Abstract
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.
Highlights
Sexual reproduction, otherwise known as amphimixis, is the most prevalent mode of reproduction found across phylogenetic boundaries of multi-cellular organisms over two billion years
Given the importance of Boechera genus in evolutionary point of view, with its intrinsic characteristics to give rise to a number of independent populations with apomictic mode of reproduction and its origin from a habitat with elevated environmental stress, the main questions, which we address in this work are: (1) If there are specific gene expression alterations at the seedling stage, i.e., way in advance of the apomeiotic germline transition as a preparatory mechanism for apomixis-specific gene expression program, which could likely be continued at the reproductive stage of development
A little over 3000 Boechera genes were found differentially expressed between Apo-1 and Sex-1 seedlings, accounting for about 15% of the total number of corresponding Arabidopsis loci qualified for differential analyses upon heterologous mapping
Summary
Otherwise known as amphimixis, is the most prevalent mode of reproduction found across phylogenetic boundaries of multi-cellular organisms over two billion years. Following the “restoration” view of Bernstein and co-workers that sex evolved for the repair of DNA lesions, a refined hypothesis proposes that meiosis has selectively been retained in evolution mainly for its role in repair of DNA damage caused by oxidative stress and reactive oxygen species (ROS), instead of its role in generation of recombination [summarized in (Horandl and Hadacek, 2013)] The latter view advocates that redox status between oxidized DNA and a key meiotic protein could be necessary for generating double-strand breaks (DSB), and could possibly be considered as a consequence of genome-wide epimutations caused by DNA or histone methylation changes that restrict deleterious transposable elements (de Massy, 2013; Zamudio et al, 2015).
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