Increased apomixis expression concurrent with genetic and epigenetic variation in a newly synthesized Eragrostis curvula polyploid

Zappacosta, Diego; Ochogavía, Ana Claudia; Rodrigo, Juan Manuel; Romero, José R.; Meier, M.; Garbus, Ingrid; Pessino, Silvina Claudia; Echenique, Viviana

doi:10.1038/srep04423

Cited by 26 publications

(42 citation statements)

References 22 publications

(39 reference statements)

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“…Our data show strong similarities to previous MSAP studies on the UNST1131 plant, which was obtained by chromosome doubling in a seed of the diploid plant UNST1122, as some of the polymorphisms identified had similarity to repetitive sequences [22]. Moreover, sequences with similarity to transposable elements have been shown to be differentially expressed in sexual and apomictic E .…”

Section: Resultssupporting

confidence: 85%

Apomixis frequency under stress conditions in weeping lovegrass (Eragrostis curvula)

et al. 2017

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To overcome environmental stress, plants develop physiological responses that are triggered by genetic or epigenetic changes, some of which involve DNA methylation. It has been proposed that apomixis, the formation of asexual seeds without meiosis, occurs through the temporal or spatial deregulation of the sexual process mediated by genetic and epigenetic factors influenced by the environment. Here, we explored whether there was a link between the occurrence of apomixis and various factors that generate stress, including drought stress, in vitro culture, and intraspecific hybridization. For this purpose, we monitored the embryo sacs of different weeping lovegrass (Eragrostis curvula [Schrad.] Nees) genotypes after the plants were subjected to these stress conditions. Progeny tests based on molecular markers and genome methylation status were analyzed following the stress treatment. When grown in the greenhouse, the cultivar Tanganyika INTA generated less than 2% of its progeny by sexual reproduction. Plants of this cultivar subjected to different stresses showed an increase of sexual embryo sacs, demonstrating an increased expression of sexuality compared to control plants. Plants of the cv. Tanganyika USDA did not demonstrate the ability to generate sexual embryo sacs under any conditions and is therefore classified as a fully apomictic cultivar. We found that this change in the prevalence of sexuality was correlated with genetic and epigenetic changes analyzed by MSAP and AFLPs profiles. Our results demonstrate that different stress conditions can alter the expression of sexual reproduction in facultative tetraploid apomictic cultivars and when the stress stops the reproductive mode shift back to the apomixis original level. These data together with previous observations allow us to generate a hypothetical model of the regulation of apomixis in weeping lovegrass in which the genetic/s region/s that condition apomixis, is/are affected by ploidy, and is/are subjected to epigenetic control.

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Section: Resultssupporting

confidence: 85%

Apomixis frequency under stress conditions in weeping lovegrass (Eragrostis curvula)

et al. 2017

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“…In addition to the previous data that apomixis is largely epigenetically controlled via pathways of DNA methylation in several apomictic plant systems (Garcia-Aguilar et al, 2010; Zappacosta et al, 2014; reviewed in Hand and Koltunow, 2014), and also by observing the fact that DNA methylation pathway members are deregulated in Boechera apomictic cell types (Schmidt et al, 2014) and generally at different developmental stages of Boechera apomicts (unpublished data), our data indicating control of MPS1 and ASY1 by DNA methylation highlights the importance of an epigenetic angle underlying meiotic deregulation. In this work, we have provided indirect evidence that global DNA methylation might possibly control the apomict-specific transcriptional regulation of stress and meiotic genes in the seedlings in a ploidy-independent manner, though this effect could be coupled to a rather marginal DNA-damaging effect of zebularine (Liu et al, 2015).…”

Section: Discussionsupporting

confidence: 78%

“…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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“…Similar values were obtained for maize and flax (Vicient 2010, González andDeyholos 2012), species with a different repetitive content, thus suggesting that TE transcriptional activity is maintained at low levels independently of the repetitive content in the species. The retrotransposon-related sequences content for libraries Ec02 and Ec04 has been previously estimated to be 0.7 and 1.5 % (an e-value ≤ e -8 ), respectively (Zappacosta et al 2014). Here, as expected, a less stringent condition (Table 2, an e-value ≤ e -3 ) leads to a higher number of retrotransposon-related sequences, resulting to be 1.21 and 1.77 %, respectively.…”

Section: Discussionsupporting

confidence: 52%

Repetitive sequences in Eragrostis curvula cDNA EST libraries obtained from genotypes with different ploidy

Romero¹,

Selva²,

Pessino³

et al. 2016

Biol. plant.

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Eragrostis curvula (Schrad) Nees (weeping lovegrass) represents important cultivated forage in semiarid regions, and the most useful cultivars are tetraploid and reproduce by pseudogamous diplosporous apomixis. We previously produced a series of genetically related E. curvula lines that provide a suitable system for the identification of gene(s) involved in diplosporous apomixis and ploidy, including a natural apomictic tetraploid (T), a diploid sexual line (D), and a tetraploid sexual plant (C). A collection of expressed sequence tags (ESTs) was generated from cDNA libraries obtained from panicles of the D, T, and C, and leaves of the T. The present study aimed to analyze the repetitive content of these four cDNA libraries and further identify and characterize transposable element (TE)-related ESTs. Repetitive sequences were identified through the interface RepeatMasker (RM) using the database Repbase Update and further classification of TEs was performed manually from the RM output. The different contribution of ESTs with identity to TEs among libraries was further evaluated, and such differences were validated through RT-qPCR. We found that the percentage of repetitive content in the leaf cDNA library was almost double than in inflorescence libraries, with retrotransposons contributing mostly in all libraries. The expression of TE-related ESTs was compared in cDNA samples extracted from D, T, and C leaves or inflorescences revealing that seven mRNAs containing MuDR-like DNA transposons, Gypsy-like, and Copia-like retrotransposons were differentially represented according to tissue, reproductive mode, or ploidy. The euploid series of Eragrostis curvula is a useful model to the study of epigenomic changes produced after changes in ploidy. The present work constitutes the first detailed report on repetitive sequences of Eragrostis curvula at the transcriptome level.

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Increased apomixis expression concurrent with genetic and epigenetic variation in a newly synthesized Eragrostis curvula polyploid

Cited by 26 publications

References 22 publications

Apomixis frequency under stress conditions in weeping lovegrass (Eragrostis curvula)

Apomixis frequency under stress conditions in weeping lovegrass (Eragrostis curvula)

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

Repetitive sequences in Eragrostis curvula cDNA EST libraries obtained from genotypes with different ploidy

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