Abstract
Understanding the interrelationship between the phylogeny of developmental control genes and the evolution of morphological features is a central goal of evolutionary developmental biology (evo-devo). It requires that one distinguishes properly between gene genealogy and function. Gene duplication, gene loss and speciation in combination with differential changes in gene function can generate complex evolutionary scenarios that require additional terms beyond homology for a proper description. Use and possible misuse of these terms, including “orthology”, “paralogy” and “subfunctionalization”, is exemplifed withAGAMOUS-like genes encoding transcription factors involved in flower and fruit development. This MADS-box gene subfamily demonstrates that homologous genes in different species with (almost) indentical functions can be paralogues rather than orthologues, corroborating that functional similarity of genes is not a valid criterion for orthology. Homeosis fails some tests of homology, but might be of greater evolutionary importance than previously assumed, justifying yet another term, “homocracy”. It describes organs that share the expression of the same patterning genes, irrespective of the homology of these organs. All in all this article opts for a careful use of a limited and well-chosen set of terms describing gene relationships and function, rather than the inflationary production of novel terms that may seem to be precise, but whose obscurity hampers communication.
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Abouheif, E., Akam, M., Dickinson, W.J., Holland, P.W.H., Meyer, A., Patel, N.H., Raff, R.A., Roth, V.L., Wray, G.A., 1997. Homology and developmental gens. Trends Genet. 13, 432–433.
Allen, K.D., 2002. Assying gene content inArabidopsis. Proc. Natl. Acad. Sci. USA 99, 9568–9572.
Bateman, R.M., DiMichele, W.A., 2002. Generating and filtering major phenotypic novelties: neoGoldschmidtian saltation revisited. In: Cronk, Q.C.B., Bateman, R.M., Hawkins, J.A. (Eds.), Developmental Genetics and Plant Evolution. Taylor & Francis, London, pp. 109–159.
Baum, D.A., Donoghue, M.J., 2002. Transference of function, heterotopy and the evolution of plant development. In: Cronk, Q.C.B., Bateman, R.M., Hawkins, J.A. (Eds.), Developmental Genetics and Plant Evolution. Taylor & Francis, London, pp. 52–69.
Becker, A., Theißen, G., 2003. The major clades of MADS-box genes and their role in the development and evolution of flowering plants. Mol. Phys. Evol. 29, 464–489.
Bolker, J.A., Raff, R.A., 1996. Developmental genetics and traditional homology. Bioessays 18, 489–494.
Bradley, D., Carpenter, R., Sommer, H., Hartley, N., Coen, E., 1993. Complementary floral homeotic phenotypes result from opposite orientations of a transposon at the Plena-locus ofAntirrhinum. Cell 72, 85–95.
Butler, A.B., Saidel, W.M., 2000. Defining sameness: historical, biological, and generative homology. Bioessays 22, 846–853.
Davies, B., Motte, P., Peck, E., Saedler, H., Sommer, H., Schwarz-Sommer, Z., 1999.PLENA andFARINELLI: redundancy and regulatory interaction between twoAntirrhinum MADS-box factors controlling flower development. EMBO J 18, 4023–4034.
Dickinson, W.J., 1995. Molecules and morphology: where’s the homology? Trends Genet. 11, 119–121.
Egel, R., 2000. How ‘homology’ entered genetics. Trends Genet. 16, 437–439.
Fitch, W.M., 1970. Distinguishing homologous from analogous proteins. Syst. Zool. 19, 99–113.
Fitch, W.M., 2000. Homology—a personal view on some of the problems. Trends Genet. 16, 227–231.
Force, A., Lynch, M., Pickett, F.B., Amores, A., Yan, Y.-I., Postlethwait, J., 1999. Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151, 1531–1545.
Gogarten, J.P., Olendzenski, L., 1999. Orthologs, paralogs and genome comparisons. Curr. Opin. Genet. Dev. 9, 630–636.
Kanno, A., Saeki, H., Kameya, T., Saedler, H., Theissen, G., 2003. Heterotopic expression of class B floral homeotic genes supports a modified ABC model for tulip (Tulipa gesneriana). Plant Mol. Biol. 52, 831–841.
Kramer, E.M., Di Stilio, V.S., Schluter, P.M., 2003. Complex patterns of gene duplication in the APETALA3 and PISTILLATA lineages of the Ranunculaceae. Intern. J. Plant Sci. 164, 1–11.
Kramer, E.M., Jaramillo, M.A., Di Stilio, V.S., 2004. Patterns of gene duplication and functional evolution during the diversification of the AGAMOUS subfamily of MADS box genes in angiosperms. Genetics 166, 1011–1023.
Krizek, B.A., Meyerowitz, E.M., 1996. The Arabidopsis homeotic genes APETALA3 and PISTILLATA are sufficient to provide the B class organ identity function. Development 122, 11–22.
Lewis, E.B., 1994. Homeosis: the first 100 years. Trends Genet. 10, 341–343.
Liljegren, S.J., Ditta, G.S., Eshed, Y., Savidge, B., Bowman, J.L., Yanofsky, M.F., 2000.SHATTER-PROOF MADS-box genes control seed dispersal inArabidopsis. Nature 404, 766–770.
Mindell, D.P., Meyer, A., 2001. Homology evolving. Trends Ecol. Evol. 16, 434–440.
Nielsen, C., Martinez, P., 2003. Patterns of gene expression: homology or homocracy? Dev. Genes Evol. 213, 149–154.
Ohno, S., 1970. Evolution by Gene Duplication. Springer, Berlin.
Ohta, T., 1980. Evolution and Variation of Multigene Families, Lecture Notes in Biomathematics, vol. 37. Springer, Berlin.
Ouzounis, C., 1999. Orthology: another terminology muddle. Trends Genet. 15, 445.
Patterson, C., 1988. Homology in classical and molecular biology. Mol. Biol. Evol. 5, 603–625.
Prince, V.E., Pickett, F.B., 2002. Splitting pairs: the diverging fates of duplicate genes. Nat. Rev. Genet. 3, 827–837.
Riedl, R., 1977. A systems-analytical approach to macro-evolutionary phenomena. Quart. Rev. Biol. 52, 351–370.
Ronse De Craene, L.P. 2003. The evolutionary significance of homeosis in flowers: a morphological perspective. Int. J. Plant Sci. 164, S225-S235.
Rutishauser, R., Isler, B., 2001. Developmental genetics and morphological evolution of flowering plants, especially bladderworts (Utricularia): fuzzy Arberian morphology complements classical morphology. Ann. Bot. 88, 1173–1202.
Sattler, R., 1994. Homology, homeosis, and process morphology in plants. In: Hall, B.K. (Ed.), The Hierarchical Basis of Comparative Biology. Academic Press, New York, pp. 423–475.
Sonnhammer, E.L.L., Koonin, E.V., 2002. Orthology, paralogy and proposed classification for paralog subtypes. Trends Genet. 18, 619–620.
Svensson, M.E., 2004. Homology and homocracy revisited: gene expression patterns and hypotheses of homology. Dev. Genes Evol. 214, 418–421.
Tautz, D., 1998. Debatable homologies. Nature 395, 17–19.
Theißen, G., 2000. Shattering developments. Nature 404, 711–713.
Theißen, G., 2002. Orthology: secret life of genes. Nature 415, 741.
Theißen, G., Kim, J., Saedler, H., 1996. Classification and phylogeny of the MADS-box multigene family suggest defined roles of MADS-box gene subfamilies in the morphological evolution of eukaryotes. J. Mol. Evol. 43, 484–516.
Theißen, G., Becker, A., Di Rosa, A., Kanno, A., Kim, J.T., Münster, T., Winter, K.-U., Saedler, H., 2000. A short history of MADS-box genes in plants. Plant Mol. Biol. 42, 115–149.
Theißen, G., Becker, A., Kirchner, C., Münster, T., Winter, K.-U., Saedler, H., 2002. How land plants learned their floral ABCs: the role of MADS-box genes in the evolutionary origin of flowers. In: Cronk, Q.C.B., Bateman, R.M., Hawkins, J.A. (Eds.), Developmental Genetics and Plant Evolution. Taylor & Francis, London, pp. 173–205.
Wagner, G.P., Laubichler, M.D., 2004. Rupert Riedl and the re-synthesis of evolutionary and developmental biology: body plan and evolvability. J. Exp. Zool. (Mol. Dev. Evol.) 302B, 92–102.
Wray, G.A., Abouheif, E., 1998. When is homology not homology? Curr. Opin. Genet. Dev. 8, 675–680.
Yanofsky, M.F., Ma, H., Bowman, J.L., Drews, G.N., Feldman, K.A., Meyerowitz, E.M., 1990. The protein encoded by theArabidopsis homeotic geneAGAMOUS resembles transcription factors. Nature 346, 35–39.
Zahn, L.M., Leebens-Mack, J., Arrington, J.A., Hu, Y., Landherr, L., dePamphilis, C., Becker, A., Theissen, G., Ma, H., 2005. Conservation and divergence in theAGAMOUS subfamily of MADS-box genes: evidence of independent sub- and neofunctionalization events. Evol. Dev. in press.
Zardoya, R., Abouheif, E., Meyer, A., 1996. Evolution and orthology ofhedgehog genes. Trends Genet. 12, 496–497.
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From the 46th “Phylogenetisches Symposium”, Jena, Germany, November 20–21, 2004. Theme of the symposium: “Evolutionary developmental biology-new challenges to the homology concept?”.
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Theißen, G. Birth, life and death of developmental control genes: New challenges for the homology concept. Theory Biosci. 124, 199–212 (2005). https://doi.org/10.1007/BF02814484
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DOI: https://doi.org/10.1007/BF02814484