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Review
.2013 Jan 14;14(1):1516-40.
doi: 10.3390/ijms14011516.

Role of RNA interference (RNAi) in the Moss Physcomitrella patens

Affiliations
Review

Role of RNA interference (RNAi) in the Moss Physcomitrella patens

Muhammad Asif Arif et al. Int J Mol Sci..

Abstract

RNA interference (RNAi) is a mechanism that regulates genes by either transcriptional (TGS) or posttranscriptional gene silencing (PTGS), required for genome maintenance and proper development of an organism. Small non-coding RNAs are the key players in RNAi and have been intensively studied in eukaryotes. In plants, several classes of small RNAs with specific sizes and dedicated functions have evolved. The major classes of small RNAs include microRNAs (miRNAs) and small interfering RNAs (siRNAs), which differ in their biogenesis. miRNAs are synthesized from a short hairpin structure while siRNAs are derived from long double-stranded RNAs (dsRNA). Both miRNA and siRNAs control the expression of cognate target RNAs by binding to reverse complementary sequences mediating cleavage or translational inhibition of the target RNA. They also act on the DNA and cause epigenetic changes such as DNA methylation and histone modifications. In the last years, the analysis of plant RNAi pathways was extended to the bryophyte Physcomitrella patens, a non-flowering, non-vascular ancient land plant that diverged from the lineage of seed plants approximately 450 million years ago. Based on a number of characteristic features and its phylogenetic key position in land plant evolution P. patens emerged as a plant model species to address basic as well as applied topics in plant biology. Here we summarize the current knowledge on the role of RNAi in P. patens that shows functional overlap with RNAi pathways from seed plants, and also unique features specific to this species.

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Figures

Figure 1
Figure 1
Different endogenous small interfering RNA (siRNA) pathways ofP. patens. Only PpDCLs and PpRDR6 have been functionally characterized inP. patens; evidence for proteins shown in figure comes fromArabidopsis and their homologous exist inP. patens. (A)P. patens miRNA pathway.MIR genes are transcribed by RNA polymerase II into pri-miRNA transcripts that are further processed into pre-miRNAs harboring a characteristic hairpin structure. From the stem of the pre-miRNA the miRNA/miRNA* duplex is excised by PpDCL1a and can be assisted by HYL and SE proteins. These are then methylated by HUA ENHANCER 1 (HEN1) and transported to the cytoplasm by HASTY (HST). The miRNA guide strand is selected, incorporated, and stabilized in dedicated AGO1 protein. miRNA-guided AGO1-containing RNA-induced silencing complex (RISC) directs mRNA cleavage or translation inhibition of the target transcript. Highly abundant miRNAs are either loaded into a RITS complex and subsequently interact with their target to form a duplex, or these duplexes are formed at first and then loaded into RITS. The miRNA:RNA duplexes bound by RNAi-induced transcriptional silencing complex (RITS) initiate DNA methylation at complementary genomic loci. (B)P. patens ta-siRNA pathway.TAS genes are transcribed by RNA polymerase II intoTAS precursors harbouring miR390, miR156 and miR529 binding sites. AfterTAS precursor cleavage at these miRNA sites the middle cleavage product is converted into double-stranded RNAs (dsRNA) by PpRDR6 and subsequently processed into phased ta-siRNAs by PpDCL4. ta-siRNAs are loaded into RISC where they act like miRNAs. (C)P. patens siRNA pathway from repetitive genomic regions primarily LTR-retrotransposons and helitron DNA transposons. dsRNA processed into siRNAs by PpDCL3 and HEN1-mediated siRNA stabilization, the PpDCL3-dependent 22–24 nt siRNAs caused a de-repression of LTR retrotransposon-associated reverse transcriptases pointing to an epigenetic control of these elements. (D) Secondary siRNAs inP. patens. dsRNA is synthesised from cleaved miRNA or ta-siRNA targets by RdRP and processed into secondary siRNAs that mediate cleavage of the target RNA upstream and downstream of the miRNA/ta-siRNA recognition motif resulting in an amplification of the initial small RNA trigger.
Figure 2
Figure 2
Venn diagram comparing miRNA families from the seed plantsA. thaliana (dicot) andO. sativa (monocot), the mossP. patens and the unicellular algaC. reinhardtii based on miRBase database (Release 19.0,http://www.mirbase.org/).C. reinhardtii miRNA families are species-specific since they do not show sequence similarity to miRNA families from land plants. 11 miRNA families (miR156, miR160, miR166, miR167, miR171, miR319, miR390, miR395, miR408, miR414 and miR419) are conserved betweenA. thaliana,O. sativa, andP. patens. Two additional miRNA families, (miR529 and miR535) are conserved betweenO. sativa andP. patens.
Figure 3
Figure 3
P. patens DCL mutant phenotypes. (A) Phenotypic comparison ofP. patens wild type and a ΔPpDCL1a mutant line: in mutants cell size and shape is affected, they have retarded growth, and developmental arrest at the filamentous protonema stage is obserbed. (B) Phenotypic comparison ofP. patens wild type and a ΔPpDCL1b mutant line: mutants show deviating cell division, cell size, cell shape and growth polarity, and they developed only a small number of gametophores which in addition are malformed (C) Phenotypic comparison ofP. patens wild type and a ΔPpDCL3 mutant line: mutants show accelerated gametophore development. (D) Phenotypic comparison ofP. patens wild type and ΔPpDCL4 mutant lines under standard growth conditions: mutants show several brachycytes in the protonema, colony produces relative more protonema and less leafy gametophores, gametophores are stunted in growth, and mutants are sterile (E) Phenotypic comparison ofP. patens wild type and ΔPpDCL4 mutant lines under short day conditions: mutants generates malformed gametophores, and fail to produce caulonema under dark conditions.
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