Understanding Apomixis: Recent Advances and Remaining Conundrums

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 to as a apomixis is from being among with a of that that it has It has been in flowering plant taxa, of and it is among both and it to be absent among the are of apomixis the of both and of plant for apomixis has been and is when apomixis has been for a given It that as our understanding of this and to its angiosperm be found to apomictic and some cases be study by this and of to in the of The of the is in this to the events of gametophyte formation, the events in the ovule leading to seeds in and are from a cell in the of the or from ovule that the events of meiosis and to to form an embryo from a in embryo formation fertilization, or in a of it be is apomixis form from or to a embryo The and of is on the from in the embryo There are between apomixis and plant that into the nature and possible ecological of this Apomixis is with the of that apomictic plants to in which sexual or (Asker and Jerling, 1992). In some it is that the have is known in a of as and and et al., a known of the sexual of Hieracium et al., was in the apomictic and et al., 2003). also are and use a of asexual reproduction, as or in the a of apomixis and form and of Apomixis also to the formation and of yet growing to from The of be a and contentious of in which the apomictic of reproduction is with and are found in that are the growing is as and or to the successful of as among a (Asker and Jerling, 1992). There also are that events defined the of (Asker and Jerling, 1992). apomixis is known among and species, but it is among the be a of the of the in the and the both of which are of apomixis is among plants that have as in the and but this be known of apomixis developmental the of a cell of an embryo without meiosis the development of the embryo and the to or to use an from (Koltunow, 1993, 1997). be at the level of the events of apomixis, it is that there are as of apomixis as there are plant that express the trait. have been however, and have been used to apomictic into in to the of events in the reproductive of sexual of are In apomixis, or from ovule in the of ovule apomixis the of an embryo development in plants be or (Koltunow, 1993). are on the cell that to the embryo In the cell or a cell with apomictic potential its is the cell for the embryo cell meiosis but this and development by to embryo formation that cell to form an embryo In or of the ovule, to an embryo at ovule development. and embryo in the ovule, or the embryo development the sexual embryo The of in has been on to the or of the different of the of and the form of the embryo 2001). The of apomixis in plant and the of apomictic processes that the that to the of apomixis be as as the known of structures sexual and apomictic reproduction that the reproductive but there also are In the of and embryo formation, a is of to sexual reproduction, but from the and have been (Koltunow and Grossniklaus, 2003). also in the development of and embryo with in a of of or of in embryo embryo with or an of the and of In some the embryo structure is different and used as a the being the embryo (Koltunow, in in the events of female gametophyte development are to gametophyte formation or The of the of of In as and (Asker and Jerling, and Hieracium (Koltunow et al., embryo formation be or the of the the of cell In sexual species, the cell has an cell and of a cell only in the In the however, a cell forms around the cell the of the the et al., is a species, to development. The development of a cell around the of this to as a to of the cell with the cell at the of and that and were and developed in found in embryo in the of this are with cell and of a or of the of cell development, a of In embryo and formation or be relative to that in sexual plants, the has been (Koltunow, also to in in and form seeds et al., and Grossniklaus, 2003). this and its on seed is for the of apomixis in in which in in are Apomixis is an for the of it the formation of and seed advantages of apomixis be the and multiplication of forms seed from currently the in and of the of with sexual reproduction, as and and the of in plants that are as (Hanna, 1995; and 1995; et al., Savidan, The of between crops and between in the developed the is to be the economic of for use in agricultural for in the developing the are to to the of for in the of the and greater and 2001). apomixis is among The to this to be and as and and as and It is possible that the of apomixis among crops from a of plants for for a a as apomixis that to The of the among and crops be a of this to crops are There also are apomictic of significant for use in which at some of the when have been to apomixis into crops at apomixis into et al., Savidan, from the relative have been now for yet have in terms of apomictic plants with of seed also have been in to apomictic of et al., Savidan, 2001). it that in terms of to apomixis in agricultural with apomictic species, as the and are by the to use strategies to the of the female to and 2001). We that the be the of apomixis into crops in an its use seed but for its be the that the with sexual and the the have on seed and for a given research on apomixis generally is into the of the in apomictic and the of the the of reproductive events in a sexual the apomictic systems on in the et al., and et al., et al., et al., and et al., et al., and the et al., et al., The study the and and 2000; van Dijk et al., and Hieracium (Koltunow et al., a of the has been et al., and (syn. et al., 2001; and a relative of also is for its potential to the and molecular developed in We that in years as the relative advantages of or a of systems to use 2001). the sexual study for the of apomixis, there is that and the systems of of the of and molecular for the the economic and the of the Savidan, the last 10 years, Hieracium has been developed into a model system for the and molecular study of apomixis 2001; et al., plants are for molecular studies are with a to and a that to be on at of the both sexual and apomictic and between of the have to be the inheritance of apomixis to be in to apomictic plant for the and and and et al., of Hieracium have been developed to its use in the molecular study of apomixis. The plants also are to which is of when or molecular form seed also is the of a of the is to of in of and Hieracium The events of embryo formation in sexual plants and in are and embryo formation is The of development as defined by et and embryo structures are for and In embryo form with and to form a embryo (Koltunow et al., The of in the of in at or and in in at or is by the of to light et al., 2001). in and are of the of and embryo that the initial in cell et al., 2001). also forms to an embryo (Koltunow et al., embryo embryo development was in the and with that in a sexual In the development but from In to the development in the sexual of form development in the but as this is that the and events are in the and Hieracium plants developmental of there are in the of embryo formation and in apomictic Hieracium that are to a with subsequent plant (Koltunow et al., reproduction, or of are completely in apomictic In some or it and the process to In or in plants of the or nature of the Hieracium is for apomixis, a of the are in in Hieracium for of the are maternal there is no from a form a that be into a of also are from the use of a that the be with a cell from or to to that from sexual reproduction or also be with from or to to or that have relative to the maternal to be in from are are from et al., 2003). of the of by apomictic and for that by is that the of plants be considered to be of maternal In different from the different of and different inheritance are in and this be considered in of in as in which to a embryo is the of this form of apomixis (Koltunow et al., some authors have that embryo also form 1992). with are in of and it that the of an in a similar to that in the of understanding the relative of different among the by a there has been a for to and to for years, the or of were or which were and to use on Recently, on and have been that The of et which a to is to be in that it the of for of apomixis et al., 2003). In a on the inheritance of and has been et al., 2003). which is on the of different when on the of being and to It also a for the of however, is to plants that be and it is for studies that and a of The of apomixis, is an complexity in the study of it has to be a for the of apomixis, in the of between apomixis and was used to apomictic plants of the and et al., 2000; et al., that apomixis in both and of this the of and in both and that a was to formation in plants the nature of apomixis in Hieracium et al., of study has been the of a in the seeds of The formation of or is in to of seeds and of seeds (Koltunow et al., 2000; et al., 2003). The of the additional remains a in the of the sexual process and a embryo is at the initiation of We that the additional from or that had in (Koltunow et al., a study et al., it was found that were to in a seed from a embryo The a asexual embryo is remains is the formation of from or from is completely given that an form of forms (Koltunow et al., development from both and sexual embryo an that have to of its The between and apomixis in plants an to consider the and ecological of different of reproduction et al., 2000; and 2001). et that in and the of from usage and were and yet the of embryo development are different in plants (Koltunow et al., that the of use to in plants is to be a it is a to the relative and of sexual and asexual reproduction in is by for the of a in plants et al., 2003). that is an in the of in et that the of among (syn. Hieracium at in the of the of this into that and the apomictic nature of the and 2001). have been for the (van et al., of the relationships between sexual and apomictic is to use developmental that or structures in sexual systems and to in apomictic of the used was the of a that in a female gametophyte development in sexual The of the the of and are by the of It is from the of the its and is absent the events of embryo development in gametophyte development in sexual and apomictic plants have been and in the of this has been used as a to and 2001). In both and which et al., is absent from the of the cell that which is by and as the that was in the it was possible to and processes in the however, was in the of sexual In in which the initiation of both sexual and apomictic processes be was completely absent from initial in et al., and and Hieracium et al., but in the in and also have in in the was in but an of with the of et al., 2001). in by et with initial formation were in Hieracium with to in the plants in be et al., 2001). that apomixis is an form of sexual reproduction in all of the the of in that and that with et that the of plants which be as a in but are to this has now been accumulated the of ovule and female gametophyte development in sexual plants, and this molecular for the comparative of sexual and apomictic reproduction (Koltunow and Grossniklaus, 2003). et that sexual and apomictic reproduction in Hieracium are developmental that 2003). the of reproductive from in sexual and apomictic were of and a of as or The which is for and female in et al., et al., which is to a in et al., and in of which in development et al., of was in apomictic and sexual Hieracium plants that for the also in et al., 2003). was in but in providing the molecular that from that with was in in sexual and apomictic plants, and the were the events of seed development in in from sexual Hieracium to apomictic Hieracium to and apomictic Hieracium to were with and and or The at the the (Koltunow et al., in and and in to to and ovule in the to in and by the structures are with a with a nucleus to structures are with a an embryo embryo and by the ovule the of apomictic development to initial at the of apomictic development to The with a is in a different to the which are with an initial cell ovule a embryo with embryo at the of apomictic development to ovule the of apomictic development to and at the of apomictic development to and initial are with and some form in different with the sexual are with an initial embryo structures at the of apomictic development to and from et for Apomixis in Hieracium from et al., 2003). In sexual as the development of both the embryo and the embryo is by from ovule tissues et al., et al., of that the of apomictic events in Hieracium is by from ovule and form were in that from in plants the from is known to plant and to In by and and the sexual process and a higher of was however, and continued to (Koltunow et al., 2001). from was found to similar but in and formation those in from The developmental events of apomixis in those found in in terms of the of apomictic initiation and of the process in (Koltunow et al., the plant also is of that are found to an embryo the process of (Koltunow et al., from initial to a different as a of in ovule structure from ovule a in a of in a of et al., 1997). of the of in apomictic events in The known study of inheritance in an apomictic plant was by to in of inheritance by It is known on Hieracium of the have been but from the that is that of a of to in the Hieracium the and were In with a Hieracium the in the systems which the of a higher the of the apomixis was a known in plants, and to the study of inheritance in of with the of apomixis in this It had taken years to The inheritance of apomixis has since been to be with the of a or a of in of the systems to In the et al., and et al., apomixis is to be with the by the of a inheritance also has been for in the and Hieracium et al., the inheritance of and have been in the (van Dijk et al., and in 2000; and and the inheritance of in the the inheritance of in is to be and et al., There is of in some of the with apomixis also to its to some Grimanelli et al., et al., et al., and it is that there is or only a of involved in the inheritance of apomixis in There however, some with the interpretation of In all of the cases the inheritance of apomixis was between sexual and apomictic in the of apomixis the use of the to the are and the of maternal remains be in Apomixis is a trait. it should be the of with an study to the reproductive of plant and an of in all by is that are used as a of apomixis review, 2001; and 2001). the development of embryo in and the formation of in Hieracium et al., In all there are for in the of apomixis. in an of the embryo form in the are the of but it is are from from a of the studies of our et al., with a new of inheritance in this we now that the of has been a being it that as as factors to be to the of apomixis as an in Hieracium studies also that are for the inheritance of apomixis in (van Dijk et al., 2003). with the interpretation of some of the inheritance for apomixis is that it apomixis as a that is or apomixis is in plants, and the level of asexual seed formation between observation from inheritance studies is that the level of apomixis by of the is that of the apomictic et al., be of the apomictic in an inheritance study by the authors on Hieracium the at of the seed apomixis was at in the apomictic et al., 2000; et al., 2000; to apomixis from to crops also an of this is an apomictic relative of and have been involved in an to apomictic for years the of into are for the significant of involved and for the use of for the of and the inheritance of the however, significant progress has been to to the the of apomixis into a with the of remains an the plants to no apomictic have been with 2001). have been for the of apomixis into from by Savidan, 2001). and have some in the of apomixis to that the be as or as in systems as is some that a both sexual and a to express this et al., and 2001). The nature of this be a developmental as the possible of a in (Koltunow et al., or a in Hieracium (Koltunow et al., and and or it be as the in for 2001). of the are yet sexual of the or are (Asker and Jerling, 1992). The for this remains It however, a a of current research is the of apomixis into have been have that the of apomixis be only in with a et al., 2001). Because have been (Asker and Jerling, and et al., et al., to be for the of the apomixis. In however, asexual seed formation was the of apomixis in systems its of this from et al., and and in which in are known to and the of different there are of apomixis being in sexual plants et al., 2001). there is some in cases about the of the plants used were sexual of et al., 2001). the has been by a sexual plant was the of an apomictic of has been in a of plants, and apomixis is in the also is a among and the of and is to have in in and 2001; et al., 2001a). The of inheritance in however, also the of or in plants et al., that a of and to the of events of and in only to apomixis but also to developmental as and a of the with that there are between apomixis and that between has been a in the formation of apomictic and that different of apomixis and phenomena are all of a model on the of a of this is and it be used to apomixis in species, are to be et a on that be the in this and the of reproductive all are of There is growing for the of in apomictic species, and it is involved in the inheritance of apomixis in the and et al., and et a seed for reproductive with and found that apomictic and plants had a higher sexual The to be for apomictic Hieracium and by was by et a by which the of apomictic and We have that at of are in Hieracium species, but the relative of in sexual and apomictic has been established and Therefore, the of be the of asexual seed formation its and this have to the of observation and however, the that sexual should have asexual and sexual reproduction is to the of between of a and is to et al., 2003). It also has been that the inheritance of apomixis be by the of a or to the of this the of apomixis in a but of the a the of an are in providing an for this to a in the of that in a apomixis be only a were by plants, but all were observation to that the a when in form in the have been for et al., and et al., et al., There are however, in which there to be a with the of apomixis. In for a of apomixis et al., in this apomictic be but this to be at the level of the the there is growing that a of is to in a the formation of and the of are of the of a analogous to that is in (Asker and Jerling, 1992). have been among the of apomictic are to the of being which we to be a of the we a of of reproductive from both sexual and apomictic of that the from the a higher of and and We that in Hieracium at a is its and limits the of in the in and also the in apomixis the inheritance of at as in and and (van Dijk and in the of the by as a In this a the inheritance of only of a of apomixis, as without to the of in this The inheritance of apomixis the of an this but it also to an in the are in plants, and are involved in the formation of and 2000; et al., 2003). Therefore, in a similar to the of this be to the formation of and to process by The of the involved in apomixis to be in of the apomictic systems only a of have been to be for the inheritance of the trait. In a has been taken to the of the The and mapping in have been from in species, of which are of crops. The with the inheritance of apomixis in the to be no has been found in sexual et al., 1993, et al., 2001a). the was found in the apomictic relative also as a et al., 2001a). to this have its molecular were to with the without an that this be with a of the of to it that this of at in et al., and be the as et that the to a of a similar is with the relative an that were in with the with the inheritance of in this plant et al., et al., 2001). is also a of this to the involved in apomixis. of the of this are with but it to to a of the sexual et al., 2001a). also is being used in a The of apomixis in this plant is as a et al., 2001). are known for et the of with in and are to the use as and were in with the et al., all of the considerable with the in the with the inheritance of apomixis to a different of that et al., 2001a). et also the of to in and et similar for the systems progress is being the mapping of in (van Dijk et al., et al., and and There is some for with apomixis in and for in that similar with also in the is a and of but is to be or The of about with apomixis is it the of the mapping is in this to the that be by a but in a of and to the mapping It also should be that plants are sexual as and have and have of those of In mapping is in a or the with apomixis are and of a is be to that the are from the this the in and be an but it is also with the of of to to be involved in mapping et that of to apomixis be to the of with a accumulated the of apomixis. The of about the of in and is known of the molecular of apomixis that the essential be were the nature of the are to be as as (Koltunow and Grossniklaus, 2003). of plants be of is yet to this are et al., 2001). In light of the strategies to involved in apomixis are being on a be to and apomictic from the has been used to from into an apomictic the of which be for et al., on the of also was in Hieracium the of