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Plant and Cell Physiology Advance Access originally published online on May 12, 2009
Plant and Cell Physiology 2009 50(6):1019-1031; doi:10.1093/pcp/pcp068
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© The Author 2009. Published by Oxford University Press on behalf of Japanese Society of Plant Physiologists. All rights reserved. For permissions, please email: journals.permissions@oxfordjournals.org

Rapid Paper

Epidermal Cell Density is Autoregulated via a Secretory Peptide, EPIDERMAL PATTERNING FACTOR 2 in Arabidopsis Leaves

Kenta Hara1, Toshiya Yokoo1, Ryoko Kajita1, Takaaki Onishi1, Saiko Yahata1, Kylee M. Peterson2, Keiko U. Torii2 and Tatsuo Kakimoto1,*

1Department of Biological Science, Graduate School of Sciences, Osaka University, Toyonaka, Osaka, 560-0043 Japan
2Department of Biology, University of Washington, Seattle, WA 98195, USA

*Corresponding author: E-mail, kakimoto{at}bio.sci.osaka-u.ac.jp; Fax +81-6-6850-5421.


  Abstract

Regulation of the number of cells is critical for development of multicellular organisms. During plant epidermal development, a protodermal cell first makes a fate decision of whether or not to be the meristemoid mother cell (MMC), which undergoes asymmetric cell division forming a meristemoid and its sister cell. The MMC-derived lineage produces all stomatal guard cells and a large proportion of non-guard cells. We demonstrate that a small secretory peptide, EPIDERMAL PATTERING FACTOR 2 (EPF2), is produced by the MMC and its early descendants, and negatively regulates the density of guard and non-guard epidermal cells. Our results suggest that EPF2 inhibits cells from adopting the MMC fate in a non-cell-autonomous manner, thus limiting the number of MMCs. This feedback loop is critical for regulation of epidermal cell density. The amino acid sequence of EPF2 resembles that of EPF1, which is known to control stomatal positioning. Over-expression of EPF1 also inhibits stomatal development, but EPF1 can act only on a later developmental process than EPF2. Overexpression and promoter swapping experiments suggested that the protein functions of EPF1 and EPF2, rather than the expression patterns of the genes, are responsible for the specific functions. Although targets of EPF1 and EPF2 are different, both EPF1 and EPF2 require common putative receptor components TOO MANY MOUTHS (TMM), ERECTA (ER), ERECTA LIKE 1 (ERL1) and ERL2 in order to function.

Keywords: epidermis - cell density - stomata - pavement cell - negative feedback - Arabidopsis

Abbreviations: bHLH, basic helix–loop–helix; CaMV, cauliflower mosaic virus; EPF, EPIDERMAL PATTERNING FACTOR; ER, ERECTA; ERL, ERECTA LIKE; GFP, green fluorescent protein; GMC, guard mother cell; MAPK, mitogen-activated protein kinase; MMC, meristemoid mother cell; RT–PCR, reverse transcription–PCR; SLGC, stomatal lineage ground cell; SPCH, SPEECHLESS; TMM, TOO MANY MOUTHS; YDA, YODA.

Nucleotide sequence information for EPFL3 and EPFL7 have been deposited in the DDBJ with accession numbers AB499312 [GenBank] and AB499313 [GenBank] , respectively.

(Received April 27, 2009; Accepted May 7, 2009)
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