The disease resistance protein SNC1 represses the biogenesis of microRNAs and phased siRNAs

Abstract

Plants evolved an array of disease resistance genes (R genes) to fight pathogens. In the absence of pathogen infection, NBS-LRR genes, which comprise a major subfamily of R genes, are suppressed by a small RNA cascade involving microRNAs (miRNAs) that trigger the biogenesis of phased siRNAs (phasiRNAs) from R gene transcripts. However, whether or how R genes influence small RNA biogenesis is unknown. In this study, we isolate a mutant with global defects in the biogenesis of miRNAs and phasiRNAs in Arabidopsis thaliana and trace the defects to the over accumulation and nuclear localization of an R protein SNC1. We show that nuclear SNC1 represses the transcription of miRNA and phasiRNA loci, probably through the transcriptional corepressor TPR1. Intriguingly, nuclear SNC1 reduces the accumulation of phasiRNAs from three source R genes and concomitantly, the expression of a majority of the ~170R genes is up-regulated. Taken together, this study suggests an R gene-miRNA-phasiRNA regulatory module that amplifies plant immune responses.

Plant evolution and environmental adaptation unveiled by long-read whole-genome sequencing ofSpirodela

“…Different from land plants, where expression of disease resistance genes is inducible by exposure to pathogens, aquatic plants are in constant contact with a diverse population of microorganisms. This adaptation is also consistent with the low level of the 24-nt siRNAs, possibly due to reduced expression of DCL3 and PolIV in Spirodela fronds (Table 2), which are known to guide DNA methylation and be involved in the silencing of repeat sequences like retrotransposons and tandemly repeated disease-resistant genes in angiosperms (39,40). Because of the neotenous growth of Spirodela, there is less of a need to guard against retrotransposition during meiosis than in land plants, but, as we can see here, also for the repression of its immune system.…”

Plant microRNAs: Biogenesis, Homeostasis, and Degradation

“…The transcription co-activator complex mediator plays a general role in recruiting Pol II to MIR promoters during transcription initiation (Kim et al, 2011). MIR transcription is not only regulated by locus-specific transcription factors and regulators, but is also globally modulated by the CCR4-NOT (for Carbon Catabolite Repression 4-Negative on TATA-less) complex subunit NOT2, the Elongator complex subunits ELP2 and ELP5, the MYB-R2R3 type transcription factor Cell Division Cycle 5 (CDC5), the DOF (for DNA binding with One Finger) transcription factor Cycling DOF Factor 2 (CDF2), the Protein Phosphatase 4 complex, the disease resistance R protein SNC1 (for Suppressor of npr1-1 , Constitutive 1) and its transcriptional corepressor Topless-Related 1 (TPR1) (Wang et al, 2013, 2019; Zhang et al, 2013; Fang et al, 2015a; Sun et al, 2015; Cai et al, 2018). A general effect of these proteins on MIR transcription may be related to their interactions with members of the miRNA processing machinery such as DCL1.…”

Sugar Signaling and Post-transcriptional Regulation in Plants: An Overlooked or an Emerging Topic?

“…Interestingly, the relationship between miRNA biosynthesis and the cellular energy status is also supported by the fact that the transient overexpression of the energy-sensing SnRK1 in protoplasts leads to the repression of a variety of miRNAs ( Confraria et al, 2013 ). These include miRNA159B (involved in leaf senescence, Huo et al, 2015 ), miRNA161 (induces the expression of PPR genes, Cai et al, 2018 ), miRNA775A (no function reported to date), and miRNA824A (involved in flowering time regulation, Hu et al, 2014 ) and might be involved in SnRK1-dependent energy signaling. However, the molecular regulatory network involved in this SnRK1-dependent miRNA biosynthesis remains an open question.…”