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American Society of Plant Biologists
Patterns of Gene Expression in ApomixisNews and Reviews Editor neckardt{at}aspb.org
Many plants have the curious and fascinating ability to produce seeds asexually. In this process, known as apomixis, female gametes develop without meiosis (or with abnormal meiosis) and embryos develop without fertilization. Apomixis occurs in many wild species and in a few agronomically important species such as citrus and mango, but not in any of the major cereal crops. Because it offers the promise of the fixation and indefinite propagation of a desired genotype, there is a great deal of interest in engineering this ability to produce clonal seeds into crops, especially cereals (Spillane et al., 2001
Although it is a complex process, apomixis often is inherited as a simple Mendelian trait, which may suggest that it is controlled by relatively few "master" regulatory genes. It is thought that apomixis may have evolved (probably multiple times) through modifications of the normal sexual reproduction pathway, rather than constituting a novel pathway distinct from sexual reproduction (Grimanelli et al., 2001
Sexual reproduction in diploid angiosperms is characterized by double fertilization. After meiosis and the production of haploid sperm and egg cells within the anthers and ovules, respectively, two male sperm (released from a single pollen grain) enter the female gametophyte (embryo sac); one fuses with the egg cell to produce the diploid embryo, and the other fuses with two central cell nuclei to form the triploid endosperm tissue. In the female ovule, meiosis within the megaspore mother cell produces four haploid megaspores, three of which disintegrate soon thereafter and only one of which (the functional megaspore or "selected spore") enlarges to form the embryo sac. During apomixis, meiosis is circumvented and an embryo develops in the absence of fertilization.
Apomixis in Hieracium initiates with aposporous embryo sac formation, meaning that an embryo sac structure develops from a somatic cell (aposporous initial cell) within the ovule, completely bypassing meiosis, and then both endosperm and embryo develop autonomously without fertilization (Koltunow et al., 1998
Apomixis does not occur in Arabidopsis (although it is known among some species of the closely related genus Arabis). Nonetheless, it is apparent that there is a great deal to be learned about the molecular mechanisms involved in apomixis from our best-characterized plant genetics model system. Chaudhury and Peacock (1993)
To examine the molecular relationships between sexual and apomictic pathways, Tucker et al. used fusion constructs of
SPL is required for both male and female sporogenesis in Arabidopsis (Yang et al., 1999  ). In sexual Hieracium, AtSPL:GUS expression was localized specifically to developing anthers and ovules, and within the ovule it was restricted to the megaspore mother cell. Expression declined subsequently and was absent during functional megaspore selection, in contrast to that in Arabidopsis, in which AtSPL:GUS activity continued to mark later events of megasporogenesis (although expression was absent from functional megaspores in Arabidopsis and Hieracium). The ovules of apomictic Hieracium produce cytologically distinguishable megaspore mother cells, megaspores, and aposporous initials. When an aposporous initial cell is formed, adjacent megaspores subsequently degenerate, and the aposporous initial cell enlarges, divides, and proceeds through apomictic embryo and endosperm development. Interestingly, Tucker et al. found that, in apomictic Hieracium ovules, AtSPL:GUS was expressed in megaspore mother cells but not in aposporous initial cells. This result provides molecular evidence for the idea that aposporous initial cells develop from somatic cells within the ovule and do not share identity with megaspore mother cells. A positive marker for aposporous initial cells might reveal more about the early events surrounding the initiation of these cells and how they control the fate of megaspore mother cells.
The FIS-class genes are important regulators of endosperm development in Arabidopsis (Chaudhury et al., 2001 ). Mutations in MEA/FIS1, FIS2, or FIE/FIS3 all result in the initiation of fertilization-independent endosperm development. After fertilization, developing embryos of these mutants are aborted (and embryo development is not initiated in the absence of fertilization). Thus, the FIS-class genes play an important role in coordinating endosperm and embryo development during sexual reproduction, and homologs of these genes might be expected to play an important role in apomixis, although this remains to be tested (reviewed by Grossniklaus et al., 2001). MEA and FIE encode proteins similar to Polycomb group proteins in Drosophila, which form multimeric complexes that regulate gene expression via effects on chromatin structure. FIS2 encodes a Zn-finger protein that is homologous with Su(z)12, which is a component of Polycomb chromatin-remodeling complexes in human and Drosophila (Chaudhury et al., 2001). Tucker et al. found that the expression patterns of AtMEA:GUS, AtFIS2:GUS, and AtFIE:GUS were similar, but not identical, in transgenic Arabidopsis relative to sexual Hieracium. Expression of the three genes was associated primarily with the maturing embryo and later stages of endosperm development. In both sexual Hieracium and Arabidopsis, the expression of AtFIS2:GUS appeared in the functional megaspore (located at the chalazal end of the ovule) after the initiation of nuclear division: in Hieracium, as soon as the nucleus began to divide, and in Arabidopsis, slightly later, during maturation of the embryo sac at the eight-nuclei stage. However, in marked contrast to Arabidopsis, expression of AtFIS2:GUS in sexual Hieracium also was observed after meiosis in the three megaspores destined to degenerate at the micropylar end of the ovule, before the appearance of GUS activity in the functional chalazal megaspore. And in contrast to sexual Hieracium, AtFIS2:GUS expression was observed in all four megaspores and in the cell layer enveloping them in apomictic Hieracium plants, all of which were destined for degeneration. Expression was completely absent from aposporous initial cells until their first nuclear division, similar to the pattern observed for functional chalazal megaspores in sexual plants. These observations suggest that FIS genes play a slightly different role in Hieracium relative to Arabidopsis, a role that could be related to the capacity for apomixis and autonomous seed development in Hieracium. The expression patterns of FIS and SPL markers in Hieracium and Arabidopsis support the notion that aposporous initial cells do not share identity with megaspore mother cells but they subsequently assume the identity of the functional megaspore. The similarity of expression patterns of the AtFIS:GUS marker genes, and of the additional marker AtSERK1:GUS, at later stages of ovule and seed development in sexual and apomictic Hieracium suggests that sexual and apomictic pathways share common molecular regulatory features and are not distinct pathways. These results support that idea that the apomictic developmental program is comparable to sexual development except for two specific switch points, meiosis and fertilization. These observations have potentially important implications for the engineering of apomixis in crop species, suggesting that barriers to apomixis occur very early in embryo sac development. If these barriers can be overcome, the later stages of embryo and endosperm development might be expected to proceed as normal. An important question is whether these programs are fixed or have flexibility under particular influences, which might be examined by further use of these and additional reproductive molecular markers.
One of the critical barriers to apomixis in cereal crops is a strict requirement for the maintenance of a 2:1 ratio of maternal-to-paternal genomes in endosperm tissue. In many plants, and most cereal crops, deviations from this 2:1 ratio leads to seed abortion (Birchler, 1993
Birchler, J. (1993). Dosage analysis of maize endosperm development. Annu. Rev. Genet. 27, 181–204.[CrossRef][Web of Science][Medline] Chaudhury, A.M., Koltunow, A.M., Payne, T., Luo, M., Tucker, M.R., Dennis, E.S., and Peacock, W.J. (2001). Control of early seed development. Annu. Rev. Cell Dev. Biol. 17, 677–691.[CrossRef][Web of Science][Medline] Chaudhury, A.M., and Peacock, J.W. (1993). Approaches to isolating apomictic mutants in Arabidopsis thaliana: Prospects and progress. In Apomixis: Exploiting Hybrid Vigor in Rice, G.S. Khush, ed (Manila, The Philippines: International Rice Research Institute), pp. 66–71. Grimanelli, D., Leblanc, O., Perotti, E., and Grossniklaus, U. (2001). Developmental genetics of gametophytic apomixis. Trends Genet. 17, 597–604.[CrossRef][Web of Science][Medline] Grossniklaus, U., Spillane, C., Page, D.R., and Köhler, C. (2001). Genomic imprinting and seed development: Endosperm formation with and without sex. Curr. Opin. Plant Biol. 4, 21–27.[CrossRef][Web of Science][Medline]
Hecht, V., Vielle-Calzada, J.-P., Harog, M.V., Schmidt, E.D., Boutilier, K., Grossniklaus, U., and de Vries, S.C. (2001). The Arabidopsis SOMATIC EMBRYOGENESIS RECEPTOR KINASE 1 gene is expressed in developing ovules and embryos and enhances embryogenic competence in culture. Plant Physiol. 127, 803–816. Koltunow, A., and Grossniklaus, U. (2003). Apomixis: A developmental perspective. Annu. Rev. Plant Biol. 54, 547–574.[CrossRef][Medline] Koltunow, A., Johnson, S.D., and Bicknell, R.A. (1998). Sexual and apomictic development in Hieracium. Sex. Plant Reprod. 11, 213–230.[CrossRef]
Luo, M., Bilodeau, P., Dennis, E.S., Peacock, W.J., and Chaudhury, A. (2000). Expression and parent-of-origin effects for FIS2, MEA, and FIE in the endosperm and embryo of developing Arabidopsis seeds. Proc. Natl. Acad. Sci. USA 97, 10637–10642.
Ohad, N., Margossian, L., Hsu, Y.C., Williams, C., Repetti, P., and Fischer, R.L. (1996). A mutation that allows endosperm development without fertilization. Proc. Natl. Acad. Sci. USA 93, 5319–5324.
Schiefthaler, U., Balasubramanian, S., Sieber, P., Chevalier, D., Wisman, E., and Schneitz, K. (1999). Molecular analysis of NOZZLE, a gene involved in pattern formation and early sporogenesis during sex organ development in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 96, 11664–11669. Spillane, C., Steimer, A., and Grossniklaus, U. (2001). Apomixis in agriculture: The quest for clonal seeds. Sex. Plant Reprod. 14, 179–187.
Tucker, M.R., Araujo, A.G., Paech, N.A., Hecht, V., Schmidt, E.D.L., Rossell, J.-B., de Vries, S.C., and Koltunow, A.M.G. (2003). Sexual and apomictic reproduction in Hieracium subgenus Pilosella are closely interrelated developmental pathways. Plant Cell 15, 1524–1537.
Yang, W.C., Ye, D., Xu, J., and Sundaresan, V. (1999). The SPOROCYTELESS gene of Arabidopsis is required for initiation of sporogenesis and encodes a novel nuclear protein. Genes Dev. 13, 2108–2117. This article has been cited by other articles:
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APOMICTIC DEVELOPMENT
ORIGIN OF THE EMBRYO...
-glucuronidase (GUS) with a variety of Arabidopsis genes (promoter:GUS or chimeric protein fusion constructs) that are associated with different aspects of sexual reproduction in this species. These markers were introduced into sexual and apomictic Hieracium plants, and their expression patterns were monitored during ovule and seed development. The same constructs also were introduced into Arabidopsis for a comparison with sexual Hieracium. The Arabidopsis marker sequences used were from SPOROCYTELESS (SPL)/NOZZLE, which is required for male and female sporogenesis in Arabidopsis (Schiefthaler et al., 1999
