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Abstract
The 24-nucleotides (nt) phased secondary small interfering RNA (phasiRNA) is a unique class of plant small RNAs abundantly expressed in monocot anthers at early meiosis. Previously, 44 intergenic regions were identified as the loci for longer precursor RNAs of 24-nt phasiRNAs (24-PHASs) in the rice genome. However, the regulatory mechanism that determines spatiotemporal expression of these RNAs has remained elusive. ETERNAL TAPETUM1 (EAT1) is a basic-helix-loop-helix (bHLH) transcription factor indispensable for induction of programmed cell death (PCD) in postmeiotic anther tapetum, the somatic nursery for pollen production. In this study, EAT1-dependent non-cell-autonomous regulation of male meiosis was evidenced from microscopic observation of the eat1 mutant, in which meiosis with aberrantly decondensed chromosomes was retarded but accomplished somehow, eventually resulting in abortive microspores due to an aberrant tapetal PCD. EAT1 protein accumulated in tapetal-cell nuclei at early meiosis and postmeiotic microspore stages. Meiotic EAT1 promoted transcription of 24-PHAS RNAs at 101 loci, and importantly, also activated DICER-LIKE5 (DCL5, previous DCL3b in rice) mRNA transcription that is required for processing of double-stranded 24-PHASs into 24-nt lengths. From the results of the chromatin-immunoprecipitation and transient expression analyses, another tapetum-expressing bHLH protein, TDR INTERACTING PROTEIN2 (TIP2), was suggested to be involved in meiotic small-RNA biogenesis. The transient assay also demonstrated that UNDEVELOPED TAPETUM1 (UDT1)/bHLH164 is a potential interacting partner of both EAT1 and TIP2 during early meiosis. This study indicates that EAT1 is one of key regulators triggering meiotic phasiRNA biogenesis in anther tapetum, and that other bHLH proteins, TIP2 and UDT1, also play some important roles in this process. Spatiotemporal expression control of these bHLH proteins is a clue to orchestrate precise meiosis progression and subsequent pollen production non-cell-autonomously.
Highlights
Small noncoding RNAs are 20–30 nucleotides long and associate with Argonaute family proteins to serve as guide molecules for RNA silencing in various biological processes, such as cell type specification, cell proliferation, cell death, metabolic control, transposon silencing and antiviral defense [1]
We found that MEL1 (ARGONAUTE5) promotes large-scale remodeling of meiotic chromosomes with dramatic increases of histone H3 lysine 9 dimethylation, and that loss of MEL1 resulted in early meiotic arrest with few crossovers present
Our findings suggest a possibility that unknown small RNA-mediated signaling regulates male meiosis non-cell-autonomously, probably a downstream output involves large-scale chromosome remodeling promoted by Argonaute proteins, while a possibility of ETERNAL TAPETUM1 (EAT1)-dependent, but small RNA-independent signaling cannot be excluded
Summary
Small noncoding RNAs are 20–30 nucleotides (nt) long and associate with Argonaute family proteins to serve as guide molecules for RNA silencing in various biological processes, such as cell type specification, cell proliferation, cell death, metabolic control, transposon silencing and antiviral defense [1]. Rice and maize, phasiRNAs are abundantly expressed in the male reproductive organs, and in this study, the term "phasiRNA" will be used for monocot reproductive phasiRNAs derived from protein-noncoding regions. Both tasiRNA and phasiRNA are produced via miRNA-dependent primary processing, and characterized by phased alignment on both sense and antisense strands in genomic regions. The roles of phasiRNAs during plant reproduction largely remain elusive
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