The invention of WUS-like stem cell-promoting functions in plants predates leptosporangiate ferns

Plant Molecular Biology

Volumn 78, Issue 1-2, 2012, Pages 123-134

  Nardmann, Judith ^a   Werr, Wolfgang ^a  

^a UNIVERSITY OF COLOGNE   (Germany)

Author keywords

Ceratopteris WUS orthologue; Meristem; Plant evolution; WOX phylogeny

Indexed keywords

ARABIDOPSIS PROTEIN; HOMEODOMAIN PROTEIN; VEGETABLE PROTEIN; WUSCHEL PROTEIN, ARABIDOPSIS;

AMINO ACID SEQUENCE; ARTICLE; CLASSIFICATION; CYTOLOGY; FERN; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; IN SITU HYBRIDIZATION; MERISTEM; METABOLISM; MOLECULAR EVOLUTION; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYLOGENY; PLANT; PLANT CELL; PLANT ROOT; PLANT STEM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE HOMOLOGY; SPECIES DIFFERENCE; STEM CELL; STEM CELL NICHE;

AMINO ACID SEQUENCE; ARABIDOPSIS PROTEINS; EVOLUTION, MOLECULAR; FERNS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, PLANT; HOMEODOMAIN PROTEINS; IN SITU HYBRIDIZATION; MERISTEM; MOLECULAR SEQUENCE DATA; PHYLOGENY; PLANT CELLS; PLANT PROTEINS; PLANT ROOTS; PLANT STEMS; PLANTS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEQUENCE HOMOLOGY, AMINO ACID; SPECIES SPECIFICITY; STEM CELL NICHE; STEM CELLS;

ARABIDOPSIS; BRYOPHYTA; BRYOPHYTES; CERATOPTERIS; CERATOPTERIS RICHARDII; EMBRYOPHYTA; FILICOPHYTA; LYCOPODIOPHYTA; MAGNOLIOPHYTA; SPERMATOPHYTA;

EID: 82755194998     PISSN: 01674412     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11103-011-9851-4     Document Type: Article

References (34)

1. 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.
2. 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.
3. 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.
4. 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.
5. 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.
6. Evans MM, Barton MK (1997) Genetics of angiosperm shoot apical meristem development. Annu Rev Plant Physiol Plant Mol Biol 48: 673-701.
7. 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.
8. 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.
9. 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.
10. Hou GC, Hill JP (2002) Heteroblastic Root Development in Ceratopteris richardii (Parkeriaceae). Int J Plant Sci 163: 341-351.
11. Hou GC, Hill JP (2004) Developmental anatomy of the fifth shoot-borne root in young sporophytes of Ceratopteris richardii. Planta 219: 212-220.
12. Hovde S, Abate-Shen C, Geiger JH (2001) Crystal structure of the Msx-1 homeodomain/DNA complex. Biochemistry 40: 12013-12021.
13. 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.
14. 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.
15. 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.
16. 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.
17. 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.
18. 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.
19. 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.
20. 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.
21. 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.
22. 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.
23. 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.
24. Schneider H, Schuettpelz E, Pryer KM, Cranfill R, Magallon S, Lupia R (2004) Ferns diversified in the shadow of angiosperms. Nature 428: 480-481.
25. 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.
26. 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.
27. 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.
28. 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.
29. 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.
30. Sussex IM (1989) Developmental programming of the shoot meristem. Cell 56: 225-229.
31. Svingen T, Tonissen KF (2006) Hox transcription factors and their elusive mammalian gene targets. Heredity 97: 88-96.
32. van der Graaff E, Laux T, Rensing SA (2009) The WUS homeobox-containing (WOX) protein family. Genome Biol 10: 248.
33. 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.
34. Wu X, Dabi T, Weigel D (2005) Requirement of homeobox gene STIMPY/WOX9 for Arabidopsis meristem growth and maintenance. Curr Biol 15: 436-440.