Abstract
Stomata are an essential land plant innovation whose patterning and density are under genetic and environmental control. Recently, several putative ligands have been discovered that influence stomatal density, and they all belong to the EPIDERMAL PATTERNING FACTOR-LIKE family of secreted cysteine-rich peptides. Two of these putative ligands, EPF1 and EPF2, are expressed exclusively in the stomatal lineage cells and negatively regulate stomatal density. A third, EPFL6 or CHALLAH, is also a negative regulator of density, but is expressed subepidermally in the hypocotyl. A fourth, EPFL9 or STOMAGEN, is expressed in the mesophyll tissues and is a positive regulator of density. Genetic evidence suggests that these ligands may compete for the same receptor complex. Proper stomatal patterning is likely to be an intricate process involving ligand competition, regional specificity, and communication between tissue layers. EPFL-family genes exist in the moss Physcomitrella patens, the lycophyte Selaginella moellendorffii, and rice, Oryza sativa, and their sequence analysis yields several genes some of which are related to EPF1, EPF2, EPFL6, and EPFL9. Presence of these EPFL family members in the basal land plants suggests an exciting hypothesis that the genetic components for stomatal patterning originated early in land plant evolution.
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References
Abrash EB, Bergmann DC (2010) Regional specification of stomatal production by the putative ligand CHALLAH. Development 137:447–455
Bergmann DC, Lukowitz W, Somerville CR (2004) Stomatal development and pattern controlled by a MAPKK kinase. Science 304:1494–1497
Bhave NS, Veley KM, Nadeau JA, Lucas JR, Bhave SL, Sack FD (2009) TOO MANY MOUTHS promotes cell fate progression in stomatal development of Arabidopsis stems. Planta 229:357–367
Boman HG (1995) Peptide antibiotics and their role in innate immunity. Annu Rev Immunol 13:61–92
Broekaert WF, Terras FR, Cammue BP, Osborn RW (1995) Plant defensins: novel antimicrobial peptides as components of the host defense system. Plant Physiol 108:1353–1358
Casson S, Gray JE (2008) Influence of environmental factors on stomatal development. New Phytol 178:9–23
Geisler M, Nadeau J, Sack FD (2000) Oriented asymmetric divisions that generate the stomatal spacing pattern in arabidopsis are disrupted by the too many mouths mutation. Plant Cell 12:2075–2086
Hara K, Kajita R, Torii KU, Bergmann DC, Kakimoto T (2007) The secretory peptide gene EPF1 enforces the stomatal one-cell-spacing rule. Genes Dev 21:1720–1725
Hara K, Yokoo T, Kajita R, Onishi T, Yahata S, Peterson KM, Torii KU, Kakimoto T (2009) Epidermal cell density is autoregulated via a secretory peptide, EPIDERMAL PATTERNING FACTOR 2 in Arabidopsis leaves. Plant Cell Physiol 50:1019–1031
Hunt L, Gray JE (2009) The signaling peptide EPF2 controls asymmetric cell divisions during stomatal development. Curr Biol 19:864–869
Kanaoka MM, Pillitteri LJ, Fujii H, Yoshida Y, Bogenschutz NL, Takabayashi J, Zhu JK, Torii KU (2008) SCREAM/ICE1 and SCREAM2 specify three cell-state transitional steps leading to arabidopsis stomatal differentiation. Plant Cell 20:1775–1785
Kondo T, Kajita R, Miyazaki A, Hokoyama M, Nakamura-Miura T, Mizuno S, Masuda Y, Irie K, Tanaka Y, Takada S, Kakimoto T, Sakagami Y (2010) Stomatal Density is Controlled by a Mesophyll-Derived Signaling Molecule. Plant Cell Physiol 51:1–8
Lampard GR, Macalister CA, Bergmann DC (2008) Arabidopsis stomatal initiation is controlled by MAPK-mediated regulation of the bHLH SPEECHLESS. Science 322:1113–1116
MacAlister CA, Ohashi-Ito K, Bergmann DC (2007) Transcription factor control of asymmetric cell divisions that establish the stomatal lineage. Nature 445:537–540
Nadeau JA, Sack FD (2002) Control of Stomatal Distribution on the Arabidopsis Leaf Surface. Science 296:1697–1700
Ohashi-Ito K, Bergmann DC (2006) Arabidopsis FAMA controls the final proliferation/differentiation switch during stomatal development. Plant Cell 18:2493–2505
Okuda S, Tsutsui H, Shiina K, Sprunck S, Takeuchi H, Yui R, Kasahara RD, Hamamura Y, Mizukami A, Susaki D, Kawano N, Sakakibara T, Namiki S, Itoh K, Otsuka K, Matsuzaki M, Nozaki H, Kuroiwa T, Nakano A, Kanaoka MM, Dresselhaus T, Sasaki N, Higashiyama T (2009) Defensin-like polypeptide LUREs are pollen tube attractants secreted from synergid cells. Nature 458:357–361
Peterson KM, Rychel AL, Torii KU (2010) Out of the mouths of plants: the molecular basis of the evolution and diversity of stomatal development. Plant Cell 22. doi:10.1105/tpc.109.072777
Pillitteri LJ, Torii KU (2007) Breaking the silence: three bHLH proteins direct cell-fate decisions during stomatal development. Bioessays 29:861–870
Pillitteri LJ, Sloan DB, Bogenschutz NL, Torii KU (2007) Termination of asymmetric cell division and differentiation of stomata. Nature 445:501–505
Pillitteri LJ, Bogenschutz NL, Torii KU (2008) The bHLH protein, MUTE, controls differentiation of stomata and the hydathode pore in Arabidopsis. Plant Cell Physiol 49:934–943
Raven JA (2002) Selection pressures on stomatal evolution. New Phytol 153:371–386
Sachs T (1991) Pattern formation in plant tissues. Cambridge University Press, Cambridge
Schopfer CR, Nasrallah ME, Nasrallah JB (1999) The male determinant of self-incompatibility in Brassica. Science 286:1697–1700
Shpak ED, McAbee JM, Pillitteri LJ, Torii KU (2005) Stomatal patterning and differentiation by synergistic interactions of receptor kinases. Science 309:290–293
Silverstein KA, Moskal WA Jr, Wu HC, Underwood BA, Graham MA, Town CD, VandenBosch KA (2007) Small cysteine-rich peptides resembling antimicrobial peptides have been under-predicted in plants. Plant J 51:262–280
Sugano SS, Shimada T, Imai Y, Okawa K, Tamai A, Mori M, Hara-Nishimura I (2010) Stomagen positively regulates stomatal density in Arabidopsis. Nature 463:241–244
Takayama S, Shiba H, Iwano M, Shimosato H, Che FS, Kai N, Watanabe M, Suzuki G, Hinata K, Isogai A (2000) The pollen determinant of self-incompatibility in Brassica campestris. Proc Natl Acad Sci USA 97:1920–1925
Yang M, Sack FD (1995) Too many mouths and four lips mutations affect stomatal production in Arabidopsis. Plant Cell 7:2227–2239
Acknowledgments
We thank Drs. Tatsuo Kakimoto, Dominique Bergmann, and Ikuko Hara-Nishimura for insightful discussion. Our research is supported by grants from the National Science Foundation (IOB-0744892 and MCB-0855659) and PREST, Japan Science and Technology Agency to K.U.T. K.M.P. is a National Science Foundation Graduate Research Fellow.
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Rychel, A.L., Peterson, K.M. & Torii, K.U. Plant twitter: ligands under 140 amino acids enforcing stomatal patterning. J Plant Res 123, 275–280 (2010). https://doi.org/10.1007/s10265-010-0330-9
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DOI: https://doi.org/10.1007/s10265-010-0330-9