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They All Scream for ICE1/SCRM2: Core Regulatory Units in Stomatal Development

Nancy R. Hofmann
Nancy R. Hofmann
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Published July 2008. DOI: https://doi.org/10.1105/tpc.108.200711

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The developmental program of stomata includes a series of both symmetrical and asymmetrical divisions and provides an excellent, technically accessible model for the study of patterning, cell fate specification, and regulation of cell division (reviewed in Bergmann and Sack, 2007). Three basic-helix-loop-helix (bHLH) transcription factors, SPEECHLESS (SPCH), MUTE, and FAMA, have been shown to mediate this process at different steps. Kanaoka et al. (pages 1775–1785) further elucidate the regulation of stomatal development by characterizing an Arabidopsis mutant, scrm-D, that forms ectopic stomata.

The homozygous scrm-D mutant has an epidermis made entirely of stomata (see figure ). Because the scrm-D phenotype is identical to that caused by ectopic expression of MUTE, the authors examined the genetic interactions between scrm-D and the known regulators of stomatal development. They found that SCRM likely acts upstream of MUTE and FAMA and that there are dose-dependent effects of SPCH on SCRM, suggesting that they might interact at the molecular level.

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The scrm-D mutation causes ectopic stomata. In the wild-type epidermis (left), stomata are separated from each other by at least one pavement cell. The scrm-D homozygous mutant epidermis (right) is made up entirely of stomata. Bar = 20 μm.

Map-based cloning revealed that SCRM is INDUCER of CBF EXPRESSION1 (ICE1), a bHLH transcription factor that positively regulates the cold-induced transcriptome and freezing tolerance. GUS and GFP fusions showed that ICE1 is nuclear localized and is broadly expressed in stomatal lineage cells. In addition, the same R-to-H substitution found in scrm-D is able to cause ectopic stomata when introduced into SCRM2, an ICE1 paralog identified in this study. An examination of the phenotypes of ice1 and scrm2 null mutants indicated that the two proteins are redundant and act to promote sequential steps of stomatal cell development program: entry, proliferation, and terminal differentiation.

Since bHLH transcription factors form dimers, the authors tested whether these proteins heterodimerize and found that the ICE1 proteins each interact with MUTE, FAMA, and SPCH. These data suggest that ICE1 and SCRM2, which are both expressed throughout stomatal development, form dimers with MUTE, FAMA, and SPCH, which are expressed in specific cells, to regulate the formation of stomata in the epidermis.

This work demonstrates that the regulation of cell division and pattern formation in plants can be strikingly similar to that in other systems. For instance, the broadly expressed myocyte enhancer binding factor 2 family MADS box proteins interact with more restricted bHLH proteins to regulate muscle formation (reviewed in Molkentin and Olson, 1996). In addition, it has long been known that environmental factors contribute to stomatal patterning (reviewed in Casson and Gray, 2008). The finding that ICE1, a regulator of freezing tolerance, is also involved in stomatal development might provide a needed entry point into understanding the link between environmental responses and the formation of stomata.

Footnotes

  • www.plantcell.org/cgi/doi/10.1105/tpc.108.200711

References

  1. ↵
    Bergmann, D.C., and Sack, F.D. (2007). Stomatal development. Annu. Rev. Plant Biol. 58: 163–181.
    OpenUrlCrossRefPubMed
  2. ↵
    Casson, S., and Gray, J.E. (2008). Influence of environmental factors on stomatal development. New Phytol. 178: 9–23.
    OpenUrlCrossRefPubMed
  3. Kanaoka, M.M., Pillitteri, L.J., Fujii, H., Yoshida, Y., Bogenschutz, N.L., Takabayashi, J., Zhu, J.-K., and Torii, K.U. (2008). SCREAM/ICE1 and SCREAM2 specify three cell-state transitional steps leading to Arabidopsis stomatal differentiation. Plant Cell 20: 1775–1785.
  4. ↵
    Molkentin, J.D., and Olson, E.N. (1996). Combinatorial control of muscle development by basic helix-loop-helix and MADS-box transcription factors. Proc. Natl. Acad. Sci. USA 93: 9366–9373.
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They All Scream for ICE1/SCRM2: Core Regulatory Units in Stomatal Development
Nancy R. Hofmann
The Plant Cell Jul 2008, 20 (7) 1732; DOI: 10.1105/tpc.108.200711

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They All Scream for ICE1/SCRM2: Core Regulatory Units in Stomatal Development
Nancy R. Hofmann
The Plant Cell Jul 2008, 20 (7) 1732; DOI: 10.1105/tpc.108.200711
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The Plant Cell Online: 20 (7)
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Vol. 20, Issue 7
July 2008
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