A methylation status analysis of the apomixis-specific region in Paspalum spp. suggests an epigenetic control of parthenogenesis

Podio, Maricel; Cáceres, María Eugenia; Samoluk, Sergio Sebastián; Seijo, Guillermo; Pessino, Silvina Claudia; Ortiz, Juan Pablo Amelio; Pupilli, Fulvio

doi:10.1093/jxb/eru354

Cited by 48 publications

(56 citation statements)

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“…This has led to the hypothesis that the ACL region modulates epigenetic processes regulating parthenogenesis and endosperm formation. This is consistent with the finding that parthenogenesis is superimposed on sexual reproduction in this system and that DNA demethylation affects parthenogenesis but not apomeiosis [29,51]. In particular the homologue of subunit 3 of the ORIGIN RECOGNITION COMPLEX (ORC3), which is functional in sexual plants, is regulated by an apomixis specific antisense pseudogene [68] ( Table 1).…”

Section: Genes Located On Apomixis Loci Suggest That Different Regulasupporting

confidence: 89%

“…However, this view is challenged by new findings and hypotheses [6,18]. In some systems like Hieracium and likely also in Paspalum, apomixis is superimposed on sexual reproduction and dominantly silencing sexual reproduction [22,29]. Interestingly, thereby the sexual pathway can be re-established, suggesting that the gene regulatory program underlying sexual reproduction remains intact.…”

Section: The Developmental Flexibility Of Plant Reproduction Might Homentioning

confidence: 99%

“…While it has been hypothesized that these chromosomes might be relevant for apomixis expression and in particular possible implications for diplospory have been discussed, transmission of a Het chromosome alone is not sufficient for apomixis to arise [23,59]. Interestingly, the Het chromosomes and heterochromatic chromosomal regions linked to apomixis resemble features of Y-chromosomes in animals and dioecious plants for sex determination with respect to typical accumulation of transposable elements and gene loss [29,46,60]. Therefore, it is tempting to speculate that similarly to well known mechanisms in Y-chromosomes, epigenetic regulatory mechanisms might be major driving forces in regulation of apomixis.…”

Section: Genetic Loci Linked To Apomixis Typically Represent Hemizygomentioning

confidence: 99%

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Controlling Apomixis: Shared Features and Distinct Characteristics of Gene Regulation

Schmidt

2020

Genes

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In higher plants, sexual and asexual reproduction through seeds (apomixis) have evolved as alternative strategies. As apomixis leads to the formation of clonal offspring, its great potential for agricultural applications has long been recognized. However, the genetic basis and the molecular control underlying apomixis and its evolutionary origin are to date not fully understood. Both in sexual and apomictic plants, reproduction is tightly controlled by versatile mechanisms regulating gene expression, translation, and protein abundance and activity. Increasing evidence suggests that interrelated pathways including epigenetic regulation, cell-cycle control, hormonal pathways, and signal transduction processes are relevant for apomixis. Additional molecular mechanisms are being identified that involve the activity of DNA- and RNA-binding proteins, such as RNA helicases which are increasingly recognized as important regulators of reproduction. Together with other factors including non-coding RNAs, their association with ribosomes is likely to be relevant for the formation and specification of the apomictic reproductive lineage. Subsequent seed formation appears to involve an interplay of transcriptional activation and repression of developmental programs by epigenetic regulatory mechanisms. In this review, insights into the genetic basis and molecular control of apomixis are presented, also taking into account potential relations to environmental stress, and considering aspects of evolution.

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Section: Genes Located On Apomixis Loci Suggest That Different Regulasupporting

confidence: 89%

Section: The Developmental Flexibility Of Plant Reproduction Might Homentioning

confidence: 99%

Section: Genetic Loci Linked To Apomixis Typically Represent Hemizygomentioning

confidence: 99%

See 1 more Smart Citation

Controlling Apomixis: Shared Features and Distinct Characteristics of Gene Regulation

Schmidt

2020

Genes

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“…Apomictic polyploids were likely derived from initially unstable diploid apomictic hybrids, and they seem to feature high heterozygosity necessary for sustenance of apomixis due to dosage-dependent gene regulation leading to efficient management of deleterious mutations (Archetti, 2004). In addition, ploidy shifts lead to changes in epigenetic landscape, for instance in DNA methylation within several loci, and concomitant transcriptional reprogramming wired by the RNA-dependent DNA methylation (RdDM) pathways required for initiation and maintenance of apomictic traits (Verhoeven et al, 2010; Hand and Koltunow, 2014; Podio et al, 2014; Zappacosta et al, 2014). Thus, hybridization-derived polyploidy could sustain apomixis in plant populations.…”

Section: Introductionmentioning

confidence: 99%

Depletion of Key Meiotic Genes and Transcriptome-Wide Abiotic Stress Reprogramming Mark Early Preparatory Events Ahead of Apomeiotic Transition

et al. 2016

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Molecular dissection of apomixis – an asexual reproductive mode – is anticipated to solve the enigma of loss of meiotic sex, and to help fixing elite agronomic traits. The Brassicaceae genus Boechera comprises of both sexual and apomictic species, permitting comparative analyses of meiotic circumvention (apomeiosis) and parthenogenesis. Whereas previous studies reported local transcriptome changes during these events, it remained unclear whether global changes associated with hybridization, polyploidy and environmental adaptation that arose during evolution of Boechera might serve as (epi)genetic regulators of early development prior apomictic initiation. To identify these signatures during vegetative stages, we compared seedling RNA-seq transcriptomes of an obligate triploid apomict and a diploid sexual, both isolated from a drought-prone habitat. Uncovered were several genes differentially expressed between sexual and apomictic seedlings, including homologs of meiotic genes ASYNAPTIC 1 (ASY1) and MULTIPOLAR SPINDLE 1 (MPS1) that were down-regulated in apomicts. An intriguing class of apomict-specific deregulated genes included several NAC transcription factors, homologs of which are known to be transcriptionally reprogrammed during abiotic stress in other plants. Deregulation of both meiotic and stress-response genes during seedling stages might possibly be important in preparation for meiotic circumvention, as similar transcriptional alteration was discernible in apomeiotic floral buds too. Furthermore, we noted that the apomict showed better tolerance to osmotic stress in vitro than the sexual, in conjunction with significant upregulation of a subset of NAC genes. In support of the current model that DNA methylation epigenetically regulates stress, ploidy, hybridization and apomixis, we noted that ASY1, MPS1 and NAC019 homologs were deregulated in Boechera seedlings upon DNA demethylation, and ASY1 in particular seems to be repressed by global DNA methylation exclusively in the apomicts. Variability in stress and transcriptional response in a diploid apomict, which is geographically distinct from the triploid apomict, pinpoints both common and independent features of apomixis evolution. Our study provides a molecular frame-work to investigate how the adaptive traits associated with the evolutionary history of apomicts co-adapted with meiotic gene deregulation at early developmental stage, in order to predate meiotic recombination, which otherwise is thought to be favorable in stress and low-fitness conditions.

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“…Contemporary studies have brought to light many exciting discoveries regarding the epigenetic regulation of apomixis in angiosperms (Verhoeven & Preite, 2014;Zappacosta et al, 2014). Recent research has revealed that apomixis genes are highly methylated in some lineages (e.g., in Paspalum; Podio et al, 2014) and that epigenetic modifications are involved in the regulation of embryo and endosperm development in asexual flowering plants (Hojsgaard et al, 2014). Because DNA methylation can be influenced by abiotic stressors (Rapp & Wendel, 2005;Verhoeven et al, 2010) and has been shown to be heritable in some contexts (Feng et al, 2010;Ferreira de Carvahlo et al, 2016), it is reasonable to infer that epigenetic modification could lead to the heritable expression of apomixis in response to environmental cues.…”

Section: Investigating Genome Dynamics Of Apomixis In Fernsmentioning

confidence: 99%

A current perspective on apomixis in ferns

Grusz

2016

J of Sytematics Evolution

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This review provides a synopsis of apogamous reproduction in ferns and highlights important progress made in the study of fern apomixis over the past decade. First, a summary of the apomictic fern life cycle is provided, distinguishing between two pathways to diploid spore production that have been documented in apomictic ferns (premeiotic endomitosis and meiotic first division restitution) and briefly discussing the evolutionary implications of each. Next, recent trends in fern apomixis research are highlighted, exposing a shift in focus from the observation and characterization of apomixis in ferns to more integrated studies of the evolutionary and ecological implications of this reproductive mode. Peer-reviewed contributions from the past decade are then summarized, spanning the identification of new apomictic lineages through to the developmental, phylogenetic, and population genetic insights that have been made in studies of fern apomixis during that time. Gaps in our understanding of fern apomixis are also discussed, including the extent and implications of recombinant apomixis in ferns, the possible reversibility of reproductive mode (from apomictic to sexual) in ferns, and the genomic causes and consequences of apomixis in seed A u t h o r M a n u s c r i p t A u t h o r M a n u s c r i p t A u t h o r M a n u s c r i p tGrusz, 2 of 23 free vascular plants. Finally, future directions for fern apomixis research are discussed in the context of modern technological advances and recent insights from studies of apomixis in other groups.Keywords: apogamy, evolution of sex, meiosis, pteridophytes.A u t h o r M a n u s c r i p t A u t h o r M a n u s c r i p t A u t h o r M a n u s c r i p t Grusz, 3 of 23 "…apomixis is an escape from sterility, but it is an escape into a blind alley of evolution…" -Darlington, 1939A renaissance is underway in fern biology, propelled, in part, by technological advances being embraced by a growing research community. In particular, modern, cost-effective tools are enabling new inquiries into the unique fern life cycle, which alternates between independent, free-living sporophyte and gametophyte generations (Haufler et al., 2016). Among the many aspects of fern reproduction that are being examined in light of new approaches-and an improved understanding of fern evolution as a whole-is their propensity for apogamous reproduction (i.e., apomixis). This form of asexual reproduction (by spore or seed) is more common in ferns than in any other group of vascular plants. Nearly 10% of the ferns for which reproductive mode has been determined exhibit apomixis (Walker, 1985; Liu et al., 2012), compared to less than 1% in flowering plants (Bicknell & Koltunow, 2004; Becks & Alavi, 2015). Given that data on reproductive mode is lacking for the vast majority of ferns, this relative contribution of apomicts to fern diversity may well be an underestimate (Liu et al., 2012). The elevated frequency and distinctive meiotic characteristics of apomixis in ferns, which are elaborated upon bel...

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A methylation status analysis of the apomixis-specific region in Paspalum spp. suggests an epigenetic control of parthenogenesis

Cited by 48 publications

References 84 publications

Controlling Apomixis: Shared Features and Distinct Characteristics of Gene Regulation

Controlling Apomixis: Shared Features and Distinct Characteristics of Gene Regulation

Depletion of Key Meiotic Genes and Transcriptome-Wide Abiotic Stress Reprogramming Mark Early Preparatory Events Ahead of Apomeiotic Transition

A current perspective on apomixis in ferns

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