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Developmental Genetics of Gametophytic Apomixis

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Developmental Genetics of Gametophytic Apomixis 3 TßENDSin Genetics vo1.17 No.10 October 2001 597 Developmental genetics of gametophytic apomixis OlivierÍ Leblanc, Enrico Perotti and Ueli Grossniklaus Some higher plants reproduce asexually by apomixis, a naturalway of cloning revealed an intriguing paradox: although the through seeds. Apomictic plants produce progeny that are an exact genetic developmental mechanisms underlying apomixis replica ofthe mother plant.The replication is achieved through changes in the are complex, most genetic analyses suggest that female reproductive pathway such thatfemale gametes develop without meiosis apomixis is inherited as a simple mendelian trait, and embryos develop without fertilization. Although apomixis is a complex and results from one or a few mutations that affect developmentalprocess, genetic evidence suggests that it might be inheritedas a the normal course of sexual reproductiongc. simple mendeliantrait -a paradox that could be explained by recent data derived The growing popularity of apomixis research has from apomictic species and model sexual organisms. The data suggest that brought developmental biologists into the field. Their apomixis might rely more on a global deregulation of sexual reproductive perception is that apomixis is not a true novelty in developmentthan on truly newfunctions,and molecular mechanismsfor such a plant development, but rather has evolved through global deregulation can be proposed. This new understanding has direct the rearrangement of the subprograms that consequences for the engineering of apomixis in sexual crop species. an constitute a normal sexual pathwaqr'~~. application that could have an immense impact on agriculture. Understanding apomixis will probably depend on gaining a broader understanding of how these Sexual reproduction in plants entails a series of programs are regulated in sexual plants, and developmental steps that culminate in the formation investigations of sexual development are making of the seed (Box l)*,z.The process is highly regulated important contributions to apomixis research. In this and most aberrations result in abortion2. review, we have attempted to summarize these recent Nevertheless, plants have retained considerable contributions, and in particular to show how they plasticity in the possible outcomes of reproduction. might help to revise current models of the genetic (see One example is APOMIXIS Glossary), where control of apomixis. meiosis and fertilization of the egg by male gametes are bypassed to result in the production of clonal Developmental aspects of apomixis progeny without a paternal contribution. Apomixis There has been independent evolution of a therefore allows perpetuation of a fixed genotype remarkable diversity of seemingly unrelated through generationsg6. The ability to fix indefinitely apomictic mechanisms=. In this review, we focus on even highly complex genotypes, including high- one class of apomixis, GAMETOPHYTIC APOMIXIS,in which yielding hybrids, through apomixis would have the embryo originates from an unreduced gamete. tremendous advantages in plant breeding and seed Reviews on a second class of apomictic development, production (Box 2).Apomixis does not occur in the ADVENTITIOUS EMBRYONY, in which the embryo major crop species, but is found in many wild differentiates directly from a somatic cell, can be species. The genetics of apomixis in these species found elsewhere=. has been under scrutiny for several decades, with Gametophytic apomixis requires profound the aim of transferring apomixis to, or inducing modifications of the processes that govern sexuality. apomixis in, their crop relatives. These studies have Whereas in animals gametes differentiate directly Daniel GrimaneIli. Olivier Leblanc Enrico Perotti Glossary IRD-CIMMYT, Apomixis ~~ Apomixis: Asexual reproduction through seeds, often referred to as agamospermy. Project, carretera Mexico Adventitiousembryony:Asubcategoryof apomixis, in which theembryodifferentiates directlyfrom a somaticcell intheovule, without Veracruz, Km 45.5, formation a megagametophyte; often referred to as sporophytic apomixis. The sexual pathway remainsfunctional and the apomicitic Batan.Texcoco. of EI embryo relies on sexually produced endosperm. Therefore, the seeds can contain apomiciticand sexual embryos. Ed Mexico, Mexico. Gametophyticspomixis: The second subcategory of apomixis comprising diplosporous and aposporous apomixis, but excluding '%-mail: adventitious embryony. lngametophytic apomixis, the megagametophyte (embryo sac) arises from an unreduced spore. DGrimanelli @cgiar.org Diplosporous apomixis: The megagametophyte develops from an unreduced megaspore. Ueli Grouniklaua Aposporous epomixis:The megagametophyte develops from a somatic cell within the ovule. Dept of Plant Apomeiosis: Genericterm describing the failure of meiosis, via diplospory or apospory, ingametophytic apomicts. Development, Institute of Pseudogamousapomictt: Apomictic plants in which endosperm development depends on the fertilization of the central cell while the Plant Biology, embryo develops parthenogenetically. developwithoutfertilization,through Zollikerstrasse 107, Autonomous apomicts: Apomictic plants in which boththe embryo and the endosperm University ofZiirich, parthenogenesis. Parthenogenesis:Activation of embryo (or endosperm) development in the absence offertilization. CHdOO8Zii~ic_h,I Switzerland 7-- ... i I 1 I 0168-952501/5-seefrontmetterO2001 ElsevferScienceLtd.All rightsr O 10026364 I. 1 _. I 598 TRfNDSin Genetics Vol.1 No.10 October 2001 Box 1. Sexual reproduction in higher plants The lifecycle of higher plants (Fig. la) several cell divisions and extensive cell Megasporogenesis, or female meiosis alternates between a diploid sporophytic differentiation.The nuclei in red are occurs within a specialized organ of the phase, which producesthe spores through diploid (unreduced) and the nuclei in sporophyte, the ovule. It starts with the meiosis (the sporophytic phase, dark purple are haploid (reduced). differentiation of the megaspore mother blue), and a haploid gametophytic phase Fig. Ib shows sporogenesis and seed cell,which undergoes meiosis to produce (blue),which produces the gametes after development in higher plants. a tetrad of megaspores, only one of which usuallysurvives to form the functional megaspore. Microsporogenesis (male meiosis) occurs within theanthers, and producesfour microspores, all ofwhich survive. The differentiation of the spores marksthe beginning of the gametophytic generation. Both the micro- and megaspores divide Microgametophyte (n) V mitoticallyto form the multicellular gametophytes: the microgametophyte (pollen grain) on the male side and the megagametophyte (embryo sac) on the Fertilization femaleside. The mature megagametophyte is embedded in Megaspore Microspore Zygote CQ) '6 mother cell \Brmother cell /y maternal sporophytic tissue of the ovule, and typically comprises seven cells. Two ofthose cells, the egg cell and the binucleatecentral cell participate in double fertilization that is a unique feature ofthe angiosperms. The mature 0-4 two Sporogenesis Megagametogenesls Seed development microgametophyte contains sperm cells. Onefertilizes the egg, to produce the zygote and eventually the embryo. The second sperm fertilizes the central cell, producing the endosperm. Hence, the mature seed contains three types of tissue: the mlaternal tissues, and two hybrid tissues of different ploidy levels-the diploid embryo and thetriploid in Fig. I 1 TRENDS Genelics endosperm. from the meiotic products, gametogenesis in plants is and germination8, although its relative importance preceded by formation of multicellular gametophytes varies greatly hom species to species. For example, (Box 1). In the female reproductive organ (the ovule), the endosperm never forms in certain orchids and is a single cell normally becomes committed to the transient in Arabidopsis thdianu,but constitutes sexual pathway, undergoes meiosis and forms a 80-90% of mature cereal seeds. tetrad of reduced spores. One of these spores divides The switch from a normal sexual pathway (Box 1) mitotically to form a multicellular female to an apomictic pathway entails at least three major gametophyte, the embryo sac, which contains the steps (Box 3): female gametes. The three other spores degenerate. circumvention of meiosis (a process called In the male reproductive organs (the anthers), all APOMEIOSIS); meiotically produced spores undergo mitotic * development of the embryo independently of development to form mature male gameto hytes - fertilization (i.e. PARTHENOGENESIS); the pollen grains. Apollen grain usually CO sists of formation of a functional endosperm. two sperm cells contained within a large v getative These requirements are met by a variety of means in cell. Fertilization involves two pairs of ga etes. One apomictic plants, and as a result the mechanisms of sperm fuses with the egg cell to form the z gote and apomixis are numerous (Box 3), although they share eventually the embryo, and the second spe m fuses common characteristics. First, most if not all with the binucleate central cell to form the apomicts are polyploid. Second, apomixis affects only endosperm. "he endosperm has important nutritive the female reproductive pathway and male gametes and physiological functions during seed development1 are still produced through meiosis. Third, most http:/ltig.trends.com Box 2. Apomixis and its potential in agriculture Apomixis can be viewed as a short-circuited Gametophytic Sexual sexual pathway,
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