Pre-meiotic, 24-nt reproductive phasiRNAs are abundant in anthers of wheat and barley but not rice and maize

Bélanger, Sébastien; Pokhrel, Suresh; Czymmek, Kirk; Meyers, Blake C.

doi:10.1104/pp.20.00816

Cited by 22 publications

(28 citation statements)

References 56 publications

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“…We found that 21 nt reproductive phasiRNAs are present in several eudicots: wild strawberry, rose, the basal eudicot columbine, and flax. Whereas previous studies have shown that 21 nt reproductive phasiRNAs exist in one gymnosperm 8 and more widely in monocots 2 , 4 , 7 , 18 , 19 (Fig. 6a ), this pathway has not been described in several well-studied eudicot families including the Brassicaceae, Fabaceae, and Solanaceae 2 , 12 , 13 .…”

Section: Discussionmentioning

confidence: 66%

Pre-meiotic 21-nucleotide reproductive phasiRNAs emerged in seed plants and diversified in flowering plants

et al. 2021

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Plant small RNAs are important regulatory elements that fine-tune gene expression and maintain genome integrity by silencing transposons. Reproductive organs of monocots produce abundant phased, small interfering RNAs (phasiRNAs). The 21-nt reproductive phasiRNAs triggered by miR2118 are highly enriched in pre-meiotic anthers, and have been found in multiple eudicot species, in contrast with prior reports of monocot specificity. The 24-nt reproductive phasiRNAs are triggered by miR2275, and are highly enriched during meiosis in many angiosperms. Here, we report the widespread presence of the 21-nt reproductive phasiRNA pathway in eudicots including canonical and non-canonical microRNA (miRNA) triggers of this pathway. In eudicots, these 21-nt phasiRNAs are enriched in pre-meiotic stages, a spatiotemporal distribution consistent with that of monocots and suggesting a role in anther development. Although this pathway is apparently absent in well-studied eudicot families including the Brassicaceae, Solanaceae and Fabaceae, our work in eudicots supports an earlier singular finding in spruce, a gymnosperm, indicating that the pathway of 21-nt reproductive phasiRNAs emerged in seed plants and was lost in some lineages.

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Section: Discussionmentioning

confidence: 66%

Pre-meiotic 21-nucleotide reproductive phasiRNAs emerged in seed plants and diversified in flowering plants

et al. 2021

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“…Genomes of grass species are particularly rich in reproductive PHAS loci ( Patel et al, 2021 ), expressed in anthers but not in female reproductive tissues or vegetative tissues. Previous species studies identified hundreds of PHAS loci in anthers of maize ( Zhai et al, 2015 ) to thousands of PHAS loci in rice ( Fei et al, 2016 ), barley ( Bélanger et al, 2020 ), and bread wheat ( Bélanger et al, 2020 ; Zhang et al, 2020 ). Additionally, work in maize ( Teng et al, 2020 ) and rice ( Fan et al, 2016 ) showed that 21-nt and 24-nt phasiRNAs are essential to ensure proper development of meiocytes and to guarantee male fertility under normal growth conditions.…”

Section: Discussionmentioning

confidence: 99%

The Streptochaeta Genome and the Evolution of the Grasses

Seetharam

Bélanger

et al. 2021

Front. Plant Sci.

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In this work, we sequenced and annotated the genome of Streptochaeta angustifolia, one of two genera in the grass subfamily Anomochlooideae, a lineage sister to all other grasses. The final assembly size is over 99% of the estimated genome size. We find good collinearity with the rice genome and have captured most of the gene space. Streptochaeta is similar to other grasses in the structure of its fruit (a caryopsis or grain) but has peculiar flowers and inflorescences that are distinct from those in the outgroups and in other grasses. To provide tools for investigations of floral structure, we analyzed two large families of transcription factors, AP2-like and R2R3 MYBs, that are known to control floral and spikelet development in rice and maize among other grasses. Many of these are also regulated by small RNAs. Structure of the gene trees showed that the well documented whole genome duplication at the origin of the grasses (ρ) occurred before the divergence of the Anomochlooideae lineage from the lineage leading to the rest of the grasses (the spikelet clade) and thus that the common ancestor of all grasses probably had two copies of the developmental genes. However, Streptochaeta (and by inference other members of Anomochlooideae) has lost one copy of many genes. The peculiar floral morphology of Streptochaeta may thus have derived from an ancestral plant that was morphologically similar to the spikelet-bearing grasses. We further identify 114 loci producing microRNAs and 89 loci generating phased, secondary siRNAs, classes of small RNAs known to be influential in transcriptional and post-transcriptional regulation of several plant functions.

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“…Exploring the abundance of identified AGO proteins, we found that seven changed significantly during anther development: HvAGO18, HvAGO1b, HvAGO1d, HvAGO2, HvAGO4a, HvAGO5b/MEL1, and HvAGO6. Functions of all seven AGO DAPs in male reproductive organ development and/or meiosis progression are well documented ( Bélanger et al , 2020 ; Zhang et al , 2020 ; Lian et al , 2021 ).…”

Section: Discussionmentioning

confidence: 99%

“…For example, translational control of existing mRNAs may have a key role, as shown in yeast where the elongation rate can dynamically regulate selective translation of stage-specific meiotic transcripts ( Sabi and Tuller, 2019 ). Furthermore, recent studies indicate that anther-specific small RNAs, including miRNAs and phased small-interfering RNAs (phasiRNAs), regulate gene expression during male meiosis ( Dukovic-Schulze et al, 2016 ; Bélanger et al , 2020 ), and specific classes of phasiRNAs are enriched at different stages of meiosis in maize ( Zhai et al , 2015 ), rice ( Komiya et al , 2014 ; Fei et al , 2016 ), wheat, and barley ( Bélanger et al , 2020 ).…”

Section: Introductionmentioning

confidence: 99%

The proteome of developing barley anthers during meiotic prophase I

Lewandowska

Orr

Schreiber

et al. 2021

Journal of Experimental Botany

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Flowering plants reproduce sexually by combining a haploid male and female gametophyte during fertilization. Male gametophytes are localized in the anthers, each containing reproductive (meiocyte) and non-reproductive tissue necessary for anther development and maturation. Meiosis, where chromosomes pair and exchange their genetic material during a process called recombination, is one of the most important and sensitive stages in breeding, ensuring genetic diversity. Most anther development studies have focussed on transcript variation, but very few have been correlated with protein abundance. Taking advantage of a recently published barley anther transcriptomic dataset (BAnTr) and a newly developed sensitive mass spectrometry-based approach to analyse barley anther proteome, we conducted high-resolution mass spectrometry analysis of barley anthers, collected at 6 time points and representing their development from pre-meiosis to metaphase. Each time point was carefully staged using immunocytology, providing a robust and accurate staging mirroring our previous transcriptomic dataset (BAnTr). We identified more than 6,100 non-redundant proteins including 82 known and putative meiotic proteins. Although the protein abundance was relatively stable throughout prophase I, we were able to quantify the dynamic variation of 336 proteins. We present the first quantitative comparative proteomics study of barley anther development during meiotic prophase I when the important process of homologous recombination is taking place.

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Pre-meiotic, 24-nt reproductive phasiRNAs are abundant in anthers of wheat and barley but not rice and maize

Cited by 22 publications

References 56 publications

Pre-meiotic 21-nucleotide reproductive phasiRNAs emerged in seed plants and diversified in flowering plants

Pre-meiotic 21-nucleotide reproductive phasiRNAs emerged in seed plants and diversified in flowering plants

The Streptochaeta Genome and the Evolution of the Grasses

The proteome of developing barley anthers during meiotic prophase I

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