Loss of function of Arabidopsis microRNA-machinery genes impairs fertility, and has effects on homologous recombination and meiotic chromatin dynamics

Oliver, Cecilia; Pradillo, Mónica; Jover-Gil, Sara; Cuñado, N.; Ponce, Marı́a Rosa; Santos, Juan Luis

doi:10.1038/s41598-017-07702-x

Cited by 19 publications

(26 citation statements)

References 70 publications

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“…Indeed, reciprocal crosses between wild type and the heterozygous hen1-8 indicated that both male and female transmission of hen1-8 are normal (Supplementary Table S1). The discrepancy between the previous report (Oliver et al, 2017) and ours might be due to the fact that hen1-8 and hen1-2 are weaker alleles of HEN1.…”

Section: Discussioncontrasting

confidence: 99%

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HUA ENHANCER1 Mediates Ovule Development

et al. 2020

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Ovules are female reproductive organs of angiosperms, containing sporophytic integuments and gametophytic embryo sacs. After fertilization, embryo sacs develop into embryos and endosperm whereas integuments into seed coat. Ovule development is regulated by transcription factors (TF) whose expression is often controlled by microRNAs. Mutations of Arabidopsis DICER-LIKE 1 (DCL1), a microRNA processing protein, caused defective ovule development and reduced female fertility. However, it was not clear whether other microRNA processing proteins participate in this process and how defective ovule development influenced female fertility. We report that mutations of HUA ENHANCER1 (HEN1) and HYPONASTIC LEAVES 1 (HYL1) interfered with integument growth. The sporophytic defect caused abnormal embryo sac development and inability of mutant ovules to attract pollen tubes, leading to reduced female fertility. We show that the role of HEN1 in integument growth is cell-autonomous. Although AUXIN RESPONSE FACTOR 6 (ARF6) and ARF8 were ectopically expressed in mutant ovules, consistent with the reduction of microRNA167 in hen1, introducing arf6;arf8 did not suppress ovule defects of hen1, suggesting the involvement of more microRNAs in this process. Results presented indicate that the microRNA processing machinery is critical for ovule development and seed production through multiple microRNAs and their targets.

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Section: Discussioncontrasting

confidence: 99%

“…A recent study reported that the mutations of HYL1, DCL1, or HEN1 caused a reduced number of pollen and megaspore mother cells (Oliver et al, 2017). Our results strongly suggested that fertility reduction in hen1-8 was due to abnormal ovule development (Figure 3).…”

Section: Discussionsupporting

confidence: 70%

HUA ENHANCER1 Mediates Ovule Development

et al. 2020

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“…A possible explanation for this difference is the existence of the miRNA-triggered 24-nt phasiRNA pathway in monocots (Zhai et al, 2015). On the other hand, mutants of Arabidopsis miRNAmachinery genes have a relaxed meiotic chromatin conformation (Oliver et al, 2017), confirming a broad role for miRNAs in plant meiosis. Previous work in maize (Dukowic-Schulze et al, 2016) and sunflower (Helianthus annuus;Flórez-Zapata et al, 2016) meiocytes, and our results have revealed conserved miRNAs that are preferentially expressed in meiocytes, including miR390 and miR167 (Fig.…”

Section: Discussionmentioning

confidence: 99%

“…Prior analysis of Arabidopsis miRNA biogenesis loss-of-function mutants revealed a defect in meiotic chromatin morphology (Oliver et al, 2017). However, the role of specific miRNAs in meiocytes remains unclear.…”

Section: Identification Of Mirnas Preferentially Expressed In Arabidomentioning

confidence: 99%

Conservation and Divergence in the Meiocyte sRNAomes of Arabidopsis, Soybean, and Cucumber

Huang

Fang

et al. 2019

Plant Physiol.

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Meiosis is a critical process for sexual reproduction. During meiosis, genetic information on homologous chromosomes is shuffled through meiotic recombination to produce gametes with novel allelic combinations. Meiosis and recombination are orchestrated by several mechanisms including regulation by small RNAs (sRNAs). Our previous work in Arabidopsis (Arabidopsis thaliana) meiocytes showed that meiocyte-specific sRNAs (ms-sRNAs) have distinct characteristics, including positive association with the coding region of genes that are transcriptionally upregulated during meiosis. Here, we characterized the ms-sRNAs in two important crops, soybean (Glycine max) and cucumber (Cucumis sativus). Ms-sRNAs in soybean have the same features as those in Arabidopsis, suggesting that they may play a conserved role in eudicots. We also investigated the profiles of microRNAs (miRNAs) and phased secondary small interfering RNAs in the meiocytes of all three species. Two conserved miRNAs, miR390 and miR167, are highly abundant in the meiocytes of all three species. In addition, we identified three novel cucumber miRNAs. Intriguingly, our data show that the previously identified phased secondary small interfering RNA pathway involving soybean-specific miR4392 is more abundant in meiocytes. These results showcase the conservation and divergence of ms-sRNAs in flowering plants, and broaden our understanding of sRNA function in crop species.

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“…Gene expression can be controlled at the RNA level, both quantitatively and qualitatively, and at various steps during RNA processing (alternative splicing, RNA editing, RNA silencing and translation regulation among others), with important consequences for the availability of different kinds of transcripts, and ultimately of proteins. The importance of the RNA interference (RNAi) machinery during meiosis has become clear in recent years (Dukowic-Schulze et al, 2014, 2016; Flórez-Zapata et al, 2016; Wu et al, 2017; Oliver et al, 2017), with small RNAs adding additional layers to the regulation of gene expression. A good example of this are phasiRNAs, a type of 21− and 24-nt phased, secondary siRNA from non-repeat regions produced specifically in male monocot meiotic transcriptomes (Johnson et al, 2009; Song et al, 2012), and whose function remains elusive.…”

Section: Discussionmentioning

confidence: 99%

Genome-wide transcription during early wheat meiosis is independent of synapsis, ploidy level and thePh1locus

Martín

Borrill

Higgins

et al. 2018

Preprint

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Polyploidization is a fundamental process in plant evolution. One of the biggest challenges faced by a new polyploid is meiosis, particularly discriminating between multiple related chromosomes so that only homologous chromosomes synapse and recombine to ensure regular chromosome segregation and balanced gametes. Despite its large genome size, high DNA repetitive content and similarity between homoeologous chromosomes, hexaploid wheat completes meiosis in a shorter period than diploid species with a much smaller genome. Therefore, during wheat meiosis, mechanisms additional to the classical model based on DNA sequence homology, must facilitate more efficient homologous recognition. One such mechanism could involve exploitation of differences in chromosome structure between homologues and homoeologues at the onset of meiosis. In turn, these chromatin changes, can be expected to be linked to transcriptional gene activity. In this study, we present an extensive analysis of a large RNA-Seq data derived from six different genotypes: wheat, wheat-rye hybrids and newly synthesized octoploid triticale, both in the presence and absence of the Ph1 locus. Plant material was collected at early prophase, at the transition leptotene-zygotene, when the telomere bouquet is forming and synapsis between homologues is beginning. The six genotypes exhibit different levels of synapsis and chromatin structure at this stage; therefore, recombination and consequently segregation, are also different. Unexpectedly, our study reveals that neither synapsis, whole genome duplication nor the absence of the Ph1 locus are associated with major changes in gene expression levels during early meiotic prophase. Overall wheat transcription at this meiotic stage is therefore highly resilient to such alterations, even in the presence of major chromatin structural changes. This suggests that post-transcriptional and post-translational processes are likely to be more important. Thus, further studies will be required to reveal whether these observations are specific to wheat meiosis, and whether there are significant changes in post-transcriptional and post-translational modifications in wheat and other polyploid species associated with their polyploidisation.

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Loss of function of Arabidopsis microRNA-machinery genes impairs fertility, and has effects on homologous recombination and meiotic chromatin dynamics

Cited by 19 publications

References 70 publications

HUA ENHANCER1 Mediates Ovule Development

HUA ENHANCER1 Mediates Ovule Development

Conservation and Divergence in the Meiocyte sRNAomes of Arabidopsis, Soybean, and Cucumber

Genome-wide transcription during early wheat meiosis is independent of synapsis, ploidy level and thePh1locus

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