The Rise of Apomixis in Natural Plant Populations

Abstract

Apomixis, the asexual reproduction via seed, has many potential applications for plant breeding by maintaining desirable genotypes over generations. Since most major crops do not express natural apomixis, it is useful to understand the origin and maintenance of apomixis in natural plant systems. Here, we review the state of knowledge on origin, establishment and maintenance of natural apomixis. Many studies suggest that hybridization, either on diploid or polyploid cytotypes, is a major trigger for the formation of unreduced female gametophytes, which represents the first step toward apomixis, and must be combined to parthenogenesis, the development of an unfertilized egg cell. Nevertheless, fertilization of endosperm is still needed for most apomictic plants. Coupling of these three steps appears to be a major constraint for shifts to natural apomixis. Adventitious embryony is another developmental pathway toward apomixis. Establishment of a newly arisen apomictic lineage is often fostered by side-effects of polyploidy. Polyploidy creates an immediate reproductive barrier against the diploid parental and progenitor populations; it can cause a breakdown of genetic self-incompatibility (SI) systems which is needed to establish self-fertility of pseudogamous apomictic lineages; and finally, polyploidy could indirectly help to establish an apomictic cytotype in a novel ecological niche by increasing adaptive potentials of the plants. This step may be followed by a phase of diversification and range expansion, mostly described as geographical parthenogenesis. The utilization of apomixis in crops must consider the potential risks of pollen transfer and introgression into sexual crop fields, which might be overcome by using pollen-sterile or cleistogamous variants. Another risk is the escape into natural vegetation and potential invasiveness of apomictic plants which needs careful management and consideration of ecological conditions.

Keywords: apomictic crops; grass cultivars; polyploidy; reproductive assurance; sexuality; speciation; triploid bridge.

FIGURE 1

Main developmental pathways of natural apomixis in flowering plants (adapted from Hörandl, 2018). Meiotic developmental pathways (c,e) and biparental seed development (d,e) (green gametophytes, embryo, and endosperm tissues); apomictic developmental pathways (a,b,d) and maternal seed development (a–c,e) (yellow gametophytes and endosperm tissue, red egg-cell and embryo tissue); blue seed embryo is derived from a fertilized unreduced egg-cell. MMC, megaspore mother cell; MC, megaspore; NC, nucellus cell; B_III hybrid, offspring produced by fertilization of unreduced egg cells. Size of nuclei corresponds to relative ploidy level.

FIGURE 2

Hypothetical scheme of evolutionary pathways to apomixis in natural populations. (a) starting population; (b) emergence of apomixis elements and rise of first polyploid plants; (c) stabilization of functional, pollen-independent apomixis in triploids; (d) formation of even-ploid apomictic, pseudogamous polyploids; (e) formation of even polyploids and reversal to sexual reproduction.