Apomicts that produce unreduced parthenogenetic eggs are generally polyploid and occur in at least 33 of 460 families of angiosperms. Embryo sacs of these apomicts form precociously from ameiotic megaspore mother cells (diplospory) or adjacent somatic cells (apospory). Polysporic species (bisporic and tetrasporic) are sexual and occur in at least 88 families. Their embryo sacs also form precociously, but only non-critical portions of meiosis are affected. It is hypothesized that (i) the partial to complete replacement of meiosis by embryo sac formation in apomictic and polysporic species results from asynchronously-expressed duplicate genes that control female development, (ii) duplicate genes result from polyploidy or paleopolyploidy (diploidized polyploidy with chromatin from multiple genomes), (iii) apomixis results from competition between nearly complete sets of asynchronously-expressed duplicate genes, and (iv) polyspory and polyembryony result from competition between incomplete sets of asynchronously-expressed duplicate genes. Phylogenetic and genomic studies were conducted to evaluate this hypothesis. Apomictic, polysporic, and polyembryonic species tended to occur together in cosmopolitan families in which temporal variation in female development is expected, apomicts were generally polyploid with few chromosomes per genome (it = 9.6 0.4 SE), and polysporic and polyembryonic species were paleopolyploid with many chromosomes per genome (a = 15.7 f 0.6 and 13.2 f 0.4, respectively). These findings support the proposed duplicate-gene asynchrony hypothesis and further suggest asexual reproduction in apomicts preserves primary genomes, sexual reproduction in polysporic and polyembryonic polyploids accelerates paleopolyploidization, and paleopolyploidization may sometimes eliminate gene duplications required for apomixis while retaining duplications required for polyspory or polyembryony. Hence, apomixis, with its long-term reproductive stability, may occasionally serve as an evolutionary springboard in the evolution of normal and developmentally-novel paleopolyploid sexual species and genera. 0 1997 The Linnean Sorirty of Inndon ADDITIONAL KEY WORDS:-apospory -diplospory -embryology -evolutionparthenogenesis ~ phylogeny ~ polyploidy -pseudogamy.
Apomixis in angiosperms is asexual reproduction from seed. Its importance to angiospermous evolution and biodiversity has been difficult to assess mainly because of insufficient taxonomic documentation. Thus, we assembled literature reporting apomixis occurrences among angiosperms and transferred the information to an internet database (http://www.apomixis.uni-goettingen.de). We then searched for correlations between apomixis occurrences and well-established measures of taxonomic diversity and biogeography. Apomixis was found to be taxonomically widespread with no clear tendency to specific groups and to occur with sexuality at all taxonomic levels. Adventitious embryony was the most frequent form (148 genera) followed by apospory (110) and diplospory (68). All three forms are phylogenetically scattered, but this scattering is strongly associated with measures of biodiversity. Across apomictic-containing orders and families, numbers of apomict-containing genera were positively correlated with total numbers of genera. In general, apomict-containing orders, families, and subfamilies of Asteraceae, Poaceae, and Orchidaceae were larger, i.e., they possessed more families or genera, than non-apomict-containing orders, families or subfamilies. Furthermore, many apomict-containing genera were found to be highly cosmopolitan. In this respect, 62% occupy multiple geographic zones. Numbers of genera containing sporophytic or gametophytic apomicts decreased from the tropics to the arctic, a trend that parallels general biodiversity. While angiosperms appear to be predisposed to shift from sex to apomixis, there is also evidence of reversions to sexuality. Such reversions may result from genetic or epigenetic destabilization events accompanying hybridization, polyploidy, or other cytogenetic alterations. Because of increased within-plant genetic and genomic heterogeneity, range expansions and diversifications at the species and genus levels may occur more rapidly upon reversion to sexuality. The significantly-enriched representations of apomicts among highly diverse and geographically-extensive taxa, from genera to orders, support this conclusion.
In angiosperms, there are two pathways of reproduction through seeds: sexual, or amphimictic, and asexual, or apomictic. The essential feature of apomixis is that an embryo in an ovule is formed autonomously. It may form from a cell of the nucellus or integuments in an otherwise sexual ovule, a process referred to as adventitious embryony. Alternatively, the embryo may form by parthenogenesis from an unreduced egg that forms in an unreduced embryo sac. The latter may form from an ameiotic megasporocyte, in which case it is referred to as diplospory, or from a cell of the nucellus or integument, in which case it is referred to as apospory. Progeny of apomictic plants are generally identical to the mother plant. Apomixis has been seen over the years as either a gain-or loss-of-function over sexuality, implying that the latter is the default condition. Here, we consider an additional point of view, that apomixis may be anciently polyphenic with sex and that both reproductive phenisms involve anciently canalized components of complex molecular processes. This polyphenism viewpoint suggests that apomixis fails to occur in obligately sexual eukaryotes because genetic or epigenetic modifications have silenced the primitive sex apomixis switch and/or disrupted molecular capacities for apomixis. In eukaryotes where sex and apomixis are clearly polyphenic, apomixis exponentially drives clonal fecundity during reproductively favorable conditions, while stress induces sex for stresstolerant spore or egg formation. The latter often guarantees species survival during environmentally harsh seasons.
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