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Regulation of Apomixis: Learning from Sexual Experience Daniel Rodriguez-Leal and Jean-Philippe Vielle-Calzada

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Regulation of Apomixis: Learning from Sexual Experience Daniel Rodriguez-Leal and Jean-Philippe Vielle-Calzada Available online at www.sciencedirect.com Regulation of apomixis: learning from sexual experience Daniel Rodriguez-Leal and Jean-Philippe Vielle-Calzada Apomixis is a natural form of asexual reproduction through develops autonomously into an embryo, by parthenogen- seeds that leads to viable offspring genetically identical to the esis (gametophytic apomixis). In the latter case, the mother plant. New evidence from sexual model species unreduced female gametophyte can be formed from an indicates that the regulation of female gametogenesis and seed aberrant meiotic cycle that prevents reduction and recom- formation is also directed by epigenetic mechanisms that are bination (diplospory) or from direct differentiation of crucial to control events that distinguish sexuality from somatic cells in the ovule (apospory). In most cases, apomixis, with important implications for our understanding of the formation of the endosperm is still dependent on the evolutionary forces that shape structural variation and fertilization of the central cell (pseudogamy), although diversity in plant reproduction. rare cases of autonomous development of the endosperm have been also reported [4]. Address Group of Reproductive Development and Apomixis, Laboratorio Nacional de Geno´ mica para la Biodiversidad, CINVESTAV, Irapuato, The introduction of apomixis into sexual crops has been Guanajuato, Mexico perceived as a revolutionary technology that could allow the perpetual self-production of improved hybrids, and Corresponding author: Vielle-Calzada, Jean-Philippe the genetic fixation of any desired heterozygous geno- ([email protected]) type. Apomixis was initially investigated by plant embryologists that characterized the cytological basis Current Opinion in Plant Biology 2012, 15:549–555 of apomictic reproduction in a wide group of species, This review comes from a themed issue on Cell signaling and gene describing its structural variants and prevalent develop- regulation mental pathways [4,5]. Their efforts lead those of a few Edited by Jerzy Paszkowski and Robert A. Martienssen visionary breeders that attempted its transfer by inter- For a complete overview see the Issue and the Editorial specific hybridization between important sexually Available online 20th September 2012 reproducing crops (maize, rice, pearl millet) and some of their apomictic wild relatives (Tripsacum dactyloides, 1369-5266/$ – see front matter, # 2012 Elsevier Ltd. All rights Elymus rectisetus,andPennisteum squamulatum,respect- reserved. ively [6]. Although the strategy proved unsuccessful http://dx.doi.org/10.1016/j.pbi.2012.09.005 from an applied perspective, resulting interspecific hybrids presently represent a unique resource for un- derstanding the genetic components that control apo- Introduction mixis. Over the past two decades, research has focused Although originally defined to include all known forms of on studying the genetic basis and molecular mechanisms vegetative propagation [1], apomixis has been restricted that regulate apomictic reproduction through either the to name a series of inherited developmental mechanisms elucidation of the genetic control of reproductive that give rise to clonal seeds by circumventing meiotically methods in natural apomicts in comparison to their derived chromosome reduction and fertilization of the sexual counterparts, or through the identification of egg cell in the ovule. In sexual flowering plants, a single gene function in sexual model species as a means to generative cell (a female archesporium or a megaspore elucidate the developmentalmechanismsthatrelateto mother cell) undergoes meiosis to produce four chromo- components of apomixis, such as the formation of unre- somally reduced cells (the megaspores). In the majority of duced female gametes, or the autonomous development sexual species, a single functional megaspore gives rise to of the embryo or endosperm [7,8]. the female gametophyte [2,3]. After significant cellular enlargement, the nucleus of the functional megaspore Recent results in Arabidopsis and maize have provided new usually undergoes three rounds of mitosis before giving evidence indicating that genetic basis of female gameto- rise to a gametophyte composed of seven cells: two genesis and seed formation are directed by epigenetic companion synergids, the egg cell, a binucleated central mechanisms that are crucial to control events that dis- cell and three antipodals (Figure 1). Double fertilization tinguish sexual from apomictic development. The discov- of both the egg and central cell is necessary to trigger ery of these epigenetic components is transforming our embryogenesis and endosperm development, respect- current view of the structural variation and diversity that ively. By contrast, apomictic plants can form embryos prevails at key steps of plant female gametogenesis, with directly from a somatic cell in the unfertilized profound implications for understanding the evolutionary ovule (adventitious embryony) or from chromosomally trends that shape innovations in reproductive development unreduced female gametophytes in which the egg cell and adaptation. www.sciencedirect.com Current Opinion in Plant Biology 2012, 15:549–555 550 Cell signaling and gene regulation Figure 1 CC An EC TTetradetrad SSyy Sexual mitosismitosis + development cecellularizationllularization 2NFG2NFG meiosismeiosis mitomitosissis + Diplospory cellularizatiocellularizationn mitosismitosis PEmbPEmb Al ectopicectopic gametophytesgametophytes mitosismitosis + Apospory cellularizationcellularization NEmbNEmb NEmbNEN ectopic embryosembryos somaticsomatic Adventitious embryogenesis embryony PT Current Opinion in Plant Biology Sexual and apomictic development in flowering plants. During sexual development, a single cell undergoes meiosis to produce a tetrad of chromosomally reduced cells (the megaspores); in most cases a single functional megaspore gives rise to the female gametophyte composed of two synergids (Sy; orange), the egg cell (EC; blue), a binucleated central cell (CC; pink) and three antipodals (brown). By contrast, apomictic plants can form embryos directly from a somatic cell in the developing ovule (nucellar embryos, NEmb; adventitious embryony) or from chromosomally unreduced female gametophytes in which the egg cell develops autonomously into an embryo, by parthenogenesis (PEmb; gametophytic apomixis). In the latter case, the unreduced female gametophyte can be formed from an aberrant meiotic cycle that prevents reduction and recombination (diplospory) or from direct differentiation of somatic cells in the ovule (apospory). Additional legend: Tetrad, tetrad of haploid nuclei; 2NFG, 2-nuclear unreduced female gametophyte; AI, aposporous initial cell. Genetic control of apomixis not been investigated, segregating populations in several Apomixis is genetically controlled, but the basis of its apomictic grasses that retain a variable frequency of inheritance remains often contradictory and elusive [6]. residual sexuality show that the inheritance of unreduced Genetic analysis is complicated by the absence of sexually female gametophyte formation (through either diplospory functional female gametes; as a consequence, apomictic or apospory) is simple. In most species under study, the genotypes can only be used as male parents and cannot be basic components of apomixis can be explained by one self-fertilized to generate segregating populations. or two dominant loci that control unreduced gamete Whereas the inheritance of adventitious embryony has formation and parthenogenesis, respectively; however, Current Opinion in Plant Biology 2012, 15:549–555 www.sciencedirect.com Regulation of apomixis: learning from sexual experience Rodriguez-Leal and Vielle-Calzada 551 polyploidy, segregation distortion [9,10], suppressed recombinationally suppressed, and rich in long terminal recombination [6], epistatic interactions [6], naturally repeat transposable elements [20]. active modifiers [8], and environmental effects [4], com- plicate their genetic analysis. To this date, no genes Apomixis and the epigenetic regulation of associated with these loci have been demonstrated to sexual development control components of natural apomixis. In Hieracium The initiation of apomixis invariably occurs during early praeltum, a member of the subgenus Pilosella, deletion ovule ontogeny; sexual and apomictic development can analysis showed that aposporous apomixis is controlled coexist within the same ovule, or within different ovules of by the LOSS OF APOMEIOSIS (LOA) and LOSS OF a same individual, suggesting that apomixis could have PARTHENOGENESIS (LOP) loci. Whereas LOA is originated as a modified form of sexual reproduction that required for aposporous cell differentiation and suppres- has undergone deregulation of key developmental steps sion of all sexually derived megaspores, the gametophytic during gametogenesis [8]. Because mechanisms such as activity of LOP is necessary for autonomous development diplospory are directly dependent on the abnormal division of embryo and endosperm [11,12]. Deletion of LOA or of a meiotic precursor, mutations affecting meiosis are LOP results in reversion to sexuality, indicating that apo- particularly interesting for understanding crucial aspects mixis is imposed over a default sexual pathway that is of apomixis [2]. The combination of meiotic mutants that interrupted by any of these unrelated loci. Intriguingly, can generate non-reduced female gametophytes with a LOA function requires the initiation of megaspore
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