Andrew L. Eamens

University of the Sunshine Coast

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i-10 index

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Peter M. Waterhouse

Queensland University of Technology

Brett Nixon

University of Newcastle Australia

Christopher P. L. Grof

University of Newcastle Australia

Joseph L. Pegler

University of Newcastle Australia

Matthew D. Dun

University of Newcastle Australia

Jackson M. J. Oultram

University of Newcastle Australia

Ming‐Bo Wang

Nantong University

Geoffry N. De Iuliis

University of Newcastle Australia

Shaun J. Curtin

University of Minnesota

Neil A. Smith

Commonwealth Scientific and Industrial Research Organisation

Cooperative Institutions

University of Newcastle Australia

Commonwealth Scientific and Industrial Research Organisation

Hunter Medical Research Institute

Plant Industry

Agriculture and Food

ACT Government

University of Sydney

University of Queensland

Chinese Academy of Sciences

University of Chinese Academy of Sciences

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Characterisation of mouse epididymosomes reveals a complex profile of microRNAs and a potential mechanism for modification of the sperm epigenome

Scientific Reports (2016)

Jackson N. Reilly Eileen A. McLaughlin Simone J. Stanger Amanda L. Anderson Kate Hutcheon

Recent evidence has shown that the sperm epigenome is vulnerable to dynamic modifications arising from a variety of paternal environment exposures and that this legacy can serve as an important determinant of intergenerational inheritance. It has been postulated that such exchange is communicated to maturing spermatozoa via the transfer of small non-protein-coding RNAs (sRNAs) in a mechanism mediated by epididymosomes; small membrane bound vesicles released by the soma of the male reproductive tract (epididymis). Here we confirm that mouse epididymosomes encapsulate an impressive cargo of >350 microRNAs (miRNAs), a developmentally important sRNA class, the majority (~60%) of which are also represented by the miRNA signature of spermatozoa. This includes >50 miRNAs that were found exclusively in epididymal sperm and epididymosomes, but not in the surrounding soma. We also documented substantial changes in the epididymosome miRNA cargo, including significant fold changes in almost half of the miRNAs along the length of the epididymis. Finally, we provide the first direct evidence for the transfer of several prominent miRNA species between mouse epididymosomes and spermatozoa to afford novel insight into a mechanism of intercellular communication by which the sRNA payload of sperm can be selectively modified during their post-testicular maturation.

Epigenome

10.1038/srep31794

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Citations (195)

Sub-chronic elevation in ambient temperature drives alterations to the sperm epigenome and accelerates early embryonic development in mice

bioRxiv (Cold Spring Harbor Laboratory) (2024)

Natalie A. Trigg John E. Schjenken Jacinta H. Martin David A. Skerrett‐Byrne Shannon P. Smyth

Forecasted increases in the prevalence and severity of extreme weather events accompanying changes in climatic behavior pose potential risk to the reproductive capacity of humans and animals of ecological and agricultural significance. While several studies have revealed that heat stress induced by challenges such as testicular insulation can elicit a marked negative effect on the male reproductive system, and particularly the production of spermatozoa, less is known about the immediate impact on male reproductive function following sub-chronic whole-body exposure to elevated ambient temperature. To address this knowledge gap, we exposed unrestrained male mice to heat stress conditions that emulate a heat wave (daily cycle of 8 h at 35°C followed by 16 h at 25°C) for a period of seven days. Neither the testes or epididymides of heat exposed male mice exhibited evidence of gross histological change, and similarly, spermatozoa of exposed males retained their functionality and ability to support embryonic development. However, the embryos generated from heat exposed spermatozoa experienced pronounced changes in gene expression linked to acceleration of early embryo development, aberrant blastocyst hatching and increased fetal weight. Such changes were causally associated with an altered sperm small non-coding RNA (sncRNA) profile, such that these developmental phenotypes were recapitulated by microinjection of wild-type embryos sired by control spermatozoa with RNAs extracted from heat exposed spermatozoa. Such data highlight that even a relatively modest excursion in ambient temperature can affect male reproductive function and identify the sperm sncRNA profile as a particular point of vulnerability to this imposed environmental stress.

Epigenome

Elevation (ballistics)

10.1101/2024.07.22.604196

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Citations (1)

Acrylamide modulates the mouse epididymal proteome to drive alterations in the sperm small non-coding RNA profile and dysregulate embryo development

Cell Reports (2021)

Natalie A. Trigg David A. Skerrett‐Byrne Miguel J. Xavier Wei Zhou Amanda L. Anderson

Paternal exposure to environmental stressors elicits distinct changes to the sperm sncRNA profile, modifications that have significant post-fertilization consequences. Despite this knowledge, there remains limited mechanistic understanding of how paternal exposures modify the sperm sncRNA landscape. Here, we report the acute sensitivity of the sperm sncRNA profile to the reproductive toxicant acrylamide. Furthermore, we trace the differential accumulation of acrylamide-responsive sncRNAs to coincide with sperm transit of the proximal (caput) segment of the epididymis, wherein acrylamide exposure alters the abundance of several transcription factors implicated in the expression of acrylamide-sensitive sncRNAs. We also identify extracellular vesicles secreted from the caput epithelium in relaying altered sncRNA profiles to maturing spermatozoa and dysregulated gene expression during early embryonic development following fertilization by acrylamide-exposed spermatozoa. These data provide mechanistic links to account for how environmental insults can alter the sperm epigenome and compromise the transcriptomic profile of early embryos.

Epigenome

Toxicant

10.1016/j.celrep.2021.109787

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Citations (34)

RNA Silencing in Plants: Yesterday, Today, and Tomorrow

PLANT PHYSIOLOGY (2008)

Andrew L. Eamens Ming‐Bo Wang Neil A. Smith Peter M. Waterhouse

Yesterday

RNA Silencing

RNA world hypothesis

Trans-acting siRNA

RNA-induced transcriptional silencing

RNA-induced silencing complex

10.1104/pp.108.117275

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Citations (311)

Additional file 1 of The abundance of a transfer RNA-derived RNA fragment small RNA subpopulation is enriched in cauda spermatozoa

Figshare (2020)

Simone J. Stanger Ilana R. Bernstein Amanda L. Anderson Kate Hutcheon Matthew D. Dun

Additional file 1: Table S1. Abundance of 19- to 36-nt small RNAs in epididymal spermatozoa, Table S2. Small RNA species abundance in spermatozoa sourced from the mouse epididymis, Table S3. Abundance of 27–35-nt tRFs in caput, corpus and cauda spermatozoa, Table S4. Abundance of cauda spermatozoa enriched tRF5 small RNAs, Table S5. RT-qPCR confirmation of tRF5 small RNA enrichment in cauda spermatozoa, Table S6. Abundance of the cauda spermatozoa enriched tRF5 small RNA population across epithelial cells, epididymosomes and spermatozoa sourced from the caput, corpus and cauda epididymis.

Fragment (logic)

10.6084/m9.figshare.13173712

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A bidirectional gene trap construct suitable for T‐DNA and Ds‐mediated insertional mutagenesis in rice (Oryza sativa L.)

Plant Biotechnology Journal (2004)

Andrew L. Eamens Christopher Blanchard Elizabeth S. Dennis Narayana M. Upadhyaya

Summary A construct suitable for genome‐wide transfer‐DNA (T‐DNA) and subsequent transposon‐based ( Ds ) gene trapping has been developed for use in rice ( Oryza sativa ). This T‐DNA/ Ds construct contains: Ds terminal sequences immediately inside T‐DNA borders for subsequent Ds mobilization; promoterless green fluorescent protein ( sgfpS65T ) and β‐glucuronidase ( uidA ) reporter genes, each fused to an intron (from Arabidopsis GPA1 gene) to enable bidirectional gene trapping by T‐DNA or Ds ; an ampicillin resistance gene ( bla ) and a bacterial origin of replication ( ori ) to serve as the plasmid rescue system; an intron‐containing hygromycin phosphotransferase gene ( hph ) as a selectable marker or Ds tracer; and an intron‐containing barnase gene in the binary vector backbone (VB) to select against transformants carrying unwanted VB sequences. More than a threefold increase over previously reported reporter gene‐based gene trapping efficiencies was observed in primary T‐DNA/ Ds transformant rice lines, returning an overall reporter gene expression frequency of 23%. Of the plant organs tested, 3.3–7.4% expressed either reporter at varying degrees of organ or tissue specificity. Approximately 70% of the right border (RB) flanking sequence tags (FSTs) retained 1–6 bp of the RB repeat and 30% of the left border (LB) FSTs retained 5–23 bp of the LB repeat. The remaining FSTs carried deletions of 2–84 bp inside the RB or 1–97 bp inside the LB. Transposition of Ds from the original T‐DNA was evident in T‐DNA/ Ds callus lines super‐transformed with a transposase gene ( Ac ) construct, as indicated by gene trap reporter activity and rescue of new FSTs in the resulting double transformant lines.

Transposase

Insertional mutagenesis

Genetically modified rice

10.1111/j.1467-7652.2004.00081.x

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Citations (37)

The Arabidopsis thaliana Double-Stranded RNA Binding Proteins DRB1 and DRB2 Are Required for miR160-Mediated Responses to Exogenous Auxin

Genes (2024)

Kathy Zimmerman Joseph L. Pegler Jackson M. J. Oultram David A. Collings Ming‐Bo Wang

DOUBLE-STRANDED RNA BINDING (DRB) proteins DRB1, DRB2, and DRB4 are essential for microRNA (miRNA) production in Arabidopsis thaliana (Arabidopsis) with miR160, and its target genes, AUXIN RESPONSE FACTOR10 (ARF10), ARF16, and ARF17, forming an auxin responsive miRNA expression module crucial for root development. Methods: Wild-type Arabidopsis plants (Columbia-0 (Col-0)) and the drb1, drb2, and drb12 mutants were treated with the synthetic auxin 2,4-dichlorophenoxyacetic acid (2,4-D), and the miR160-mediated response of these four Arabidopsis lines was phenotypically and molecularly characterized. Results: In 2,4-D-treated Col-0, drb1 and drb2 plants, altered miR160 abundance and ARF10, ARF16, and ARF17 gene expression were associated with altered root system development. However, miR160-directed molecular responses to treatment with 2,4-D was largely defective in the drb12 double mutant. In addition, via profiling of molecular components of the miR160 expression module in the roots of the drb4, drb14, and drb24 mutants, we uncovered a previously unknown role for DRB4 in regulating miR160 production. Conclusions: The miR160 expression module forms a central component of the molecular and phenotypic response of Arabidopsis plants to exogenous auxin treatment. Furthermore, DRB1, DRB2, and DRB4 are all required in Arabidopsis roots to control miR160 production, and subsequently, to appropriately regulate ARF10, ARF16, and ARF17 target gene expression.

10.3390/genes15121648

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RNA silencing in plants: Yesterday, today, and tomorrow

Science & Engineering Faculty (2008)

Andrew L. Eamens M.B. Wang Neil A. Smith Peter M. Waterhouse

RNA silencing has become a major focus of molecular biology and biomedical research around the world. This is highlighted by a simple PubMed search for “RNA silencing,” which retrieves almost 9,000 articles. Interest in gene silencing-related mechanisms stemmed from the early 1990s, when this phenomenon was first noted as a surprise observation by plant scientists during the course of plant transformation experiments, in which the introduction of a transgene into the genome led to the silencing of both the transgene and homologous endogenes. From these initial studies, plant biologists have continued to generate a wealth of information into not only gene silencing mechanisms but also the complexity of these biological pathways as well as revealing their multilevel interactions with one another. The plant biology community has also made significant advancements in exploiting RNA silencing as a powerful tool for gene function studies and crop improvements. In this article, we (1) review the rich history of gene silencing research and the knowledge it has generated into our understanding of this fundamental mechanism of gene regulation in plants; (2) describe examples of the current applications of RNA silencing in crop plants; and (3) discuss improvements in RNA silencing technology and its potential application in plant science.

RNA Silencing

RNA-induced silencing complex

Trans-acting siRNA

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DRB2, DRB3 and DRB5 function in a non-canonical microRNA pathway inArabidopsis thaliana

Plant Signaling & Behavior (2012)

Andrew L. Eamens Ki Wook Kim Peter M. Waterhouse

DOUBLE-STRANDED RNA BINDING (DRB) proteins have been functionally characterized in viruses, prokaryotes and eukaryotes and are involved in all aspects of RNA biology. Arabidopsis thaliana (Arabidopsis) encodes five closely related DRB proteins, DRB1 to DRB5. DRB1 and DRB4 are required by DICER-LIKE (DCL) proteins DCL1 and DCL4 to accurately and efficiently process structurally distinct double-stranded RNA (dsRNA) precursor substrates in the microRNA (miRNA) and trans-acting small-interfering RNA (tasiRNA) biogenesis pathways respectively. We recently reported that DRB2 is also involved in the biogenesis of specific miRNA subsets. ( 1) Furthermore, the severity of the developmental phenotype displayed by the drb235 triple mutant plant, compared with those expressed by either drb2, drb3 and drb5 single mutants, or double mutant combinations thereof, indicates that DRB3 and DRB5 function in the same non-canonical miRNA pathway as DRB2. Through the use of our artificial miRNA (amiRNA) plant expression vector, pBlueGreen ( 2) (,) ( 3) we demonstrate here that unlike DRB2, DRB3 and DRB5 are not involved in the dsRNA processing stages of the miRNA biogenesis pathway, but are required to mediate RNA silencing of target genes of DRB2-associated miRNAs.

Dicer

RNA Silencing

Trans-acting siRNA

10.4161/psb.21518

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Citations (61)

Gene regulation by translational inhibition is determined by Dicer partnering proteins

Science & Engineering Faculty (2015)

Rodrigo S. Reis Gene Hart‐Smith Andrew L. Eamens Marc R. Wilkins Peter M. Waterhouse

MicroRNAs (miRNAs) are small regulatory RNAs produced by Dicer proteins that regulate gene expression in development and adaptive responses to the environment1,2,3,4. In animals, the degree of base pairing between a miRNA and its target messenger RNA seems to determine whether the regulation occurs through cleavage or translation inhibition1. In contrast, the selection of regulatory mechanisms is independent of the degree of mismatch between a plant miRNA and its target transcript5. However, the components and mechanism(s) that determine whether a plant miRNA ultimately regulates its targets by guiding cleavage or translational inhibition are unknown6. Here we show that the form of regulatory action directed by a plant miRNA is determined by DRB2, a DICER-LIKE1 (DCL1) partnering protein. The dependence of DCL1 on DRB1 for miRNA biogenesis is well characterized7,8,9, but we show that it is only required for miRNA-guided transcript cleavage. We found that DRB2 determines miRNA-guided translational inhibition and represses DRB1 expression, thereby allowing the active selection of miRNA regulatory action. Furthermore, our results reveal that the core silencing proteins ARGONAUTE1 (AGO1) and SERRATE (SE) are highly regulated by miRNA-guided translational inhibition. DRB2 has been remarkably conserved throughout plant evolution, raising the possibility that translational repression is the ancient form of miRNA-directed gene regulation in plants, and that Dicer partnering proteins, such as human TRBP, might play a similar role in other eukaryotic systems.

Dicer

Argonaute

Ribonuclease III

Translational efficiency

Translational regulation

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