Summary
An EMS (ethyl methanesulfonate) mutagenesis effector screen performed with the STM:GUS marker line in Arabidopsis thaliana identified a loss-of-function allele of the TORNADO2 gene. The histological and genetic analyses described here implicate TRN2 in SAM function, where the peripheral zone in trn2 mutants is enlarged relative to the central stem cell zone. The trn2 mutant allele partially rescues the phenotype of shoot meristemless mutants but behaves additively to wuschel and clavata3 alleles during the vegetative phase and in the outer floral whorls. The development of carpels in trn2 wus-1 double mutant flowers indicates that pluripotent cells persist in floral meristems in the absence of TRN2 function and can be recruited for carpel anlagen. The data implicate a membrane-bound plant tetraspanin protein in cellular decisions in the peripheral zone of the SAM.
Similar content being viewed by others
References
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
Byrne ME, Simorowski J, Martienssen RA (2002) ASYMMETRIC LEAVES1 reveals knox gene redundancy in Arabidopsis. Development 129:1957–1965
Carland FM, McHale NA 1996. LOP1: a gene involved in auxin transport and vascular patterning in Arabidopsis. Development 122:1811–1819
Chomczynski P, Sacchi N (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Analytical Biochemistry 162:156–159
Clark SE, Jacobsen SE, Levin JZ, Meyerowitz EM 1996. The CLAVATA and SHOOT MERISTEMLESS loci competitively regulate meristem activity in Arabidopsis. Development 122:1567–1575
Clark SE, Williams RW, Meyerowitz EM (1997) The CLAVATA1 gene encodes a putative receptor kinase that controls shoot and floral meristem size in Arabidopsis. Cell 89:575–585
Cnops G, Wang X, Linstead P, Van Montagu M, Van Lijsebettens M, Dolan L (2000) Tornado1 and tornado2 are required for the specification of radial and circumferential pattern in the Arabidopsis root. Development 127:3385–3394
Cnops G, Neyt P, Raes J, Petrarulo M, Nelissen H, Malenica N, Luschnig C, Tietz O, Ditengou F, Palme K, Azmi A, Prinsen E, Van Lijsebettens M (2006) The TORNADO1 and TORNADO2 genes have a function in several patterning processes during early leaf development in Arabidopsis thaliana. Plant Cell 18:852–866
Endrizzi K, Moussian B, Haecker A, Levin JZ, Laux T (1996) The SHOOT MERISTEMLESS gene is required for maintenance of undifferentiated cells in Arabidopsis shoot and floral meristems and acts at a different regulatory level than the meristem genes WUSCHEL and ZWILLE. Plant J 10:967–979
Ewing B, Hillier L, Wendl MC, Green P (1998) Base-calling of automated sequencer traces using phred. I. Accuracy assessment. Genome Res 8:175–185
Fletcher JC, Brand U, Running MP, Simon R, Meyerowitz EM (1999) Signaling of cell fate decisions by CLAVATA3 in Arabidopsis shoot meristems. Science 283:1911–1914
Hemler ME (2005) Tetraspanin functions and associated microdomains. Nat Rev Mol Cell Biol 6:801–811
Irish VF, Sussex IM (1992) A fate map of the Arabidosis embryonic shoot apical meristem. Development 115:745–753
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
Kasajima I, Ide Y, Ohkama-Ohtsu N, Hayashi H, Yoneyama T, Fujiwara T (2004) A protocol for rapid DNA extraction from Arabidopsis thaliana for PCR analysis. Plant Mol Biol Rep 22:49–52
Kirch T, Simon R, Grunewald M, Werr W (2003) The DORNRÖSCHEN-ENHANCER OF SHOOT REGENERATION1 gene of Arabidopsis acts in the control of meristem ccll fate and lateral organ development. Plant Cell 15:694–705
Konieczny A, Ausubel FM (1993) A procedure for mapping Arabidopsis mutations using co-dominant ecotype-specific PCR-based markers. Plant J 4:403–410
Laux T, Mayer KF, Berger J, Jürgens G (1996) The WUSCHEL gene is required for shoot and floral meristem integrity in Arabidopsis. Development 122:87–96
Laux T, Jürgens G (1997) Embryogenesis: a new start in life. Plant Cell 9:989–1000
Lenhard M, Bohnert A, Jürgens G, Laux T (2001) Termination of stem cell maintenance in Arabidopsis floral meristems by interactions between WUSCHEL and AGAMOUS. Cell 105:805–814
Levy S, Shoham T (2005) The tetraspanin web modulates immune-signalling complexes. Nat Rev Immunol 5:136–148
Li H, Xu L, Wang H, Yuan Z, Cao X, Yang Z, Zhang D, Xu Y, Huang H (2005) The Putative RNA-dependent RNA polymerase RDR6 acts synergistically with ASYMMETRIC LEAVES1 and 2 to repress BREVIPEDICELLUS and MicroRNA165/166 in Arabidopsis leaf development. Plant Cell 17:2157–2171
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25:402–408
Lohmann JU, Hong RL, Hobe M, Busch MA, Parcy F, Simon R, Weigel D (2001) A molecular link between stem cell regulation and floral patterning in Arabidopsis. Cell 105:793–803
Long JA, Moan EI, Medford JI, Barton MK (1996) A member of the KNOTTED class of homeodomain proteins encoded by the STM gene of Arabidopsis. Nature 379:66–69
Long JA, Barton MK (1998) The development of apical embryonic pattern in Arabidopsis. Development 125:3027–3035
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
Olmos E, Reiss B, Dekker K (2003) The ekeko mutant demonstrates a role for tetraspanin-like protein in plant development. Biochem Biophys Res Commun 310:1054–1061
Reinhardt D, Pesce ER, Stieger P, Mandel T, Baltensperger K, Bennett M, Traas J, Friml J Kuhlemeier C (2003) Regulation of phyllotaxy by polar auxin transport. Nature 426:255–260
Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74:5463–5467
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
Sussex IM (1989) Developmental programming of the shoot meristem. Cell 56:225–229
Waites R, Simon R (2000) Signaling cell fate in plant meristems. Three clubs on one tousle. Cell 103:835–838
Acknowledgements
We thank Melanie Cole, Pia Neyt and Wilson Ardiles-Diaz for excellent technical assistance. This research was funded by the Deutsche Forschungsgemeinschaft through SFB 572. W-H. Chiu was a member of the Graduate College “Molecular Analysis of Plant Development” at the University of Cologne.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Chiu, WH., Chandler, J., Cnops, G. et al. Mutations in the TORNADO2 gene affect cellular decisions in the peripheral zone of the shoot apical meristem of Arabidopsis thaliana . Plant Mol Biol 63, 731–744 (2007). https://doi.org/10.1007/s11103-006-9105-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11103-006-9105-z