Apospory and Diplospory in Diploid Boechera (Brassicaceae) May Facilitate Speciation by Recombination-Driven Apomixis-to-Sex Reversals

Abstract

Apomixis (asexual seed formation) in angiosperms occurs either sporophytically, through adventitious embryony, or gametophytically, where an unreduced female gametophyte (embryo sac) forms and produces an unreduced egg that develops into an embryo parthenogenetically. Multiple types of gametophytic apomixis occur, and these are differentiated based on where and when the unreduced gametophyte forms, a process referred to as apomeiosis. Apomeiotic gametophytes form directly from ameiotic megasporocytes, as in Antennaria-type diplospory, from unreduced spores derived from 1st division meiotic restitutions, as in Taraxacum-type diplospory, or from cells of the ovule wall, as in Hieracium-type apospory. Multiple types of apomeiosis occasionally occur in the same plant, which suggests that the different types occur in response to temporal and/or spatial shifts in termination of sexual processes and onset timing of apomeiosis processes. To better understand the origins and evolutionary implications of apomixis in Boechera (Brassicaceae), we determined apomeiosis type for 64 accessions representing 44 taxonomic units. Plants expressing apospory and diplospory were equally common, and these generally produced reduced and unreduced pollen, respectively. Apospory and diplospory occurred simultaneously in individual plants of seven taxa. In Boechera , apomixis perpetuates otherwise sterile or semisterile interspecific hybrids (allodiploids) through multiple generations. Accordingly, ample time, in these multigenerational clones, is available for rare meioses to produce haploid, intergenomically recombined male and female gametes. The fusion of such gametes could then produce segmentally autoploidized progeny. If sex re-emerges among such progeny, then new and genomically unique sexual species could evolve. Herein, we present evidence that such apomixis-facilitated speciation is occurring in Boechera , and we hypothesize that it might also be occurring in facultatively apomictic allodiploids of other angiospermous taxa.

Controlling Apomixis: Shared Features and Distinct Characteristics of Gene Regulation

“…From studies of the Hieracium praeltum AIC no expression of 14 selected meiotic genes has previously been observed, consistent with the cellular fate destined to mitosis [108]. The lack of consistency likely relates to the developmental flexibility during germline formation: As apospory and diplospory both occur in Boechera at different frequencies [33], this also results in different frequencies of the determination and meiosis of the sexual MMC in addition to the AIC. Therefore, future studies focusing on proteins at cellular level will be required to disentangle their involvement in regulation of apomeiosis.…”

“…However, a consistent differential gene expression in reproductive nucellus tissues prior to apo(meiosis) could not be identified in different sexual and apomictic Boechera accessions [80,103]. Given the broad developmental flexibility during apomictic germline formation in Boechera [33], a role in regulation of developmental processes relevant for apomixis cannot be ruled out by this finding. Apart from the identification of MEM, further studies provide evidence of RNA helicases to be likely involved in regulation of apomictic development, as in Brachiaria brizantha and in Hypericum perforatum, BrizHELIC and a homologue of MATERNAL EFFECT EMBRYO ARREST29, respectively, are differentially expressed in tissues of sexual and apomictic plants [10,128].…”

“…Furthermore, in many systems studied to date, apomixis is largely facultative, setting the basis for a broad developmental flexibility. Together with the potential occurrence of reversions from apomictic reproduction to sexuality this allows to purge deleterious mutations from the genome [1,25,[31][32][33].…”

“…In aposporous Hieracium subgenus Pilosella, for example, the specification of the sexual MMC is preceding the formation of the aposporous initial cell, while the apomictic reproductive lineage subsequently suppresses further development of the sexual lineage [22]. Nevertheless, certain developmental flexibility and the formation of two gametophytes in the same ovule occurs in Hieracium praeltum and also in apomictic Boechera, providing the opportunity to reinforce the facultative nature of apomixis [33,34]. Also the occurrence of both, diplospory and apospory, demonstrates a striking flexibility of developmental concepts in Boechera [33].…”

“…Nevertheless, certain developmental flexibility and the formation of two gametophytes in the same ovule occurs in Hieracium praeltum and also in apomictic Boechera, providing the opportunity to reinforce the facultative nature of apomixis [33,34]. Also the occurrence of both, diplospory and apospory, demonstrates a striking flexibility of developmental concepts in Boechera [33]. Increasing attention is recently also given to the question, whether and how environmental factors are modulating the regulation of the reproductive programs or if they might even be sufficient to determine the reproductive mode.…”