BHLH cascade regulate 24-nt phasiRNA biogenesis in maize anther
Ontology highlight
ABSTRACT:
PROVIDER: PRJNA734322 | ENA |
REPOSITORIES: ENA
Dataset's files
| Action | DRS | |||
|---|---|---|---|---|
| SRR14703000.fastq.gz | Fastqsanger.gz | |||
| SRR14703001.fastq.gz | Fastqsanger.gz | |||
| SRR14703002.fastq.gz | Fastqsanger.gz | |||
| SRR14703003.fastq.gz | Fastqsanger.gz | |||
| SRR14703004.fastq.gz | Fastqsanger.gz |
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Project description:Anthers are the male reproductive floral organs, but loss of the 24-nt class of phased small-interfering RNAs (phasiRNAs) may confer temperature-sensitive male sterility in maize. 24-nt phasiRNAs from 176 loci are abundant coordinately in fertile maize anthers after the last periclinal divisions are complete, all four wall layers are formed, and meiosis has initiated in the pollen mother cells. In this study, we found male sterile maize ms23, ms32, and bhlh122 mutants with various degrees of tapetal defects lack 24-PHAS mRNA precursors and 24-nt phasiRNAs, which were not affected in another male sterile mutant, bhlh51. Transcription from most of 24-PHAS loci depends on bHLH122 while bHLH122 and Dcl5 transcription depends on both Ms23 and Ms32. Multiple lines of evidence suggest that 24-nt phasiRNAs biogenesis is primarily controlled at multiple layers by MS23 and MS32, with distinctive action on 24-PHAS transcription by bHLH122, creating a transcription factor cascade in maize tapetal cells.
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Project description:PhasiRNAs (phased small interfering RNAs) are a major class of plant small RNAs known to be key regulators in male reproductive development of maize and rice (Oryza sativa), among other plants. Earlier research focused primarily on premeiotic 21-nt phasiRNAs and meiotic 24-nt phasiRNAs, while new studies uncovered a premeiotic class of 24-nt phasiRNAs. The biogenesis and function of these phasiRNAs remains unclear. We conducted an integrative analysis combining small RNA sequencing and transcriptomic profiling of small RNA-associated genes across Kitaake rice anther developmental stages to map associations between sRNA-related genes and phasiRNA classes. We identified new classes of postmeiotic 21-nucleotide and postmeiotic 24-nucleotide phasiRNA-producing loci and characterized their unique accumulation patterns. Our findings reveal distinct differences in nucleotide composition and register accumulation among the phasiRNA classes, suggesting the presence of diverse mechanisms of biogenesis and function. Our results provide new insights into the regulatory complexity of phasiRNAs, establishing a foundation for further functional studies and advancing our understanding of their roles in anther development and their underlying mechanisms.
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Project description:Phased secondary siRNAs (phasiRNAs) are broadly present in the reproductive tissues of flowering plants. Monocots generate 21- and 24-nt phasiRNAs by miR2118 and miR2275 respectively from noncoding RNAs with spatial-temporal specificity during anther development. However, which ARGONAUTES (AGOs) associate with these two miRNAs remains elusive. Here we show that rice AGO1d, specifically expressed in anther wall cells before and during meiosis, associates with both miR2118 and miR2275 to mediate phasiRNA biogenesis. Furthermore, AGO1d also binds to miR2118-triggered 21-nt phasiRNAs preferentially with a 5’-terminal uridine, suggesting a dual role in phasiRNA biogenesis and function. Depletion of AGO1d causes reduction of 21- and 24-nt phasiRNAs and temperature-sensitive sterility. Anthers of the ago1d mutants at lower temperatures mainly display defects in tapetal cells and vacuolation during pollen formation. These results uncover an essential role of AGO1d in rice anther development at lower temperatures and demonstrate coordinative roles of AGO proteins during reproductive phasiRNA biogenesis and function
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Project description:In maize, 24-nt phased, secondary small interfering RNAs (phasiRNAs) are abundant in meiotic stage anthers, but their distribution and functions are not precisely known. Using laser capture microdissection (LCM), we analyzed tapetal cells, meiocytes, and other somatic cells at several stages of anther development to establish the timing of 24-PHAS precursor transcripts and the 24-nt phasiRNA products. This dataset includes 24-nt phasiRNA part of data. 24-nt phasiRNAs are found to accumulate in all cell types, with the highest levels in meiocytes, followed by tapetum.
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Project description:In maize, 24-nt phased, secondary small interfering RNAs (phasiRNAs) are abundant in meiotic stage anthers, but their distribution and functions are not precisely known. Using laser capture microdissection we analyzed tapetal cells, meiocytes, and other somatic cells at several stages of anther development to establish the timing of 24-PHAS precursor transcripts and the 24-nt phasiRNA products. By integrating RNA and small RNA (sRNA) profiling plus single-molecule and sRNA FISH (smFISH or sRNA-FISH) spatial detection, we demonstrate that the tapetum is the primary site of 24-PHAS precursor and Dcl5 transcripts and the resulting 24-nt phasiRNAs. Interestingly, 24-nt phasiRNAs accumulate in all cell types, with the highest levels in meiocytes, followed by tapetum. Our data support the conclusion that 24-nt phasiRNAs are mobile from tapetum to meiocytes and to other somatic cells. We discuss possible roles for 24-nt phasiRNAs in anther cell types.
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Project description:In grasses, 21- and 24-nt phasiRNAs are abundantly expressed in anthers and play crucial roles in anther development and male reproduction. 21-nt phasiRNAs can act in cis to direct the cleavage of their own precursor transcripts and is thought to lack trans cleavage targets in maize. Here we show that 21-nt phasiRNAs direct the cleavage of hundreds of target mRNAs in maize, with the cleavage activity being enriched in male germ cells. Interestingly, whereas 21-nt phasiRNAs in anthers (somatic anther wall cells) do not have obvious preference for a particular nucleotide at the 5’ end and target genes implicated in stress response and cellular homeostasis, 21-nt phasiRNAs in male germ cells preferentially initiate with 5’ C and associate with ZmAGO5c/MAGO2/MS28 to target genes related to meiotic processes. Our results indicate that mRNA cleavage is a conserved mechanism used by 21-nt phasiRNAs for gene regulation. However, the sequences of 21-nt phasiRNAs and their targets show low conservation in maize and rice, suggesting that 21PHAS loci and 21-nt phasiRNA targets have undergone fast divergence in monocots.
2025-05-26 | GSE279861 | GEO
Project description:In grasses, 21- and 24-nt phasiRNAs are abundantly expressed in anthers and play crucial roles in anther development and male reproduction. 21-nt phasiRNAs can act in cis to direct the cleavage of their own precursor transcripts and is thought to lack trans cleavage targets in maize. Here we show that 21-nt phasiRNAs direct the cleavage of hundreds of target mRNAs in maize, with the cleavage activity being enriched in male germ cells. Interestingly, whereas 21-nt phasiRNAs in anthers (somatic anther wall cells) do not have obvious preference for a particular nucleotide at the 5’ end and target genes implicated in stress response and cellular homeostasis, 21-nt phasiRNAs in male germ cells preferentially initiate with 5’ C and associate with ZmAGO5c/MAGO2/MS28 to target genes related to meiotic processes. Our results indicate that mRNA cleavage is a conserved mechanism used by 21-nt phasiRNAs for gene regulation. However, the sequences of 21-nt phasiRNAs and their targets show low conservation in maize and rice, suggesting that 21PHAS loci and 21-nt phasiRNA targets have undergone fast divergence in monocots.
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Project description:In grasses, 21- and 24-nt phasiRNAs are abundantly expressed in anthers and play crucial roles in anther development and male reproduction. 21-nt phasiRNAs can act in cis to direct the cleavage of their own precursor transcripts and is thought to lack trans cleavage targets in maize. Here we show that 21-nt phasiRNAs direct the cleavage of hundreds of target mRNAs in maize, with the cleavage activity being enriched in male germ cells. Interestingly, whereas 21-nt phasiRNAs in anthers (somatic anther wall cells) do not have obvious preference for a particular nucleotide at the 5’ end and target genes implicated in stress response and cellular homeostasis, 21-nt phasiRNAs in male germ cells preferentially initiate with 5’ C and associate with ZmAGO5c/MAGO2/MS28 to target genes related to meiotic processes. Our results indicate that mRNA cleavage is a conserved mechanism used by 21-nt phasiRNAs for gene regulation. However, the sequences of 21-nt phasiRNAs and their targets show low conservation in maize and rice, suggesting that 21PHAS loci and 21-nt phasiRNA targets have undergone fast divergence in monocots.
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Project description:Maize anthers, the male reproductive floral organs, express two classes of phased, small interfering RNAs (phasiRNAs). RNA profiling from ten sequential cohorts of staged maize anthers plus mature pollen revealed that 21-nt phased siRNAs (21-phasiRNAs) from 463 loci appear abruptly after germinal and initial somatic cell fate specification and then diminish, while 24-nt phased siRNAs (24-phasiRNAs) from 176 loci coordinately accumulate during meiosis and persist as haploid gametophytes differentiate into pollen. RNA sequencing of anther developmental mutants, together with in situ RNA hybridization detection of phasiRNA biogenesis factors, demonstrated that 21-phasiRNAs and 24-phasiRNAs are independently regulated. Furthermore, 21-phasiRNAs require epidermal cells while 24-phasiRNAs require functional tapetal cells. Maize phasiRNAs and mammalian PIWI-interacting RNAs (piRNAs) illustrate convergent evolution of small RNAs to support male reproduction.
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Project description:Maize anthers, the male reproductive floral organs, express two classes of phased, small interfering RNAs (phasiRNAs). RNA profiling from ten sequential cohorts of staged maize anthers plus mature pollen revealed that 21-nt phased siRNAs (21-phasiRNAs) from 463 loci appear abruptly after germinal and initial somatic cell fate specification and then diminish, while 24-nt phased siRNAs (24-phasiRNAs) from 176 loci coordinately accumulate during meiosis and persist as haploid gametophytes differentiate into pollen. RNA sequencing of anther developmental mutants, together with in situ RNA hybridization detection of phasiRNA biogenesis factors, demonstrated that 21-phasiRNAs and 24-phasiRNAs are independently regulated. Furthermore, 21-phasiRNAs require epidermal cells while 24-phasiRNAs require functional tapetal cells. Maize phasiRNAs and mammalian PIWI-interacting RNAs (piRNAs) illustrate convergent evolution of small RNAs to support male reproduction.
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