Targeted suppression of siRNA biogenesis in Arabidopsis pollen reveals distinct Pol IV activities in the sperm and vegetative cell lineages

Pachamuthu, Kannan; Simon, Matthieu; Borges, Filipe

doi:10.21203/rs.3.rs-2947716/v1

Cited by 3 publications

(7 citation statements)

References 49 publications

(54 reference statements)

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“…5A ). This was recently suggested by elegant VC- and SC-specific siRNA ablation experiments ( Pachamuthu et al 2023 ) ( Fig. 4, C and D ) and is further discussed here.…”

Section: Classes Biogenesis and Functions Of Plant Sirnassupporting

confidence: 79%

The plant siRNA landscape

Vaucheret,

Voinnet

2023

The Plant Cell

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Whereas micro (mi)RNAs are considered the clean, noble side of the small RNA world, small interfering (si)RNAs are often seen as a noisy set of molecules whose barbarian acronyms reflect a large diversity of often elusive origins. 25 years after their discovery in plants, however, new classes of siRNAs are still being identified, sometimes in discrete tissues or at particular developmental stages, making the plant siRNA world substantially more complex and subtle than originally anticipated. Focusing primarily on the model Arabidopsis, we review here the plant siRNA landscape, including transposable elements (TE)-derived siRNAs, a vast array of non-TE-derived endogenous siRNAs, as well as exogenous siRNAs produced in response to invading nucleic acids such as viruses or transgenes. We primarily emphasize the extraordinary sophistication and diversity of their biogenesis and, secondarily, the variety of their known or presumed functions, including via non-cell autonomous activities, in the sporophyte, gametophyte and shortly after fertilization.

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“…5A ). This was recently suggested by elegant VC- and SC-specific siRNA ablation experiments ( Pachamuthu et al 2023 ) ( Fig. 4, C and D ) and is further discussed here.…”

Section: Classes Biogenesis and Functions Of Plant Sirnassupporting

confidence: 79%

The plant siRNA landscape

Vaucheret,

Voinnet

2023

The Plant Cell

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“…4f,h). One possible explanation is that psd acts gametophytically, within the pollen grain itself, supporting the observation that VN-derived 21-22nt easiRNA, but not SC-derived small RNA, are required for the triploid block 44 .…”

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confidence: 58%

“…RTL1 is such a viral surveillance mechanism and is induced strongly on viral infection 56 . While VN-derived easiRNA are suppressed when RTL1 is expressed in the VN, they are not suppressed when RTL1 is expressed in SC even though VN-derived easiRNA accumulate in SC 44 . An intriguing explanation might be that easiRNA pseudouridylation requires export from the VN, and RTL1 cannot recognize these easiRNA once they are pseudouridylated.…”

mentioning

confidence: 93%

“…However, easiRNAs accumulate in sperm cells, and are thought to be transported there from the VN 6–8 . In a recent study, small RNA biogenesis in the VN and in the SC were independently suppressed by expressing the RNAseIII-like protein RTL1 in each cell type 44 . We found that both VN-derived and SC-derived small RNA were enriched for Ψ, and that enrichment depended on psd (Fig.…”

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confidence: 99%

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Pseudouridine guides germline small RNA transport and epigenetic inheritance

Herridge

Dolata

Migliori

et al. 2023

Preprint

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Epigenetic modifications that arise during plant and animal development, such as DNA and histone modification, are mostly reset during gamete formation, but some are inherited from the germline including those marking imprinted genes. Small RNAs guide these epigenetic modifications, and some are also inherited by the next generation. In C. elegans, inherited small RNA precursors have poly (UG) tails, but how inherited small RNAs are distinguished in other animals and plants is unknown. Pseudouridine (Ψ) is the most abundant RNA modification but has not been explored in small RNAs. Here, we develop novel assays to detect Ψ in short RNA sequences, demonstrating its presence in mouse and Arabidopsis microRNAs and their precursors. We also detect substantial enrichment in germline small RNAs, namely epigenetically activated siRNAs (easiRNAs) in Arabidopsis pollen, and piwi-interacting piRNAs in mouse testis. In pollen, pseudouridylated easiRNAs are localized to sperm cells, and we found that PAUSED/HEN5 (PSD), the plant homolog of Exportin-t, interacts genetically with Ψ and is required for transport of easiRNAs into sperm cells from the vegetative nucleus. We further show that Exportin-t is required for the triploid block: chromosome dosage-dependent seed lethality that is epigenetically inherited from pollen. Thus, Ψ has a conserved role in marking inherited small RNAs in the germline.

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“…In contrast to other RdDM pathway mutants, nrpd1 (affected in the large subunit of Pol IV, NUCLEAR RNA POLYMERASE D1) exhibits a suppressive effect in the first generation of inbreeding ( Wang et al 2021 ), suggesting that the loss of easiRNAs and paternal DNA methylation can independently suppress the triploid block. Recent findings further support this notion, revealing that the depletion of easiRNAs in the vegetative cell of pollen (but not in sperm cells) can suppress the triploid block ( Pachamuthu et al 2023 ). Whether paternally delivered easiRNAs are causally responsible for DNA methylation changes in the endosperm as previously proposed ( Martinez et al 2018 ) remains to be investigated.…”

Section: Genomic Imprinting: An Epigenetic Phenomenon Underpinning Re...mentioning

confidence: 79%

Molecular basis and evolutionary drivers of endosperm-based hybridization barriers

Bente,

Köhler

2024

Plant Physiology

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The endosperm, a transient seed tissue, plays a pivotal role in supporting embryo growth and germination. This unique feature sets flowering plants apart from gymnosperms, marking an evolutionary innovation in the world of seed-bearing plants. Nevertheless, the importance of the endosperm extends beyond its role in providing nutrients to the developing embryo by acting as a versatile protector, preventing hybridization events between distinct species and between individuals with different ploidy. This phenomenon centers on growth and differentiation of the endosperm and the speed at which both processes unfold. Emerging studies underscore the important role played by type I MADS-box transcription factors, including the paternally expressed gene PHERES1. These factors, along with downstream signaling pathways involving auxin and abscisic acid, are instrumental in regulating endosperm development and, consequently, the establishment of hybridization barriers. Moreover, mutations in various epigenetic regulators mitigate these barriers, unveiling a complex interplay of pathways involved in their formation. In this review, we discuss the molecular underpinnings of endosperm-based hybridization barriers and their evolutionary drivers.

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Targeted suppression of siRNA biogenesis in Arabidopsis pollen reveals distinct Pol IV activities in the sperm and vegetative cell lineages

Cited by 3 publications

References 49 publications

The plant siRNA landscape

The plant siRNA landscape

Pseudouridine guides germline small RNA transport and epigenetic inheritance

Molecular basis and evolutionary drivers of endosperm-based hybridization barriers

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