformis f. sp. tritici

The Polycistronic miR166k-166h Positively Regulates Rice Immunity via Post-transcriptional Control of EIN2

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