On the origin and evolution of apomixis in Boechera

Abstract

The genetic mechanisms causing seed development by gametophytic apomixis in plants are predominantly unknown. As apomixis is consistently associated with hybridity and polyploidy, these confounding factors may either A) be the underlying mechanism for the expression of apomixis, or B) obscure the genetic factors which cause apomixis. To distinguish between these hypotheses, we analyzed the population genetic patterns of diploid and triploid apomictic lineages and their sexual progenitors in the genus Boechera (Brassicaceae). We find that while triploid apomixis is associated with hybridization, the majority of diploid apomictic lineages are likely the product of intra-specific crosses. We then show that these diploid apomicts are more likely to sire triploid apomictic lineages than conspecific sexuals. Combined with flow cytometric seed screen phenotyping for male and female components of apomixis, our analyses demonstrate that hybridization is an indirect correlate of apomixis in Boechera. KeywordsBoechera; Apomixis; Apomeiosis; Hybridization; Polyploidy Sexual, outcrossing reproduction is the ancestral state of embryo development in flowering plants (Karron et al. 2012). This breeding system has generated much of the biodiversity on earth and provides species with the potential to adapt to changing conditions, thus improving the chance for long term survival. Despite these advantages, many groups of plants have independently evolved asexual methods to produce seed (van Dijk and Vijverberg 2005;Carman 1997). Among these mechanisms, gametophytic apomixis (hereon "apomixis") is one of the most common (Hörandl and Hojsgaard 2012 requires the coordination of several independent phenotypes including the formation of an unreduced embryo sac (female apomeiosis) and embryo development from an unfertilized and unreduced egg cell (parthenogenesis). Other traits, including the production of unreduced pollen (male apomeiosis) and the development of functional endosperm (e.g. pseudogamy) are typical of apomictic genotypes (Mogie 1992;Bicknell and Koltunow 2004). Considering that apomixis evolves from sexuality, the expression of any one of these traits alone would be deleterious. For example, female apomeiosis without parthenogenesis would lead to ploidy increases after each generation (although see Van Dijk & Vijverberg, 2005). The evolutionary mechanism causing the simultaneous establishment of these traits is the foremost debate in the apomixis literature.Many authors have suggested that the genome-wide affects of hybridization and polyploidy may induce apomixis (Carman 1997;Comai et al. 2003;Madlung et al. 2002;Sharbel et al. 2010; Wang et al. 2004) as evidenced by the nearly uniform pattern of hybridity and polyploidy in apomictic lineages (Pongratz et al. 1997;Bicknell and Koltunow 2004;Mogie 1986; Asker and Jerling 1992;Nelson-Jones et al. 2002). However, this correlation may be indirect: since apomictic lineages are expected to accumulate mutations through time (Hopf et al. 1988;Kondrashov 1985), hybridity ...

Hybrid apomicts trapped in the ecological niches of their sexual ancestors

“…Introgression of apomixis alleles from apomictic diploids into different diploid sexual genotypes (43,48) may have facilitated the enormous genetic diversity characteristic of apomictic Boechera (Table S4) (see also ref. 43).…”

“…Introgression of apomixis alleles from apomictic diploids into different diploid sexual genotypes (43,48) may have facilitated the enormous genetic diversity characteristic of apomictic Boechera (Table S4) (see also ref. 43). Our data demonstrate that apomictic Boechera for the most part drift into new niches by virtue of ploidy variation although evidence for occasional ploidy-independent niche drift was also found (e.g., Fig.…”

Natural Variation in Epigenetic Pathways Affects the Specification of Female Gamete Precursors in Arabidopsis

“…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.…”

Copy Number Variation in Transcriptionally Active Regions of Sexual and Apomictic Boechera Demonstrates Independently Derived Apomictic Lineages

“…The multiple-origin hypothesis in no way implies the de novo convergent and repetitive evolution of apomixis factors via mutational processes; rather it implies either (1) convergent patterns of apomixis-specific gene expression (i.e., deregulation) triggered by frequent hybridization between different sexual lineages , or (2) the spread of singly derived apomixis factors via sex (e.g., pollen) into different sexual backgrounds (Lovell et al, 2013). Although strong evidence exists for multiple origins of apomictic lineages via hybridization between sexual Boechera species (Koch et al 2003;Dobeš et al 2004aDobeš et al , 2004bKantama et al 2007;Beck et al 2012), so far no attempt has been made to understand the number of origins or the relative evolutionary ages of these lineages.…”