IN THIS ISSUE

Planned Parenthood in Arabidopsis: FLOWERING LOCUS C

"Ontogeny recapitulates phylogeny" goes the line that persists in folkloric fashion in academic biology, most likely because it is so much fun to say. The saying is no longer taken literally by scientists who value their reputation, and Ernst Haeckel, the nineteenth-century German zoologist who first coined the phrase, has been widely discredited for having manipulated anatomical drawings so as to support the curious notion that higher animals pass through developmental stages in which they resemble their phylogenetic forerunners. Haeckel thus espoused a view of evolution as the successive addition of novel adult developmental stages onto existing programs of development. Popular notions that human fetuses transiently possess gill slits and tails are some of the more prominent myths that this view has perpetuated to the present day.

However odd Haeckel's views might seem upon objective consideration, the heuristic impact of comparative development, the field of biology that he represented, has been enormous in guiding evolutionist inquiries. The embryonic development of the human, for instance, rather than tracing a phylogenetic course from single cell to fish to ape to infant, instead reflects the unique orchestration of a genetic program that has arisen slowly through evolutionary events that are often, but not always, subtle. Indeed, the often-quoted estimation that the human genome is 98% similar to that of the chimpanzee stresses that, genetically speaking, it's not merely what you have that counts, but how—and when—you use it. Thus, mutations in key regulatory functions, and thereby in the chronology of genetic programs, often seem to have driven speciation. Evolutionists refer to such mutations, which arise so as to alter some prior "default" schedule of development, as heterochronic.

Heterochronic mutations are important phenomena not only within the grand evolutionary context, but are also valued for the information they can provide within the context of the life cycle of the given organism. The subject of developmental biology at the molecular level is, ultimately, those same key regulatory functions that have been crucial during phylogenetic development. This is not to say, as Haeckel did, that the elaboration of developmental biology is tantamount to a description of evolution itself. Nevertheless, the complexities of evolution and organismal development alike pose enormous conceptual challenges that are likely to be resolved in identifying common, key genetic processes. To the extent that Haeckel pointed the way to an underlying link between evolutionary processes and organismal development, it is perhaps fitting that his phrase, odd as it is catchy, lives on.

The terms ontogeny and phylogeny are as familiar in plant biology as they are in zoology. The fossil record speaks to the evolution of angiosperms just as it does to the evolution of vertebrates, and issues of developmental biology are the very focus of agriculture as well as basic botany. Like animal species, plants can undergo heterochronic mutations, whereby the onset of discrete developmental stages becomes either precocious or retarded, as well as homeotic mutations, such that entire organ morphologies are altered. Both types of mutation, which are developmental by definition, have also been implicated in evolutionary processes of plants just as they have been in animal evolution. (For a review of plant evolution, see Doebley and Lukens, 1999.)

Two research groups have recently presented their findings on heterochronic mutations in the reproductive life of Arabidopsis in THE PLANT CELL. Following the report of Sheldon et al. 1999 in the March issue, Michaels and Amasino, on pages 949–956 of this issue, give an account of their pursuit of a gene that is central to the timing of flowering in Arabidopsis, and thus to the very developmental process that defines angiosperms as a taxon. As might be expected a priori, such a broadly definitive process proves to be highly complex. In Arabidopsis, for instance, approximately 80 separate loci have already been discovered to affect flowering time alone, and functional analysis of many of the pertinent genes has allowed the identification of four distinct pathways of flowering (see Levy and Dean 1998 ). This complexity undoubtedly reflects the application of selective pressures to life forms literally rooted within their environment throughout their evolutionary span and also bespeaks the application of such pressures directly to the reproductive phase of the life cycle. Correspondingly, the four pathways of flowering can be designated in terms of mediating either environmental cues (i.e., the photoperiodic and vernalization promotion pathways) or inherent developmental signals (i.e., the autonomous promotion and floral repression pathways). The former pathways promote flowering in response to day length and decreased temperature, respectively, whereas the latter pathways promote and repress flowering in response to endogenous signals such as gibberellins and reduced sucrose levels, respectively.

Given the intricacies outlined above, the mechanisms whereby various cues of flowering are integrated so as to ensure reproductive success are of particular interest, and it is in this regard that Michaels and Amasino's update on the FLOWERING LOCUS C gene (FLC) is important. FLC was first identified not as the consequence of an induced mutation per se, but rather as one of two heterochronic loci occurring naturally in late-flowering ecotypes of Arabidopsis that segregated independently upon appropriate introgressive crosses into early-flowering backgrounds (Koornneef et al. 1994 ; Lee et al. 1994 ). The second of the two loci had been previously designated as FRIGIDA (FRI; Clarke and Dean 1994 ) and is now confirmed by Michaels and Amasino to be epistatic with respect to FLC. Specifically, the authors show that FLC transcripts are present only in the presence of a functional FRI gene. Especially noteworthy in this regard is the finding that exposure to decreased temperature, the environmental (vernalization) cue that is required for early flowering by plants that harbor the FRI gene, prevents transcription of FLC. The additional demonstration that FLC goes untranscribed in fri plants possessing the LUMINIDEPENDENS gene (LD; i.e., a gene of the autonomous promotion pathway) further underscores the centrality of FLC. Together, these observations identify FLC as a point of integration of environmental and endogenous flowering pathways.

Such transcript analyses are, of course, experimentally predicated on the fact that the authors have successfully cloned FLC, a feat that also enables them to define FLC as a repressor of Arabidopsis reproductive development, inasmuch as null flc mutants flower early. Furthermore, the predicted FLC protein turns out to contain a MADS domain, the DNA binding motif characteristic of several homeotic transcription factors involved in floral development (Purugganan et al. 1995 ). The account of Michaels and Amasino in this issue thus dovetails nicely with the research article of Sheldon et al. 1999 , appearing in the March issue, who isolated a late-flowering T-DNA–tagged mutant that they called flf (Sheldon et al. 1999 ). Noting that the FLF MADS box gene that they subsequently cloned is expressed in an FRI-dependent manner and maps to chromosome 5, very near to the FLC locus, the Australian group closed their report in March with a consideration of the likelihood that their FLF locus might be one and the same with the previously identified FLC. They need wonder no longer; FLF will hereafter be referred to as FLC.

The careful experimentation of Sheldon et al. resulted in a picture of the flowering program surrounding FLC that is very similar to the account given in this issue. In particular, overexpression data provided by Sheldon et al. documented the relationship of increasing FLC transcripts to retardation in flowering. The Australian group also stressed the centrality of the locus to the multiple pathways of flowering through their demonstration that, in addition to ld mutations, lesions at other vernalization-responsive loci result in upregulation of FLC; both research groups also report that FLC expression levels are refractory with respect to the photo-periodic promotion pathway.

To address integration of FLC into the endogenous pathways of flowering, Sheldon et al. made the intriguing claim that flc mutants are less responsive to the flower-inducing effects of gibberellin relative to the FLC wild type. What other chemical and macromolecular signals may bear upon FLC in its role as a putative transcription factor and repressor of flowering is an important question that, with the definitive cloning of the FLC gene, can now be pursued. It is apparent that the full complexity of the flowering pathways in Arabidopsis has yet to be appreciated. Nevertheless, the models elaborated by Michaels and Amasino as well as Sheldon et al. with regard to the FLC gene reflect concrete facts of the sort that we can look forward to seeing encompass additional branches of flowering pathways in the years to come.

REFERENCES

Clarke, J.H., and Dean, C. (1994) Mapping FRI, a locus controlling flowering time and vernalization response in Arabidopsis thaliana.. Mol. Gen. Genet. 242:81-89[CrossRef][ISI][Medline].

Doebley, J., and Lukens, L. (1998) Transcriptional regulators and the evolution of plant form. Plant Cell 10:1075-1082[Free Full Text].

Koornneef, M., Blankenstihn-de Vries, H., Hanhart, C., Soppe, W., and Peeters, T. (1994) The phenotype of some late-flowering mutants is enhanced by a locus on chromosome 5 that is not effective in the Landsberg erecta wild type. Plant J. 6:911-919[CrossRef][ISI].

Lee, I., Michaels, S.D., Masshardt, A.S., and Amasino, R.M. (1994) The late-flowering phenotype of FRIGIDA and mutations in LUMINIDEPENDENS is suppressed in the Landsberg erecta strain of Arabidopsis. Plant J. 6:903-909[CrossRef][ISI].

Levy, Y.Y., and Dean, C. (1998) The transition to flowering. Plant Cell 10:1973-1989[Free Full Text].

Michaels, S.D., and Amasino, R.M. (1999) FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repres-sor of flowering. Plant Cell 11:949-956[Abstract/Free Full Text].

Purugganan, M.D., Rounsley, S.D., Schmidt, R.J., and Yanofsky, M.F. (1995) Molecular evolution of flower development: Diversification of the plant MADS-box regulatory gene family. Genetics 140:345-356[Abstract].

Sheldon, C.S., Burn, J.E., Perez, P.P., Metzger, J., Edwards, J.A., Peacock, W.J., and Dennis, E.S. (1999) The FLF MADS box gene: A repressor of flowering in Arabidopsis regulated by vernalization and methylation. Plant Cell 11:445-458[Abstract/Free Full Text].

Related articles in Plant Cell:

FLOWERING LOCUS C Encodes a Novel MADS Domain Protein That Acts as a Repressor of Flowering

Scott D. Michaels and Richard M. Amasino
Plant Cell 1999 11: 949-956. [Abstract] [Full Text]  

This Article Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Email this article to a friend Related articles in Plant Cell Similar articles in this journal Similar articles in ISI Web of Science Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via CrossRef Citing Articles via Google Scholar Google Scholar Articles by Smith, H. B. Search for Related Content PubMed PubMed Citation Articles by Smith, H. B. Agricola Articles by Smith, H. B.