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

Abstract

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.

Ploidy-Dependent Effects of Light Stress on the Mode of Reproduction in the Ranunculus auricomus Complex (Ranunculaceae)

“…Results support the hypothesis that the oxidative lesions might mobilize the meiotic DNA repair system in the megaspore mother cell and trigger meiosis and megasporogenesis (Hörandl and Hadacek, 2013). This stimulus might increase the proportion of functional megaspores as a cellular survival strategy for the germline (Rodrigo et al, 2017), as shown remarkably in our diploids. Differential genetic stress regulation of sexual and apomictic plants was also observed in seedlings of Boechera, and may be important for the bypass of the meiotic pathway (Shah et al, 2016).…”

“…The high variability of the proportions of sexual ovules among our genetically identical polyploids supports the findings of epigenetic and transcriptional control mechanisms as the background for the phenotypic expression of apospory (Grimanelli, 2012;Schmidt et al, 2014). Our result supports the hypothesis that phenotypic features of apomixis in flowering plants are strongly affected by polyploidy (Delgado et al, 2016;Kaushal et al, 2018) and subjected to epigenetic control (Rodrigo et al, 2017).…”

“…Environmental stress plays a role as an inhibition factor under an epigenetic mechanism that disturbs or interrupts the silencing signal of apomictic-conditioning (Rodrigo et al, 2017). At least in diploid Ranunculus, the treatment might strengthen a signal transduction pathway that promotes switching from apomeiosis to meiosis, as demonstrated in facultative Boechera after drought stress (Mateo de Arias, 2015;Gao, 2018;Carman et al, 2019).…”

“…Alternation of frequencies of asexual vs. sexual reproduction was observed under abiotic stress conditions, e.g. temperature, drought stress, salt stress, and photoperiod in many different genera (Evans and Knox, 1969;Saran and de Wet, 1976;Quarin, 1986;Gounaris et al, 1991;Klatt et al, 2016;Rodrigo et al, 2017;Klatt et al, 2018). Such a condition-dependent sex is also known from other asexual eukaryotes (Ram and Hadany, 2016).…”

Apomixis Technology: Separating the Wheat from the Chaff

“…Attempts to identify components of apomixis by transcriptional profiling of reproductive organs using Differential Display PCR (DD-PCR), SuperSAGE (serial analysis of gene expression), and high-throughput sequencing on microdissected ovules revealed 1) differentially expressed genes in reproductive tissues of apomictic and sexual relatives from different plant systems (e.g., Pennisetum, [69,70]; Brachiaria, [71,72]; Panicum, [73,74]; Poa, [75], Eragrostis, [76][77][78]; Paspalum, [42,64,[79][80][81]; Hieracium, [82,83]; Hypericum [84,85]) and 2) an overall shift in gene regulation at the MMC stage and a global heterochronic gene expression between the sexual and apomeiotic ovules (e.g., Boechera, [86][87][88][89]; Paspalum [79,90,91]; Pennisetum, [92]; Hieracium, [83,93,94]; Hypericum [85,95]; Ranunculus [96,97]). Such wide-ranging de-regulation on gene expression levels between sexual and apomictic ovules affect genes encoding varied biological functions (GO classes) and regulatory pathways, including key genes of the sexual pathway, RNA-directed DNA methylation and transcription regulation, hormonal signaling, and cell cycle control (see details in the next section).…”