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First published online May 6, 2004; 10.1105/tpc.017921
© 2004 American Society of Plant Biologists Understanding Apomixis: Recent Advances and Remaining Conundrums
a Crop and Food Research, Private Bag 4704, Christchurch, New Zealand 1 To whom correspondence should be addressed. E-mail: anna.koltunow{at}csiro.au.
It has been 10 years since the last review on apomixis, or asexual seed formation, in this journal (Koltunow, 1993  ). In that article, emphasis was given to the commonalties known among apomictic processes relative to the events of sexual reproduction. The inheritance of apomixis had been established in some species, and molecular mapping studies had been initiated. The molecular relationships between apomictic and sexual reproduction, however, were completely unknown. With research progress in both sexual and apomictic systems in the intervening years, subsequent reviews on apomixis in the literature have considered the economic advantages of providing apomixis to developing and developed agricultural economies (Hanna, 1995; Savidan, 2000a) and strategies to gain an understanding of apomixis by comparison with sexual systems (Koltunow et al., 1995a; Grimanelli et al., 2001a). The potential to "synthesize apomixis" in agricultural crops in which it is currently absent by modifying steps in sexual reproduction and the possible ecological consequences of the release of "synthesized apomicts" in nature also have been discussed (van Dijk and van Damme, 2000; Grossniklaus, 2001; Spillane et al., 2001). Recently, comparative developmental features of apomixis have been considered in light of the now considerable knowledge accumulated about ovule and female gametophyte development, and seed formation in sexual plants (Koltunow and Grossniklaus, 2003). In this review, we focus on the initiation and progression of apomixis in plants that naturally express the trait. Since 1993, there has been a growing understanding of the complexity that underlies apomixis; some contentious issues have been resolved and others raised. There also have been significant advances in terms of new model systems and approaches being used to study apomixis. We structure the wider discussion around the knowledge of apomixis we have accumulated from our study of Hieracium species, or hawkweeds, a model system we established, and consider additional factors that should be taken into account to induce apomixis in crops. The continued comparative analyses of apomictic and sexual reproduction at the fundamental level in appropriate model systems remains essential for the development of successful strategies for the greater application and manipulation of apomixis in agriculture.
Apomixis in flowering plants is defined as the asexual formation of a seed from the maternal tissues of the ovule, avoiding the processes of meiosis and fertilization, leading to embryo development. The initial discovery of apomixis in higher plants is attributed to the observation that a solitary female plant of Alchornea ilicifolia (syn. Caelebogyne ilicifolia) from Australia continued to form seeds when planted at Kew Gardens in England (Smith, 1841 ). Winkler (1908) introduced the term apomixis to mean "substitution of sexual reproduction by an asexual multiplication process without nucleus and cell fusion." Therefore, some authors have chosen to use apomixis to describe all forms of asexual reproduction in plants, but this wider interpretation is no longer generally accepted. The current usage of apomixis is synonymous with the term "agamospermous" (Richards, 1997). Because seeds are found only among angiosperm and gymnosperm taxa, this definition of apomixis limits its use to those groups. In lower plants, phenomena similar to apomixis are known, but discussion remains about the use of this term in cases in which the reproductive structures involved are different yet are considered analogous (Asker and Jerling, 1992).
Although it is sometimes referred to as a botanical curiosity, apomixis is far from rare, being relatively prevalent among angiosperms, with a pattern of distribution that suggests that it has evolved many times. It has been described in >400 flowering plant taxa, including representatives of >40 families (Carman, 1997 ), and it is well represented among both monocotyledonous and eudicotyledonous plants; curiously, though, it appears to be absent among the gymnosperms. These estimates are almost certainly very conservative. Unequivocal confirmation of apomixis requires the simultaneous examination of both genetic and cytological evidence (Nogler, 1984a). Embryological examination of plant taxa for apomixis has not been exhaustive, and supporting genetic evidence is uncommon even when apomixis has been declared for a given plant. It seems likely that as our understanding of this phenomenon grows and methods to determine its presence improve, many more angiosperm taxa will be found to include apomictic representatives and some suspected cases will be revised. A recent study by Plitman (2002) supports this prediction.
Several authors have noted a marked bias in the distribution of apomixis among angiosperms (Asker and Jerling, 1992
There are other noted associations between apomixis and various plant life history traits that provide insight into the nature and possible ecological role of this phenomenon. Apomixis frequently is associated with the expression of mechanisms that limit self-fertilization (autogamy). Many apomictic plants belong to genera in which sexual members predominantly exhibit physiological self-incompatibility, dioecy, or heterostyly (Asker and Jerling, 1992 ). In some cases, it is clear that the apomicts themselves have retained such mechanisms. Dioecy is known in a number of apomicts, such as Antennaria (O'Connell and Eckert, 1999), Cortaderia (Philipson, 1978), and Coprosma (Heenan et al., 2002). Similarly, self-incompatibility, a known characteristic of the sexual biotypes of Hieracium subgenus Pilosella (Gadella, 1984, 1991; Krahulcovà et al., 1999), was demonstrated recently in the apomictic species H. aurantiacum and H. piloselloides (Bicknell et al., 2003).
Apomictic species also are almost invariably perennials, and they often use a vegetative mechanism of asexual reproduction, such as stolon or rhizome growth. Thus, in the field, through a combination of apomixis and vegetative division, apomicts can form large clonal stands, and these may persist through long periods of time. Apomixis also frequently leads to the formation and maintenance of numerous morphologically distinct, yet interfertile, varieties growing true to type from seed. The taxonomy of such agamic complexes can be a difficult and contentious task (Dickinson, 1998
All known mechanisms of apomixis share three developmental components: the generation of a cell capable of forming an embryo without prior meiosis (apomeiosis); the spontaneous, fertilization-independent development of the embryo (parthenogenesis); and the capacity to either produce endosperm autonomously or to use an endosperm derived from fertilization (Koltunow, 1993 , Carman, 1997). That said, although broad similarities can be seen at the level of the key events of apomixis, it is probably true that there are as many mechanisms of apomixis as there are plant taxa that express the trait. Some clear commonalities have been identified, however, and these have been used to categorize apomictic mechanisms into broad groupings. Figure 1 portrays these mechanisms in relation to the temporal sequence of events in the reproductive cycle of sexual plants. Two main subgroups of mechanisms are apparent. In sporophytic apomixis, or adventitious embryony, embryos arise spontaneously from ovule cells late in the temporal sequence of ovule maturation (Figure 1). Gametophytic apomixis operates through the mediation of an unreduced embryo sac. Endosperm development in these plants may be either spontaneous (autonomous) or fertilization induced (pseudogamous) (Koltunow, 1993).
Gametophytic mechanisms are further subdivided based on the cell type that gives rise to the unreduced embryo sac. In diplosporous types, the megaspore mother cell (MMC) or a cell with apomictic potential occupying its position is the progenitor cell for the unreduced embryo sac. That cell may enter meiosis but this aborts, and development proceeds by mitotic division to achieve embryo sac formation (meiotic diplospory). Alternatively, that cell might undergo direct mitosis to form an unreduced embryo sac (mitotic diplospory). In aposporous apomicts, one or more somatic cells of the ovule, called aposporous initials, give rise to an unreduced embryo sac. Aposporous initials can differentiate at various times during ovule development. Meiotically reduced and aposporous embryo sacs might coexist in the ovule, or the aposporous embryo sac might continue development while the reduced sexual embryo sac degenerates (Figures 1 and 2). The further subdivision of gametophytic mechanisms (not shown in Figure 1) has been based on characteristics related to the involvement, or avoidance, of the different phases of meiosis, the number of mitotic divisions, and the eventual form of the embryo sac (Crane, 2001
The existence of apomixis in 40 plant families and the diversity of apomictic processes suggests that the routes that led to the evolution of apomixis may be as diverse as the known cytological mechanisms. Morphological comparisons of structures formed during sexual and apomictic reproduction provide hints that the two reproductive pathways may share common elements, but there also are numerous abnormalities. In the case of diplosporous and aposporous embryo sac formation, a meiotic tetrad is not observed. Positional differentiation of aposporous initials (and adventitious embryos) occurs most frequently adjacent to cells undergoing sexual reproduction, but they do not necessarily arise from the nucellus, because epidermal and integumentary origins have been described (Koltunow and Grossniklaus, 2003 ). Irregularities also occur in the development of diplosporous and aposporous embryo sacs, with structural abnormalities more prevalent in apospory. Common abnormalities include a lack of polarization of nuclei during early mitotic divisions, odd or excessive numbers of nuclei varying in size, monopolar embryo sacs, embryo sacs with inverted polarity or an abnormal situation of the egg apparatus, and increased numbers of apparent polar nuclei. In some cases, the final embryo sac structure is quite stably different and used as a diagnostic tool, the best example being the four-nucleus Panicum-type embryo sac (Koltunow, 1993; Czapik, 1994).
Most apomicts produce viable pollen. Even in diplosporous apomicts, defects in the meiotic events of female gametophyte development are not automatically extended to male gametophyte formation or function. The presence of viable pollen provides the possibility of fertilization of unreduced eggs. In apomicts such as Taraxacum (Cooper and Brink, 1949
In apomicts, embryo and endosperm pattern formation may or may not be conserved relative to that observed in related sexual plants, although the latter has been least studied (Koltunow, 1993
Apomixis is an attractive trait for the enhancement of crop species because it mediates the formation of large genetically uniform populations and perpetuates hybrid vigor through successive seed generations. Many agronomic advantages of apomixis can be envisioned: the rapid generation and multiplication of superior forms through seed from novel, currently underused germplasms; the reduction in cost and time of breeding; the avoidance of complications associated with sexual reproduction, such as pollinators and cross-compatibility; and the avoidance of viral transfer in plants that are typically propagated vegetatively, such as potatoes (Hanna, 1995 ; Jefferson and Bicknell, 1995; Koltunow et al., 1995a, Savidan, 2000a, 2000b). The value of these opportunities will vary between crops and between production systems. For farmers in the developed world, the greatest benefit is expected to be the economic production of new, advanced, high-yielding varieties for use in mechanized agricultural systems. Conversely, for farmers in the developing world, the greatest benefits are expected to relate to the breeding of robust, high-yielding varieties for specific environments, improvements in the security of the food supply, and greater autonomy over variety ownership (Bicknell and Bicknell, 1999; Toenniessen, 2001). However, apomixis is very poorly represented among crop species. The main exceptions to this appear to be tropical and subtropical fruit trees, such as mango, mangosteen, and Citrus, and tropical forage grasses, such as Panicum, Brachiaria, Dichanthium, and Pennisetum. It is possible that the low representation of apomixis among crops arose unintentionally from a protracted human history of selecting superior plants for future cultivation. Selection for change over a parental type would work against a mechanism such as apomixis that acts to maintain uniformity. The presence of the trait among tropical fruit and grass crops may be a reflection of this effect, because focused efforts to improve these crops are comparatively recent events.
There also are few apomictic species of significant relatedness available for use in introgression programs, which may explain at least some of the difficulties experienced when attempts have been made to introduce apomixis into crops through hybridization. For example, major programs aimed at introducing apomixis into maize (Sokolov et al., 1998
Current research on apomixis generally is divided into two complementary approaches: the evaluation of the trait in natural apomictic systems, and the "synthesis" of the trait through the directed modification of reproductive events in a sexual species. Of the native monocot apomictic systems under study, most work focuses on aposporous plus pseudogamous species in the genera Panicum (Savidan, 1980 ; Chen et al., 1999), Pennisetum and Cenchrus (Roche et al., 1999), Brachiaria (Pessino et al., 1997, 1998), Paspalum (Martinez et al., 2001), and Poa (Naumova et al., 1999; Albertini et al., 2001a, 2001b) and the diplosporous plus pseudogamous genus Tripsacum (Grimanelli et al., 1998a, 1998b; Sokolov et al., 1998). The eudicot genera under study include the daisy genera Taraxacum and Erigeron (diplosporous plus autonomous) (Noyes and Rieseberg, 2000; van Dijk et al., 2003) and Hieracium (aposporous plus autonomous) (Koltunow et al., 1998, 2000). Hypericum perforatum (aposporous plus pseudogamous), a member of the St. John's wort family, has been well studied (Matzk et al., 2001, 2003), and Boechera holboellii (syn. Arabis holboellii; diplosporous plus pseudogamous) (Naumova et al., 2001; Sharbel and Mitchell-Olds, 2001), a relative of Arabidopsis, also is receiving attention for its potential to exploit the vast genetic and molecular resources developed in Arabidopsis. We suspect that these efforts may become more focused in coming years as the relative advantages of one or a small number of these systems leads to their predominant use (Bicknell, 2001). Among the sexual species under study for the synthesis of apomixis, there is little doubt that Arabidopsis, rice, and maize will remain the systems of choice because of the availability of genetic and molecular tools and, for the latter crops, the strong economic and social drivers seeking the installation of the trait (Khush, 1994; Savidan, 2000a).
During the last 10 years, Hieracium subgenus Pilosella has been developed into a model system for the genetic and molecular study of gametophytic apomixis (Bicknell, 1994a , 2001; Koltunow et al., 1998; Koltunow, 2000). These plants are highly suited for molecular studies because they are small, herbaceous perennials with a rapid generation time (3 to 6 months) and a long-day photoperiodic response that allows them to be flowered on demand at any time of the year (Yeung, 1989). Some species include both sexual and apomictic biotypes, and hybrids formed between most of the species have proven to be fertile. This allows the inheritance of apomixis to be studied using intraspecific hybridization, in contrast to many other apomictic plant systems. Methods for the micropropagation (Bicknell, 1994b), anther culture (Bicknell and Borst, 1996), genetic transformation (Bicknell and Borst, 1994), and progeny class estimation (Bicknell et al., 2003) of Hieracium have been developed to further facilitate its use in the molecular study of apomixis. The plants also are very amenable to vegetative propagation, which is of particular value when genetic or molecular manipulations affect flower form and/or seed set. Vegetative propagation also is the preferred mode of stock maintenance, because a fraction of the progeny is not true to type (see below).
In all of the wild-type apomicts of Hieracium studied to date, both the embryo and endosperm arise spontaneously inside an unreduced aposporous embryo sac (Figure 2). The initiation of apospory is stochastic in these plants, but in each form, the majority of aposporous initial cells tend to differentiate at a particular time relative to the concurrent sexual process in the ovule. This makes the plants valuable for examining factors that influence the timing of aposporous initial formation. In most of the apomictic Hieracium plants characterized to date, the sexual process usually ceases soon after apospory initiates (Koltunow et al., 1998
Endosperm development was examined recently in the autonomous apomict H. piloselloides (tall hawkwed) and compared with that in a sexual biotype, H. pilosella (mouse ear hawkweed). In the apomict, autonomous endosperm development initiates primarily, but not exclusively, from fused polar nuclei. In contrast to the fertilization-dependent endosperm development in the sexual plant, migrating clumps of nuclei form during early endosperm development in the apomict, but as nuclei numbers increase, this is rectified so that the cellularization and maturation events are cytologically indistinguishable in the two types (M. Tucker and A.M. Koltunow, unpublished results). Apomictic Hieracium plants exhibit developmental abnormalities reminiscent of epigenetic phenomena. For example, there are disturbances in the pattern of embryo formation and phyllotaxis during early seedling growth in apomictic Hieracium that are reset eventually to a normal pattern with subsequent plant growth (Koltunow et al., 1998 Sexual reproduction, or components of it, are not excluded completely in apomictic Hieracium. In some ovules, either apospory does not initiate or it fails and the meiotic process proceeds to completion. In addition, fertilization may or may not occur in these plants irrespective of the reduced or unreduced nature of the egg. Thus, Hieracium is facultative for apomixis, because a fraction of the seedlings are nonmaternal in genotype.
The coexistence of apomixis and sexuality is certainly not unique to Hieracium. For all of the mechanisms of apomixis known, and for almost all of the genotypes studied in depth, it has been reported that some degree of sexuality remains possible in apomictic plants; thus, most are regarded as facultative. True obligate apomicts, those able to form seeds by apomixis alone, are very uncommon (Asker and Jerling, 1992 ). Facultative, gametophytic apomicts are capable of hybridization using either a reduced or an unreduced egg cell. The previously described mechanisms of early egg cell wall completion and precocious embryogenesis of unreduced eggs are by no means fully penetrant. This can lead to the formation of two different types of hybrid progeny. Reduced hybrids result from the fusion of a reduced egg cell with a reduced sperm cell, whereas unreduced hybrids typically result from the mediation of an unreduced egg cell. In the nomenclatural system of Rutishauser (1948), these are referred to as BII and BIII hybrids, respectively. Harlan and De Wet (1975) termed them n+n and 2n+n hybrids, respectively, whereas Asker (1977) used the terms R- and U-hybrids. Unfortunately, all of these terms are still used in the literature, but it does appear that the system of Harlan and De Wet (1975) is now the most popular choice, and we will continue with its use in this article. A further progeny class of note in these plants are n+0 seedlings, or "polyhaploids." These plants result from the parthenogenetic development of a reduced egg cell, leading to the formation of a plant with a ploidy state less than that of the parent. Although male meiosis and male gamete function are typically normal in gametophytic apomicts, the formation and use of unreduced pollen also has been observed (Matzk et al., 2001). Both the formation of unreduced gametes and the parthenogenetic development of unfertilized egg cells are widely recorded phenomena in sexual species (Grossniklaus, 2001); however, they are typically much more frequent events among apomicts. In the case of H. aurantiacum and H. piloselloides, the rates of parthenogenesis (which includes 2n+0 and n+0 progeny) were 97.6 and 98.0%, respectively (Bicknell et al., 2003) (Figure 3) compared with reported examples of 0.11% for maize and 0.018% for Datura (Kimber and Riley, 1963).
An important practical outcome of the diversity of progeny types produced by apomictic Hieracium, and for that matter by most other apomicts, is that the progeny of these plants cannot be considered to be uniformly of clonal, maternal origin. In particular, because different progeny classes result from the different actions of segregation (meiosis) and recombination (fertilization), different inheritance ratios are expected in each progeny class, and this fact must be considered in any analysis of trait transmission. Even in sporophytic apomicts such as Citrus, in which spontaneous embryogenesis adjacent to a reduced embryo sac is the defining manifestation of this form of apomixis (Koltunow et al., 1995b ), some authors have noted that unreduced embryo sacs do also form (Naumova, 1992). Plants with unexpectedly high ploidy levels are frequently observed in breeding populations of Citrus, and it seems likely that such individuals arise following the fertilization of an unreduced egg cell, in a manner similar to that seen in gametophytic apomicts.
Given the importance of understanding the relative levels of different progeny types among the seedlings produced by a facultative apomict, there has been a strong need for robust methodologies to determine these levels and to isolate representative subpopulations for separate analysis. For many years, the nonmaternal ("aberrant" or "off-type") progeny of apomicts were identified through morphological scoring, chromosome counting, or progeny cross methods, which were too inaccurate and too expensive to warrant their use on any scale. Recently, methods based on flow cytometry and transgenesis have been published that address these limitations. The method of Matzk et al. (2000)
The facultative expression of apomixis, therefore, is an experimental complexity in the study of these plants. However, it has proven to be a valuable tool for exploring the unique biology of apomixis, particularly in the analysis of interactions between apomixis and sexuality. For example, polyhaploidy (n+0) was used to isolate diploid apomictic plants of the species H. aurantiacum and H. piloselloides (Bicknell, 1997
Another area of study has been the origin of multiple embryos, a common occurrence in the seeds of many apomicts. The formation of multiple viable embryos, or polyembryony, is evident in up to 10% of H. aurantiacum seeds and 17% of H. piloselloides seeds (Koltunow et al., 2000
The interplay between sexuality and apomixis in facultative plants provides an opportunity to consider the evolutionary and ecological implications of these different modes of reproduction (Krahulcovà et al., 2000
One means of assessing the relationships between sexual and apomictic pathways is to use developmental markers that identify specific cells or structures in sexual systems and to examine their expression in apomictic plants. One of the earliest used was the biochemical detection of callose, a ß-1,3-linked glucan that accumulates in a distinctive manner during female gametophyte development in sexual plants. The walls of the MMC (or megasporocyte), the tetrad of megaspores (Figure 2), and degenerating megaspores are marked by the temporary accumulation of callose. It is lost from the walls of the selected megaspore during its expansion and is absent once the mitotic events of embryo sac development initiate.
Differences in callose deposition during gametophyte development in sexual and apomictic plants have been noted, and in the case of Tripsacum, this has been used as a screening tool to identify apomicts (Leblanc and Mazzucato, 2001
Considerable information has now been accumulated concerning the regulation of ovule and female gametophyte development in sexual plants, and this provides molecular tools for the comparative analysis of sexual and apomictic reproduction (Koltunow and Grossniklaus, 2003 ). Tucker et al. (2003) provided strong evidence that sexual and apomictic reproduction in Hieracium are related developmental pathways that share common regulatory programs (Eckardt, 2003). They examined the expression patterns of several reproductive marker genes from Arabidopsis in sexual and apomictic Hieracium. These markers were fusion constructs of ß-glucuronidase (GUS) and a variety of Arabidopsis genes as promoter:GUS or chimeric protein fusions. The markers included SPOROCYTELESS (SPL/NOZZLE), which is required for male and female sporogenesis in Arabidopsis (Schiefthaler et al., 1999; Yang et al., 1999), SOMATIC EMBRYO RECEPTOR KINASE1 (SERK1), which is thought to play a role in embryogenesis (Hecht et al., 2001), and three independent FIS class genes, mutations in any one of which result in fertilization-independent endosperm development (Luo et al., 2000). An astonishing conservation of expression pattern was observed in apomictic and sexual Hieracium plants using these chimeric genes that for the most part also reflected patterns observed in Arabidopsis (Tucker et al., 2003). AtSPL:GUS was expressed in MMCs but not in aposporous initials, providing the first molecular evidence that these cells develop from somatic cells that do not share identity with MMCs. SERK1:GUS expression was conserved in pattern in sexual and apomictic plants, and the three FIS chimeric genes were expressed coordinately during the early events of seed development in Hieracium.
The main differences in spatial and temporal expression pattern occurred early in ovule development and, in marked contrast to Arabidopsis AtFIS2:GUS, was expressed at the completion of meiosis in both sexual and apomictic Hieracium (Figure 4). The spatial pattern of expression, however, differed in sexual and apomictic plants. In sexual Hieracium, expression of AtFIS2:GUS was observed in the three megaspores destined to degenerate, was absent from the single cell layer enveloping them (nucellar epidermis) destined for degeneration, and was absent from the selected megaspore until the first nuclear division of embryo sac formation. By contrast, in two apomictic Hieracium species with differing modes of aposporous embryo sac formation, AtFIS2:GUS expression was observed in all four megaspores and the enveloping nucellar epidermis, all of which were destined for degeneration. Expression of AtFIS2:GUS was absent from aposporous initials until their first nuclear division, similar to the expression profile observed for the functional megaspore in sexual plants (Figure 4). We speculate that the spatial differences in AtFIS2:GUS expression in sexual and apomictic plants might reflect gene expression shifts associated with aposporous initial cell commitment to the events of embryo sac initiation and the concomitant displacement of the sexual pathway. Therefore, FIS genes might play a different role in Hieracium relative to that in Arabidopsis that could be related to the capacity for apomixis and autonomous seed development (Eckardt, 2003
The findings of Tucker et al. (2003) indicate that sexual and apomictic pathways in Hieracium share common gene expression profiles and thus common molecular regulatory features, indicating that they are not distinct pathways (Figure 4). The form of apomixis in Hieracium (apospory coupled with autonomous embryo and endosperm development) appears to differ from sexual reproduction in a very limited number of ways. Specifically, it is comparable to sexual development except for two specific switch points: meiosis and fertilization. For apomixis to occur in Hieracium, the developmental program of one or at most a few cells is altered, and this appears to be sufficient to enable them to bypass meiosis yet mimic the normal program seen in the descendants of a selected megaspore. Later development bypasses fertilization but still moves through the normal embryo and endosperm developmental programs (Figure 5). These data suggest that apomixis is a deregulation of the sexual reproductive program in space and time, leading to cell fate changes and the omission of steps critical to sexual progression. It is conceivable that different types of apomixis, as seen in other species, might arise depending on when and where this deregulation occurs (Koltunow and Grossniklaus, 2003). Figure 1 also portrays this concept in the sense that it depicts the three broad classes of apomictic mechanisms as operating within the framework of the sexual reproductive cycle. Differential and subtractive hybridization have been attempted to isolate genes relevant to apomictic reproduction (Vielle-Calzada et al., 1996; Guerin et al., 2000; Pessino et al., 2001). Although not exhaustive, these have failed to find genes specific to structures arising from apomictic development when the expression of these genes has been examined (Guerin et al., 2000). Although negative in context, this observation further supports the proposal that sexual and apomictic developmental pathways differ primarily at the level of regulation of common elements.
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INTRODUCTION
WHAT IS APOMIXIS?
