A current perspective on apomixis in ferns

Abstract

This review provides a synopsis of apogamous reproduction in ferns and highlights important progress made in the study of fern apomixis over the past decade. First, a summary of the apomictic fern life cycle is provided, distinguishing between two pathways to diploid spore production that have been documented in apomictic ferns (premeiotic endomitosis and meiotic first division restitution) and briefly discussing the evolutionary implications of each. Next, recent trends in fern apomixis research are highlighted, exposing a shift in focus from the observation and characterization of apomixis in ferns to more integrated studies of the evolutionary and ecological implications of this reproductive mode. Peer-reviewed contributions from the past decade are then summarized, spanning the identification of new apomictic lineages through to the developmental, phylogenetic, and population genetic insights that have been made in studies of fern apomixis during that time. Gaps in our understanding of fern apomixis are also discussed, including the extent and implications of recombinant apomixis in ferns, the possible reversibility of reproductive mode (from apomictic to sexual) in ferns, and the genomic causes and consequences of apomixis in seed A u t h o r M a n u s c r i p t A u t h o r M a n u s c r i p t A u t h o r M a n u s c r i p tGrusz, 2 of 23 free vascular plants. Finally, future directions for fern apomixis research are discussed in the context of modern technological advances and recent insights from studies of apomixis in other groups.Keywords: apogamy, evolution of sex, meiosis, pteridophytes.A u t h o r M a n u s c r i p t A u t h o r M a n u s c r i p t A u t h o r M a n u s c r i p t Grusz, 3 of 23 "…apomixis is an escape from sterility, but it is an escape into a blind alley of evolution…" -Darlington, 1939A renaissance is underway in fern biology, propelled, in part, by technological advances being embraced by a growing research community. In particular, modern, cost-effective tools are enabling new inquiries into the unique fern life cycle, which alternates between independent, free-living sporophyte and gametophyte generations (Haufler et al., 2016). Among the many aspects of fern reproduction that are being examined in light of new approaches-and an improved understanding of fern evolution as a whole-is their propensity for apogamous reproduction (i.e., apomixis). This form of asexual reproduction (by spore or seed) is more common in ferns than in any other group of vascular plants. Nearly 10% of the ferns for which reproductive mode has been determined exhibit apomixis (Walker, 1985; Liu et al., 2012), compared to less than 1% in flowering plants (Bicknell & Koltunow, 2004; Becks & Alavi, 2015). Given that data on reproductive mode is lacking for the vast majority of ferns, this relative contribution of apomicts to fern diversity may well be an underestimate (Liu et al., 2012). The elevated frequency and distinctive meiotic characteristics of apomixis in ferns, which are elaborated upon bel...

A Reappraisal of the Evolutionary and Developmental Pathway of Apomixis and Its Genetic Control in Angiosperms

“…Each of these two alternative spore-generating pathways yields chromosomally unreduced spores (i.e., diplospores) which then germinate. Within leptosporangiate ferns, nearly half of the families contain one or more apomictic taxa [26]. Interestingly, the frequency of apomixis seems significantly correlated with species diversity, but any significant relationship was found between apomixis and diversification rates [27].…”

“…Apomixis has been detected in ferns (where this is better referred as to apogamy, i.e., development of a sporophyte from a gametophyte without fertilization), is rare in gymnosperms and very common in angiosperms [25]. Apomictic fern lineages have been documented only in recent years [26], distinguishing between two pathways to diploid spore production (premeiotic endomitosis, more common, and meiotic first division restitution, less frequently observed). Each of these two alternative spore-generating pathways yields chromosomally unreduced spores (i.e., diplospores) which then germinate.…”

Molecular phylogeny and divergence times of Onosma (Boraginaceae s.s.) based on nrDNA ITS and plastid rpl32‐trnL(UAG) and trnH–psbA sequences

“…ex Boiss. Several biological factors have been proposed to cause incomplete concerted evolution, such as apomixis, long generation times, hybridization and polyploidization (Suh et al 1993, Sang et al 1995, Campbell et al 1997, Grimm and Denk 2008, Hribova et al 2011, Grusz 2016, Shang et al 2016, Xu et al 2017. Onosma species are biennial and perennial herbs, some with woody stock and rhizome, and no apomictic taxa have been reported (Riedl 1967, Kolarcik et al 2014.…”

Genetic and genomic aspects of hybridization in ferns

“…Most apomictic ferns undergo an endomitosis immediately preceding meiosis, resulting in the production of unreduced spores with the same ploidy and, presumably, the same genotype as their parent sporophyte. New sporophytes are produced apogamously by forming directly from gametophyte somatic cells (Döpp, ; Manton, ; see Grusz, for a detailed discussion of apomixis and apogamy in ferns).…”