Abstract:The co-occurrence of apomixis (asexual reproduction) and polyploidy in plants has been the subject of debate in regard to the origin and evolution of asexuality. In recent years, polyploidy has been postulated as a maintenance and stabilization factor rather than as a source of apomixis origin. It is assumed polyploidy facilitates the compensation for mutation accumulation, and hence, the rare occurrence of diploid apomixis indirectly supports this finding. Nevertheless, diploid apomicts exist and are successf… Show more
“…Several studies have raised the possibility that alternative reproductive pathways, such as tetraspory or asexual reproduction through seeds (apomixis), evolved as a response to hybridization, genomic collisions, or unstable climatic environment (Carman, 1997;Voigt-Zielinski et al, 2012;Lovell et al, 2013;Hojsgaard et al, 2014). Segregating F2 populations of ecotypic crosses showed a continuous distribution of the frequency of ectopic configurations, suggesting that the genetic factors influencing the phenotype are quantitative and conserved among different ecotypes.…”
In angiosperms, the transition to the female gametophytic phase relies on the specification of premeiotic gamete precursors from sporophytic cells in the ovule. In Arabidopsis thaliana, a single diploid cell is specified as the premeiotic female gamete precursor. Here, we show that ecotypes of Arabidopsis exhibit differences in megasporogenesis leading to phenotypes reminiscent of defects in dominant mutations that epigenetically affect the specification of female gamete precursors. Intraspecific hybridization and polyploidy exacerbate these defects, which segregate quantitatively in F2 populations derived from ecotypic hybrids, suggesting that multiple loci control cell specification at the onset of female meiosis. This variation in cell differentiation is influenced by the activity of ARGONAUTE9 (AGO9) and RNA-DEPENDENT RNA POLYMERASE6 (RDR6), two genes involved in epigenetic silencing that control the specification of female gamete precursors. The pattern of transcriptional regulation and localization of AGO9 varies among ecotypes, and abnormal gamete precursors in ovules defective for RDR6 share identity with ectopic gamete precursors found in selected ecotypes. Our results indicate that differences in the epigenetic control of cell specification lead to natural phenotypic variation during megasporogenesis. We propose that this mechanism could be implicated in the emergence and evolution of the reproductive alternatives that prevail in flowering plants.
“…Several studies have raised the possibility that alternative reproductive pathways, such as tetraspory or asexual reproduction through seeds (apomixis), evolved as a response to hybridization, genomic collisions, or unstable climatic environment (Carman, 1997;Voigt-Zielinski et al, 2012;Lovell et al, 2013;Hojsgaard et al, 2014). Segregating F2 populations of ecotypic crosses showed a continuous distribution of the frequency of ectopic configurations, suggesting that the genetic factors influencing the phenotype are quantitative and conserved among different ecotypes.…”
In angiosperms, the transition to the female gametophytic phase relies on the specification of premeiotic gamete precursors from sporophytic cells in the ovule. In Arabidopsis thaliana, a single diploid cell is specified as the premeiotic female gamete precursor. Here, we show that ecotypes of Arabidopsis exhibit differences in megasporogenesis leading to phenotypes reminiscent of defects in dominant mutations that epigenetically affect the specification of female gamete precursors. Intraspecific hybridization and polyploidy exacerbate these defects, which segregate quantitatively in F2 populations derived from ecotypic hybrids, suggesting that multiple loci control cell specification at the onset of female meiosis. This variation in cell differentiation is influenced by the activity of ARGONAUTE9 (AGO9) and RNA-DEPENDENT RNA POLYMERASE6 (RDR6), two genes involved in epigenetic silencing that control the specification of female gamete precursors. The pattern of transcriptional regulation and localization of AGO9 varies among ecotypes, and abnormal gamete precursors in ovules defective for RDR6 share identity with ectopic gamete precursors found in selected ecotypes. Our results indicate that differences in the epigenetic control of cell specification lead to natural phenotypic variation during megasporogenesis. We propose that this mechanism could be implicated in the emergence and evolution of the reproductive alternatives that prevail in flowering plants.
“…7D). High variability in pollen morphology and unreduced pollen formation, in addition to tolerance to deviations from the sexual endosperm balance number, have been described for some Boechera taxa (Böcher, 1951(Böcher, , 1954Voigt et al, 2007;Aliyu et al, 2010;Voigt-Zielinski et al, 2012). Despite this variability, castration experiments (Böcher, 1951) and extensive flow cytometric analyses of seeds (Aliyu et al, 2010) strongly support selection pressure for the maintenance of unreduced pollen development to fulfill endosperm balance requirements in diploid apomicts.…”
Section: Bspupg2 Arose Via Genome Rearrangementsmentioning
confidence: 99%
“…Besides the formation of unreduced female gametes, apomictic Boechera spp. also produce unreduced pollen, as demonstrated by the fact that diploids and triploids produce seeds almost exclusively with hexaploid (6C = (Voigt et al, 2007;Aliyu et al, 2010;Voigt-Zielinski et al, 2012). Hence, strong selection pressure to maintain a balanced two maternal-to-one paternal genome ratio (i.e.…”
“…Several apomictic Boechera (diploid or polyploid) had been classified under B. holboellii clade and/or several others previously belong to this clade, e.g., B. divaricarpa (used in this study) had been reclassified into “trashcan” hybrids involving sexuals like B. stricta and B. sparsifolia (Rushworth et al, 2011). Diploids and polyploids (e.g., triploids) can be tractable within these “ holboeleii and hybrid” clades (Naumova et al, 2001; Aliyu et al, 2010; Voigt-Zielinski et al, 2012), and current studies in several labs focus on the genome evolution of the identified apomictic diploids and their sexual parents by genome sequencing. Although exhaustive comparative studies have not yet been conducted, Roy concluded that B. holboellii apomictic populations are likely polyphyletic with substantial allelic variation thus greater fixed heterozygosity than what were observed for B. gunnisoniana , a stand-alone monophyletic apomictic triploid (Roy, 1995).…”
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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