Abstract
The growth of land plants depends on stem cell-containing meristems which show major differences in their architecture from basal to higher plant species. In Arabidopsis, the stem cell niches in the shoot and root meristems are promoted by WUSCHEL (WUS) and WOX5, respectively. Both genes are members of a non-ancestral clade of the WUS-related homeobox (WOX) gene family, which is absent in extant bryophytes and lycophytes. Our analyses of five fern species suggest that a single WUS orthologue was present in the last common ancestor (LCA) of leptosporangiate ferns and seed plants. In the extant fern Ceratopteris richardii, the WUS pro-orthologue marks the pluripotent cell fate of immediate descendants of the root apical initial, so-called merophytes, which undergo a series of stereotypic cell divisions and give rise to all cell types of the root except the root cap. The invention of a WUS-like function within the WOX gene family in an ancestor of leptosporangiate ferns and seed plants and its amplification and sub-functionalisation to different stem cell niches might relate to the success of seed plants, especially angiosperms.
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References
Bordoli L, Kiefer F, Arnold K, Benkert P, Battey J, Schwede T (2009) Protein structure homology modeling using SWISS-MODEL workspace. Nat Protoc 4:1–13
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 of Antirrhinum. Cell 72:85–95
Brand U, Fletcher JC, Hobe M, Meyerowitz EM, Simon R (2000) Dependence of stem cell fate in Arabidopsis on a feedback loop regulated by CLV3 activity. Science 289:617–619
Breuninger H, Rikirsch E, Hermann M, Ueda M, Laux T (2008) Differential expression of WOX genes mediates apical-basal axis formation in the Arabidopsis embryo. Dev Cell 14:867–876
Deveaux Y, Toffano-Nioche C, Claisse G, Thareau V, Morin H, Laufs P, Moreau H, Kreis M, Lecharny A (2008) Genes of the most conserved WOX clade in plants affect root and flower development in Arabidopsis. BMC Evol Biol 8:291
Evans MM, Barton MK (1997) Genetics of angiosperm shoot apical meristem development. Annu Rev Plant Physiol Plant Mol Biol 48:673–701
Gehring WJ, Muller M, Affolter M, Percival-Smith A, Billeter M, Qian YQ, Otting G, Wuthrich K (1990) The structure of the homeodomain and its functional implications. Trends Genet 6:323–329
Haecker A, Gross-Hardt R, Geiges B, Sarkar A, Breuninger H, Herrmann M, Laux T (2004) Expression dynamics of WOX genes mark cell fate decisions during early embryonic patterning in A. thaliana. Development 131:657–668
Hirakawa Y, Kondo Y, Fukuda H (2010) TDIF peptide signaling regulates vascular stem cell proliferation via the WOX4 homeobox gene in Arabidopsis. Plant Cell 22:2618–2629
Hou GC, Hill JP (2002) Heteroblastic Root Development in Ceratopteris richardii (Parkeriaceae). Int J Plant Sci 163:341–351
Hou GC, Hill JP (2004) Developmental anatomy of the fifth shoot-borne root in young sporophytes of Ceratopteris richardii. Planta 219:212–220
Hovde S, Abate-Shen C, Geiger JH (2001) Crystal structure of the Msx-1 homeodomain/DNA complex. Biochemistry 40:12013–12021
Ikeda M, Mitsuda N, Ohme-Takagi M (2009) Arabidopsis WUSCHEL is a bifunctional transcription factor that acts as a repressor in stem cell regulation and as an activator in floral patterning. Plant Cell 21:3493–3505
Jackson D (1991) In situ hybridization in plants. In: Bowles DJ, Gurr SJ, McPerson M (eds) Molecular Plant pathology: a practical approach. Oxford University Press, Oxford, pp 163–174
Kieffer M, Stern Y, Cook H, Clerici M, Maulbetsch C, Laux T, Davies B (2006) Analysis of the transcription factor WUSCHEL and its functional homologue in Antirrhinum reveals a potential mechanism for their roles in meristem maintenance. Plant Cell 18:560–573
Kissinger CR, Liu BS, Martin-Blanco E, Kornberg TB, Pabo CO (1990) Crystal structure of an engrailed homeodomain-DNA complex at 2.8 A resolution: a framework for understanding homeodomain-DNA interactions. Cell 63:579–590
Lau S, Ehrismann JS, Schlereth A, Takada S, Mayer U, Jürgens G (2010) Cell-cell communication in Arabidopsis early embryogenesis. Eur J Cell Biol 89:225–230
Mayer KF, Schoof H, Haecker A, Lenhard M, Jürgens G, Laux T (1998) Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem. Cell 95:805–815
Nardmann J, Werr W (2006) The shoot stem cell niche in angiosperms: expression patterns of WUS orthologues in rice and maize imply major modifications in the course of mono- and dicot evolution. Mol Biol Evol 23:2492–2504
Nardmann J, Reisewitz P, Werr W (2009) Discrete shoot and root stem cell-promoting WUS/WOX5 functions are an evolutionary innovation of angiosperms. Mol Biol Evol 26:1745–1755
Pryer KM, Schneider H, Smith AR, Cranfill R, Wolf PG, Hunt JS, Sipes SD (2001) Horsetails and ferns are a monophyletic group and the closest living relatives to seed plants. Nature 409:618–622
Rothwell GW, Nixon KC (2006) How does the inclusion of fossil data change our conclusions about the phylogenetic history of euphyllophytes? Int J Plant Sci 167:737–749
Sarkar AK, Luijten M, Miyashima S, Lenhard M, Hashimoto T, Nakajima K, Scheres B, Heidstra R, Laux T (2007) Conserved factors regulate signalling in A. thaliana shoot and root stem cell organizers. Nature 446:811–814
Schneider H, Schuettpelz E, Pryer KM, Cranfill R, Magallon S, Lupia R (2004) Ferns diversified in the shadow of angiosperms. Nature 428:480–481
Schoof H, Lenhard M, Haecker A, Mayer KF, Jürgens G, Laux T (2000) The stem cell population of Arabidopsis shoot meristems in maintained by a regulatory loop between the CLAVATA and WUSCHEL genes. Cell 100:635–644
Schott O, Billeter M, Leiting B, Wider G, Wuthrich K (1997) The NMR solution structure of the non-classical homeodomain from the rat liver LFB1/HNF1 transcription factor. J Mol Biol 267:673–683
Shimizu R, Ji J, Kelsey E, Ohtsu K, Schnable PS, Scanlon MJ (2009) Tissue specificity and evolution of meristematic WOX3 function. Plant Physiol 149:841–850
Stahl Y, Wink RH, Ingram GC, Simon R (2009) A signaling module controlling the stem cell niche in Arabidopsis root meristems. Curr Biol 19:909–914
Stout SC, Clark GB, Archer-Evans S, Roux SJ (2003) Rapid and efficient suppression of gene expression in a single-cell model system, Ceratopteris richardii. Plant Physiol 131:1165–1168
Sussex IM (1989) Developmental programming of the shoot meristem. Cell 56:225–229
Svingen T, Tonissen KF (2006) Hox transcription factors and their elusive mammalian gene targets. Heredity 97:88–96
van der Graaff E, Laux T, Rensing SA (2009) The WUS homeobox-containing (WOX) protein family. Genome Biol 10:248
Wang Y, Addess KJ, Chen J, Geer LY, He J, He S, Lu S, Madej T, Marchler-Bauer A, Thiessen PA, Zhang N, Bryant SH (2007) MMDB: annotating protein sequences with Entrez’s 3D-structure database. Nucleic Acids Res 35:D298–D300
Wu X, Dabi T, Weigel D (2005) Requirement of homeobox gene STIMPY/WOX9 for Arabidopsis meristem growth and maintenance. Curr Biol 15:436–440
Acknowledgments
We thank Dr. J. Chandler and Pascal Reisewitz for suggestions, stimulating discussions and critically reading the manuscript, Heike Shahbodaghi-Rückert for excellent technical assistance. We especially wish to thank Leslie Hickok for providing Ceratopteris richardii spores. This work was supported by the Deutsche Forschungsgemeinschaft through SFB 680 and grant WE 1262/7.
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Nardmann, J., Werr, W. The invention of WUS-like stem cell-promoting functions in plants predates leptosporangiate ferns. Plant Mol Biol 78, 123–134 (2012). https://doi.org/10.1007/s11103-011-9851-4
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DOI: https://doi.org/10.1007/s11103-011-9851-4