Comparative RNA profiling identifies stage-specific phasiRNAs and coexpressed Argonaute genes in Bambusoideae and Pooideae species

Sébastien Bélanger; Junpeng Zhan; Yunqing Yu; Blake C. Meyers

doi:10.1093/plcell/koae308

Comparative RNA profiling identifies stage-specific phasiRNAs and coexpressed Argonaute genes in Bambusoideae and Pooideae species

Sébastien Bélanger (Lead / Corresponding author)
, Junpeng Zhan
, Yunqing Yu
, Blake C. Meyers (Lead / Corresponding author)

DArcy Thompson Unit

Research output: Contribution to journal › Article › peer-review

2 Citations (Scopus)

Abstract

Phased, small interfering RNAs (PhasiRNAs) play a crucial role in supporting male fertility in grasses. Earlier work in maize (Zea mays) and rice (Oryza sativa) - and subsequently many other plant species - identified premeiotic 21-nucleotide (nt) and meiotic 24-nt phasiRNAs. More recently, a group of premeiotic 24-nt phasiRNAs was discovered in the anthers of 2 Pooideae species, barley (Hordeum vulgare) and bread wheat (Triticum aestivum). Whether premeiotic 24-nt phasiRNAs and other classes of reproductive phasiRNAs are conserved across Pooideae species remains unclear. We conducted comparative RNA profiling of 3 anther stages in 6 Pooideae species and 1 Bambusoideae species. We observed complex temporal accumulation patterns of 21-nt and 24-nt phasiRNAs in Pooideae and Bambusoideae grasses. In Bambusoideae, 21-nt phasiRNAs accumulated during meiosis, whereas 24-nt phasiRNAs were present in both premeiotic and postmeiotic stages. We identified premeiotic 24-nt phasiRNAs in all 7 species examined. These phasiRNAs exhibit distinct biogenesis mechanisms and potential Argonaute effectors compared to meiotic 24-nt phasiRNAs. We show that specific Argonaute genes coexpressed with stage-specific phasiRNAs are conserved across Bambusoideae and Pooideae species. Our degradome analysis identified a set of conserved miRNA target genes across species, while 21-nt phasiRNA targets were species-specific. Cleavage of few targets was observed for 24-nt phasiRNAs. In summary, this study demonstrates that premeiotic 24-nt phasiRNAs are present across Bambusoideae and Pooideae families, and the temporal accumulation of other classes of 21-nt and 24-nt phasiRNA differs between bamboo and Pooideae species. Furthermore, targets of the 3 classes of phasiRNAs may be rapidly evolving or undetectable.

Original language	English
Article number	koae308
Number of pages	19
Journal	Plant Cell
Volume	37
Early online date	18 Nov 2024
DOIs	https://doi.org/10.1093/plcell/koae308
Publication status	Published - Jan 2025

ASJC Scopus subject areas

Plant Science

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10.1093/plcell/koae308

Cite this

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title = "Comparative RNA profiling identifies stage-specific phasiRNAs and coexpressed Argonaute genes in Bambusoideae and Pooideae species",

abstract = "Phased, small interfering RNAs (PhasiRNAs) play a crucial role in supporting male fertility in grasses. Earlier work in maize (Zea mays) and rice (Oryza sativa) - and subsequently many other plant species - identified premeiotic 21-nucleotide (nt) and meiotic 24-nt phasiRNAs. More recently, a group of premeiotic 24-nt phasiRNAs was discovered in the anthers of 2 Pooideae species, barley (Hordeum vulgare) and bread wheat (Triticum aestivum). Whether premeiotic 24-nt phasiRNAs and other classes of reproductive phasiRNAs are conserved across Pooideae species remains unclear. We conducted comparative RNA profiling of 3 anther stages in 6 Pooideae species and 1 Bambusoideae species. We observed complex temporal accumulation patterns of 21-nt and 24-nt phasiRNAs in Pooideae and Bambusoideae grasses. In Bambusoideae, 21-nt phasiRNAs accumulated during meiosis, whereas 24-nt phasiRNAs were present in both premeiotic and postmeiotic stages. We identified premeiotic 24-nt phasiRNAs in all 7 species examined. These phasiRNAs exhibit distinct biogenesis mechanisms and potential Argonaute effectors compared to meiotic 24-nt phasiRNAs. We show that specific Argonaute genes coexpressed with stage-specific phasiRNAs are conserved across Bambusoideae and Pooideae species. Our degradome analysis identified a set of conserved miRNA target genes across species, while 21-nt phasiRNA targets were species-specific. Cleavage of few targets was observed for 24-nt phasiRNAs. In summary, this study demonstrates that premeiotic 24-nt phasiRNAs are present across Bambusoideae and Pooideae families, and the temporal accumulation of other classes of 21-nt and 24-nt phasiRNA differs between bamboo and Pooideae species. Furthermore, targets of the 3 classes of phasiRNAs may be rapidly evolving or undetectable.",

author = "S{\'e}bastien B{\'e}langer and Junpeng Zhan and Yunqing Yu and Meyers, \{Blake C.\}",

year = "2025",

month = jan,

doi = "10.1093/plcell/koae308",

language = "English",

volume = "37",

journal = "Plant Cell",

issn = "1040-4651",

publisher = "American Society of Plant Biologists",

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TY - JOUR

T1 - Comparative RNA profiling identifies stage-specific phasiRNAs and coexpressed Argonaute genes in Bambusoideae and Pooideae species

AU - Bélanger, Sébastien

AU - Zhan, Junpeng

AU - Yu, Yunqing

AU - Meyers, Blake C.

PY - 2025/1

Y1 - 2025/1

N2 - Phased, small interfering RNAs (PhasiRNAs) play a crucial role in supporting male fertility in grasses. Earlier work in maize (Zea mays) and rice (Oryza sativa) - and subsequently many other plant species - identified premeiotic 21-nucleotide (nt) and meiotic 24-nt phasiRNAs. More recently, a group of premeiotic 24-nt phasiRNAs was discovered in the anthers of 2 Pooideae species, barley (Hordeum vulgare) and bread wheat (Triticum aestivum). Whether premeiotic 24-nt phasiRNAs and other classes of reproductive phasiRNAs are conserved across Pooideae species remains unclear. We conducted comparative RNA profiling of 3 anther stages in 6 Pooideae species and 1 Bambusoideae species. We observed complex temporal accumulation patterns of 21-nt and 24-nt phasiRNAs in Pooideae and Bambusoideae grasses. In Bambusoideae, 21-nt phasiRNAs accumulated during meiosis, whereas 24-nt phasiRNAs were present in both premeiotic and postmeiotic stages. We identified premeiotic 24-nt phasiRNAs in all 7 species examined. These phasiRNAs exhibit distinct biogenesis mechanisms and potential Argonaute effectors compared to meiotic 24-nt phasiRNAs. We show that specific Argonaute genes coexpressed with stage-specific phasiRNAs are conserved across Bambusoideae and Pooideae species. Our degradome analysis identified a set of conserved miRNA target genes across species, while 21-nt phasiRNA targets were species-specific. Cleavage of few targets was observed for 24-nt phasiRNAs. In summary, this study demonstrates that premeiotic 24-nt phasiRNAs are present across Bambusoideae and Pooideae families, and the temporal accumulation of other classes of 21-nt and 24-nt phasiRNA differs between bamboo and Pooideae species. Furthermore, targets of the 3 classes of phasiRNAs may be rapidly evolving or undetectable.

AB - Phased, small interfering RNAs (PhasiRNAs) play a crucial role in supporting male fertility in grasses. Earlier work in maize (Zea mays) and rice (Oryza sativa) - and subsequently many other plant species - identified premeiotic 21-nucleotide (nt) and meiotic 24-nt phasiRNAs. More recently, a group of premeiotic 24-nt phasiRNAs was discovered in the anthers of 2 Pooideae species, barley (Hordeum vulgare) and bread wheat (Triticum aestivum). Whether premeiotic 24-nt phasiRNAs and other classes of reproductive phasiRNAs are conserved across Pooideae species remains unclear. We conducted comparative RNA profiling of 3 anther stages in 6 Pooideae species and 1 Bambusoideae species. We observed complex temporal accumulation patterns of 21-nt and 24-nt phasiRNAs in Pooideae and Bambusoideae grasses. In Bambusoideae, 21-nt phasiRNAs accumulated during meiosis, whereas 24-nt phasiRNAs were present in both premeiotic and postmeiotic stages. We identified premeiotic 24-nt phasiRNAs in all 7 species examined. These phasiRNAs exhibit distinct biogenesis mechanisms and potential Argonaute effectors compared to meiotic 24-nt phasiRNAs. We show that specific Argonaute genes coexpressed with stage-specific phasiRNAs are conserved across Bambusoideae and Pooideae species. Our degradome analysis identified a set of conserved miRNA target genes across species, while 21-nt phasiRNA targets were species-specific. Cleavage of few targets was observed for 24-nt phasiRNAs. In summary, this study demonstrates that premeiotic 24-nt phasiRNAs are present across Bambusoideae and Pooideae families, and the temporal accumulation of other classes of 21-nt and 24-nt phasiRNA differs between bamboo and Pooideae species. Furthermore, targets of the 3 classes of phasiRNAs may be rapidly evolving or undetectable.

UR - https://www.scopus.com/pages/publications/85214320209

U2 - 10.1093/plcell/koae308

DO - 10.1093/plcell/koae308

M3 - Article

C2 - 39556763

AN - SCOPUS:85214320209

SN - 1040-4651

VL - 37

JO - Plant Cell

JF - Plant Cell

M1 - koae308

ER -

Comparative RNA profiling identifies stage-specific phasiRNAs and coexpressed Argonaute genes in Bambusoideae and Pooideae species

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