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.

Controlling Apomixis: Shared Features and Distinct Characteristics of Gene Regulation

“…Apart from the occurrence of apomixis in the genera Draba, Erysimum, and Parrya, in Brassicaceae apomixis is only represented in Boechera and the related genus Phounicaulis [23]. The absence of apomixis in Amborella as basal sister clade of angiosperms might rather indicate that it is derived, however, this alone cannot be taken as sufficient indication [6]. Moreover, the distinctiveness of the different types of apomixis like sporophytic and gametophytic apomixis, but also of apospory and diplospory, suggests that they represent non-homologous mechanisms that arose independently [24].…”

“…While polyploidy has long been regarded as a precondition for apomixis, the identification of diploid apomicts, e.g., in the genus Boechera has changed this view [27]. In Boechera, apomixis arose recurrently by hybridization and intra-specific crosses, and also outside Boechera evidence for hybrid origin is given for an increasing number of apomictic taxa [6,28].…”

“…As this would allow the fixation of advantageous and complex genotypes, it has an outstanding potential for crop seed production. However, although apomixis is phylogenetically distributed in all major groups of angiosperms and occurs in more than 400 species [1][2][3][4][5][6][7], it is largely absent in major crop species. Therefore, engineering of apomixis for harnessing in agriculture is a longstanding aim [8][9][10].…”

“…It is commonly accepted that apomixis derived several times independently and that distinct types of apomixis are represented in higher plants [6,15]: First, sporophytic apomixis is distinguished from gametophytic apomixis, as the apomictic embryos either originate directly from sporophytic cells or from the egg cell formed in the gametophyte, respectively. Sporophytic apomixis, also known as adventitious embryony, is widespread throughout the plant kingdom and is particularly frequent e.g., in Citrus and Orchidaceae [6,16]. In sporophytic apomixis, one or more adventitious embryos derive from sporophytic cells of the nucellus, which is surrounding the sexually formed gametophyte ( Figure 2B).…”

“…In sporophytic apomixis, one or more adventitious embryos derive from sporophytic cells of the nucellus, which is surrounding the sexually formed gametophyte ( Figure 2B). Unlike sexual reproduction, which usually leads to the formation of a single embryo per seed, adventitious embryony is frequently marked by polyembryony [6]. Both the sexually derived embryo and its asexual siblings compete for resources of the endosperm ( Figure 2B).…”