MicroRNAs and trans-acting siRNAs (ta-siRNAs) have important regulatory roles in development. Unlike other developmentally important regulatory molecules, small RNAs are not known to act as mobile signals during development. Here, we show that low-abundant, conserved ta-siRNAs, termed tasiR-ARFs, move intercellularly from their defined source of biogenesis on the upper (adaxial) side of leaves to the lower (abaxial) side to create a gradient of small RNAs that patterns the abaxial determinant AUXIN RESPONSE FACTOR3. Our observations have important ramifications for the function of small RNAs and suggest they can serve as mobile, instructive signals during development.Supplemental material is available at http://www.genesdev.org.Received December 7, 2008; revised version accepted January 21, 2009. Small RNAs, such as microRNAs (miRNAs), trans-acting siRNAs (ta-siRNAs), and endogenous siRNAs, regulate diverse developmental processes in multicellular organisms. The comprehensive role of these small RNAs in mediating development is best visualized by their complex and varied expression patterns (Juarez et al. 2004;Wienholds et al. 2005;Nogueira et al. 2007). However, the mechanisms underlying the origins of these discrete accumulation patterns remain largely obscure. Direct localization of miRNA primary transcripts suggests that this complexity arises in part from transcriptional control (Aboobaker et al. 2005;Nogueira et al. 2009). Additionally, the post-transcriptional processing of small RNA precursors is contingent upon the presence of necessary biogenesis factors, the restricted activity of which can contribute to the final spatiotemporal localization of mature small RNAs (Viswanathan et al. 2008). The intercellular movement of small RNAs could also feasibly contribute to their final localization patterns. However, even though the movement of siRNAs during systemic silencing is a well-documented phenomenon (Dunoyer et al. 2005;Voinnet 2005), no instances of intercellular movement of endogenous small RNAs have as of yet been reported (Parizotto et al. 2004;Alvarez et al. 2006). ta-siRNAs, a plant-specific small RNA class with roles in development, depend for their biogenesis on both miRNA activity and siRNA pathway components (Peragine et al. 2004;Vazquez et al. 2004;Allen et al. 2005). miRNAguided cleavage triggers entry of ta-siRNA precursor transcripts into RNA-DEPENDENT RNA POLYMER-ASE6 (RDR6)-dependent and SUPPRESSOR OF GENE SILENCING3 (SGS3)-dependent pathways and sets the register for phased, 21 nucleotide ta-siRNA production by DICER-LIKE4 ( Phenotypes resulting from mutations in TAS3 ta-siRNA biogenesis factors are mediated through the misregulation of tasiR-ARF targets, especially ARF3. Expression of ARF3 trangenes insensitive to tasiR-ARF regulation produce vegetative phase change defects similar to tasiR-ARF pathway mutations (Fahlgren et al. 2006;Hunter et al. 2006). The range of pleiotropic defects observed in such plants demonstrates the importance of this pathway to multiple aspects of leaf d...
Small RNAs are important regulators of gene expression. In maize, adaxial/abaxial (dorsoventral) leaf polarity is established by an abaxial gradient of microRNA166 (miR166), which spatially restricts the expression domain of class III homeodomain leucine zipper (HD-ZIPIII) transcription factors that specify adaxial/upper fate. Here, we show that leafbladeless1 encodes a key component in the trans-acting small interfering RNA (ta-siRNA) biogenesis pathway that acts on the adaxial side of developing leaves and demarcates the domains of hd-zipIII and miR166 accumulation. Our findings indicate that tasiR-ARF, a ta-siRNA, and miR166 establish opposing domains along the adaxial-abaxial axis, thus revealing a novel mechanism of pattern formation.Supplemental material is available at www.genesdev.org.Received January 8, 2007; revised version accepted February 20, 2007. In both animals and plants, many developmentally important regulatory genes are predicted targets of microRNAs (miRNAs), which suggests that such small RNAs constitute a class of developmental determinants (Alvarez-Garcia and Miska 2005;Jones-Rhoades et al. 2006). Patterning and outgrowth of lateral organs in plants depend on the specification of adaxial/abaxial (dorsoventral) polarity in the incipient primordium. This asymmetry is established through the polarized expression of class III homeodomain leucine zipper (HD-ZIPIII) transcription factors that specify adaxial/upper cell fate (McConnell et al. 2001;Emery et al. 2003;Juarez et al. 2004a). The adaxial-specific expression of hd-zipIII family members is delineated by the expression pattern of a 21-nucleotide (nt) miRNA, miR166, which directs the cleavage of hd-zipIII transcripts (Juarez et al. 2004a;Kidner and Martienssen 2004). In maize, miR166 accumulates most abundantly immediately below the incipient leaf, but a gradient of miR166 extends into the abaxial side of the initiating organ that establishes organ polarity (Juarez et al. 2004a).Specification of adaxial/abaxial organ polarity in maize also requires the activity of leafbladeless1 (lbl1). Recessive mutations in lbl1 lead to a variable abaxialization of leaves (Timmermans et al. 1998). The weak lbl1-ref allele causes a partial loss of adaxial identity revealed as patches of abaxial cells on the upper leaf surface, whereas leaves of the severe ragged seedling1 allele (lbl1-rgd1) are often radially symmetric and completely abaxialized (Fig. 1A). Expression of the hd-zipIII family member rld1 is reduced in lbl1 mutants. Conversely, increased levels of hd-zipIII expression in Rld1-O mutants, which carry a miR166-insensitive allele of rld1, can fully suppress the vegetative defects of lbl1 (Juarez et al. 2004b). lbl1 thus contributes to organ polarity by regulating the accumulation of rld1 transcripts on the adaxial side of the developing leaf.Here, we show that lbl1 encodes a homolog of SUPPRESSOR-OF-GENE-SILENCING3 (SGS3), which is specifically required for the biogenesis of trans-acting small interfering RNAs (ta-siRNAs) (Peragine et al. 2...
The manuscript by Alves et al. entitled "Genome-wide identification and characterization of tRNA-derived RNA fragments in land plants" describes the identification and characterization of tRNAderived sRNA fragments in plants. By combining bioinformatic analysis and genetic and molecular approaches, we show that tRF biogenesis does not rely on canonical microRNA/siRNA processing machinery (i.e., independent of DICER-LIKE proteins). Moreover, we provide evidences that the Arabidopsis S-like Ribonuclease 1 (RNS1) might be involved in the biogenesis of tRFs. Detailed analyses showed that plant tRFs are sorted into different types of ARGONAUTE proteins and that they have potential target candidate genes. Our work advances the understanding of the tRF biology in plants by providing evidences that plant and animal tRFs shared common features and raising the hypothesis that an interplay between tRFs and other sRNAs might be important to fine-tune gene expression and protein biosynthesis in plant cells. Small RNA (sRNA) fragments derived from tRNAs (3'-loop, 5'-loop, anti-codon loop), named tRFs, have been reported in several organisms, including humans and plants. Although they may interfere with gene expression, their biogenesis and biological functions in plants remain poorly understood. Here, we capitalized on small RNA sequencing data from distinct species such as Arabidopsis thaliana, Oryza sativa, and Physcomitrella patens to examine the diversity of plant tRFs and provide insight into their properties. In silico analyzes of 19 to 25-nt tRFs derived from 5' (tRF-5s) and 3'CCA (tRF-3s) tRNA loops in these three evolutionary distant species showed that they are conserved and their abundance did not correlate with the number of genomic copies of the parental tRNAs. Moreover, tRF-5 is the most abundant variant in all three species. In silico and in vivo expression analyses unraveled differential accumulation of tRFs in Arabidopsis tissues/organs, suggesting that they are not byproducts of tRNA degradation. We also verified that the biogenesis of most Arabidopsis 19-25 nt tRF-5s and tRF-3s is not primarily dependent on DICER-LIKE proteins, though they seem to be associated with ARGONAUTE proteins and have few potential targets. Finally, we provide evidence that Arabidopsis ribonuclease RNS1 might be involved in the processing and/or degradation of tRFs. Our data support the notion that an interplay between tRFs and other sRNAs might be important to fine tune gene expression and protein biosynthesis in plant cells.
SUMMARYFruit ripening in tomato (Solanum lycopersicum L.) is well understood at the molecular level. However, information regarding genetic pathways associated with tomato ovary and early fruit development is still lacking. Here, we investigate the possible role(s) of the microRNA156/SQUAMOSA promoter-binding protein-like (SPL or SBP box) module (miR156 node) in tomato ovary development. miR156-targeted S. lycopersicum SBP genes were dynamically expressed in developing flowers and ovaries, and miR156 was mainly expressed in meristematic tissues of the ovary, including placenta and ovules. Transgenic tomato cv. MicroTom plants over-expressing the AtMIR156b precursor exhibited abnormal flower and fruit morphology, with fruits characterized by growth of extra carpels and ectopic structures. Scanning electron microscopy and histological analyses showed the presence of meristem-like structures inside the ovaries, which are probably responsible for the ectopic organs. Interestingly, expression of genes associated with meristem maintenance and formation of new organs, such as LeT6/TKN2 (a KNOX-like class I gene) and GOBLET (a NAM/ CUC-like gene), was induced in developing ovaries of transgenic plants as well as in the ovaries of the natural mutant Mouse ear (Me), which also displays fruits with extra carpels. Conversely, expression of the MADS box genes MACROCALYX (MC) and FUL1/TDR4, and the LEAFY ortholog FALSIFLORA, was repressed in the developing ovaries of miR156 over-expressors, suggesting similarities with Arabidopsis at this point of the miR156/SPL pathway but with distinct functional consequences in reproductive development. Altogether, these observations suggest that the miR156 node is involved in maintenance of the meristematic state of ovary tissues, thereby controlling initial steps of fleshy fruit development and determinacy.
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