Morphology as Clue to Developmental Regulation: Stomata
Volume 1, Issue 3, July 2013, Pages: 30-44
Received: Jul. 30, 2013; Published: Aug. 20, 2013
Views 2487      Downloads 205
Valentin Krassilov, Institute of Evolution, University of Haifa, Mount Carmel, Haifa 31905, Israel
Alex Berner, Israel Institute of Technology, Haifa, 32000, Israel
Sophia Barinova, Institute of Evolution, University of Haifa, Mount Carmel, Haifa 31905, Israel
Article Tools
Follow on us
Incipient stomata might have appeared in thalloid alga-like land plants as sporophytic structures homologous to gametangial conceptacles of their isomorphic gametophytes and developed in association with vascular tissue and cuticle. Historically, stomatal evolution is correlated with growth habits and synecological events like the early terrestrial plant expansion from wetland to dryland habitats or the appearance of arboreal and grass canopies. The general tendency of elaboration and aggregation of stomatal complexes was reversed with reduction of vegetative growth at such phylum initiating events as the origin of angiosperms. Stomata links ambient environment with leaf surface air layer and the air of intercellular spaces, balancing the reduction and oxidation reactions involved in photosynthesis. Adaptive responses to environmental change require adjustments of transpiration rates through stomatal density regulation, such as revealed in Ricotia lunaria ecotypes of mesic and xeric slopes of a canyon, with the differences in Stomatal Index comparable to those obtained by experimental exposure to mildly elevated CO2 levels. Long term responses include morphological elaboration of stomatal complexes and their aggregates providing for developmental stability, scarcely impaired by occasional aberrations. Distribution of stomatal complexes correlates with vascularizaton and wax biosynthesis controlled by auxin and ABA hormones respectively at the cell differentiation level. Stomatal transcription factors respond to the interfering auxin/brassinosteroid/ABA signaling mediated by kinaze receptors and their ligands. Stomatal developmental feedbacks are probably conferred by the pH activated protease and oxidative stress activated (’mitogen activated’) protein kinase cascades. This way the hormonal response to environmental pressure is converted into the chemical free energy potential of phosphorylation contributing to internal energy of structural innovation. Universality of this scheme may explain correlation of stomatal development with the whole plant growth habit, ecology and evolution.
Plant Evolution, Developmental Regulation, Stomata
To cite this article
Valentin Krassilov, Alex Berner, Sophia Barinova, Morphology as Clue to Developmental Regulation: Stomata, Plant. Vol. 1, No. 3, 2013, pp. 30-44. doi: 10.11648/j.plant.20130103.11
D. Berger and T.A. Altmann, "Subtilisin-like serine protease involved in the regulation of stomatal density and distribution in Arabidopsis thaliana," Genes and Dev., vol. 14, pp. 1119-1131, 2000
J. A. Nadeau and F.D. Sack, "Control of stomatal distribution on the Arabidopsis leaf surface," Science, vol. 296, pp.1697–1700, 2002.
J. A. Nadeau and F. D. Sack, "Stomatal development in Arabidopsis," in The Arabidopsis Book, C. R. Somerville and E. M. Meyerowitz, Eds. Rockville MD: Am. Soc. Plant Biol., 2002, pp. 1543–8120.
D. Bergmann, "Stomatal development: from neighbourly to global communication," Current Opinion in Plant Biol., vol. 9(5), pp. 478-483, 2006.
D. C. Bergmann, W. Lukowitz and C. R. Somerville, "Stomatal development and pattern controlled by a MAPKK kinase," Science, vol. 304, pp. 1494–1497, 2004.
D. C. Bergmann and F. D. Sack, "Stomatal development," Annual Rev. Plant Biol., vol. 56, pp. 163 – 181, 2007.
E. D. Shpak, C. T. Berthiaume, E. J. Hill and K. U. Torii, "Synergistic interaction of three ERECTA-family receptor-like kinases controls Arabidopsis organ growth and flower development by promoting cell proliferation," Development, vol. 131, pp. 1491–1501, 2004.
K. Hara, R. Kajita, K. U. Torii, D. C. Bergmann and T. Kakimoto, "The secretory peptide gene EPF1 enforces the stomatal one-cell-spacing rule," Genes and Development, vol. 21(14), pp. 1720-1725, 2007.
S. Casson and J. E. Gray, "Influence of environmental factors on stomatal development," New Phytologist, vol. 178(1), pp. 9-23, 2008.
M. M. Kanaoka, L. J. Pillitteri, H. Fujii, Y. Yoshida, N. L. Bogenschutz, J. Takabayashi, J.-K. Zhu and K.U. Toriial, "SCREAM/ICE1 and SCREAM2 specify three cell-state transitional steps leading to Arabidopsis stomatal differentiation," Plant Cell, vol. 20(7), pp. 1775-1785, 2008.
L. J. Pillitteri, N. L. Bogenschutz, and K. U. Torii, "The bHLH protein, MUTE, controls differentiation of stomata and the hydathode pore in Arabidopsis," Plant and Cell Physiol., vol. 49(6), pp. 934-943, 2008.
P. K. Jewaria, T. Hara, H. Tanaka, T. Kondo, S. Betsuyaku, S. Sawa, Y. Sakagami, S. Aimoto and T. Kakimoto, "Differential effects of peptides stomagen, EPF1, and EPF2 on activation of the MAP kinase MPK6 and the SPCH protein level," Plant Cell Physiol., vol. 49(6), pp. 934-943, 2008.
M. Khan, W. Rozhon, J. Bigeard, D. Pflieger, S. Husar, A. Pitzschke, M. Teige, C. Jonak, H. Hirt and B. Poppenberger, "Brassinosteroid-regulated GSK3/shaggy-like kinases phosphorylate MAP kinase kinases, which control stomata development in Arabidopsis thaliana, J. Biol. Chem., vol. 288, pp. 7519-7527, March 2013.
L. J. Pillitteri and J. Dong, "Stomatal Development in Arabidopsis," The Arabidopsis Book, vol. 11, pp. e0162, June 2013.
K. M. Peterson, R. L. Rychel, K. U. Torii, "Out of the mouths of plants: the molecular basis of the evolution and diversity of stomatal development," Plant Cell, vol. 22(2), pp. 296-306, June 2010.
V. A. Krassilov, "On classification of stomata," Palaeontol. J. (Moscow), vol. 1, pp. 102-109, 1968. (В. А. Красилов, "О классификации устьиц," Палеонтол. Ж., № 1, стр. 102-109, 1968).
V. A. Krassilov, "Xeromorphism as climatic indicator," Palaeontol. J. (Moscow), vol. 2, pp. 3-12, 1997. (В.А. Красилов, "Ксероморфизм как климатический индикатор, " Палеонтол. Ж., № 2б стр. 3-12, 1997).
V. A. Krassilov, "Electron microscopy of stomatal guard cells. Palaeontol. J. (Moscow), vol. 3, pp. 128-130, 1978a. (В. А. Красилов, "Электронная микроскопия замыкающих клеток устьиц," Палеонтол. Ж., № 3, стр. 128-130, 1978а).
V. A. Krassilov, "Bennettitalean stomata," Palaeobotanist, vol. 25, pp. 179-184, 1978b.
V. A. Krassilov, "Orestovia and the origin of vascular plants," Lethaia, vol. 14, pp. 235-250, 1981.
V. A. Krassilov, "Scytophyllum and the origin of angiosperm leaf characters," Paleontol. J. (Moscow), vol. 29(A), pp. 63–75, 1995.
V. A. Krassilov, Angiosperm origins: morphological and ecological aspects. Sophia: Pensoft, 1997, 270 pp.
V. A. Krassilov, Cercidiphyllum and fossil allies: morphological interpretation and general problems of plant evolution and development. Sophia: Pensoft, 2010, 150 pp., 43 Plates.
V. A. Krassilov and S. Polevova, "Devonian thalloid plants (Orestoviaceae) and associated spore tetrads," Palaeobotanist, vol. 61, pp. 359-372, 2012.
V. A. Krassilov, Terrestrial palaeoecology and global change. Sophia: Pensoft, 2003, 464 pp.
V. A. Krassilov and E. V. Karasev, "Paleofloristic evidence of climate change near and beyond the Permian - Triassic boundary," Palaeogeography, Palaeoclimatology, Palaeoecology, vol. 284(3-4), pp. 326-336, 2009.
A. K. Srivastava, V.A. Krassilov and D. Agnihotri, "Peltasperms in the Permian of India and their bearing on Gondwanaland: reconstruction and climatic interpretation," Palaeogeography, Palaeoclimatology, Palaeoecology, vol. 310, pp. 393–399, 2011.
V. A. Krassilov, Paleoecology of terrestrial plants. Basic Principles and techniques. N.Y.–Toronto: Wiley, 283 pp., 1975.
S. Meyen, Fundamentals of paleobotany. New York: Chapman and Hall, 432 pp. 1987.
T. N. Taylor, E. L. Taylor and M.Krings, Paleobotany: The biology and evolution of fossil plants. Amsterdam: Academic Press, 2009, 1252 pp.
V. A. Krassilov, "Late Cretaceous gymnosperms from Sakhalin and the terminal Cretaceous event," Palaeontology, vol. 21, pp. 893-905, 1978c.
G. Hagen, and T. Guilfoyle, "Auxin-responsive gene expression: genes, promoters and regulatory factors," Plant Mol. Biol., vol. 49(3-4), pp. 373-385, 2002.
M. Yang and F. D. Sack, "The too many mouths and four lips Mutations Affect Stomatal Production in Arabidopsis," Plant Gell, vol. 7, pp. 2227-2239, 1995.
K. Hara, T. Yokoo, R. Kajita, T. Onishi, S. Yahata, K. M. Peterson, K. U. Torii and T. Kakimoto, "Epidermal cell density is autoregulated via a secretory peptide, EPIDERMAL PATTERNING FACTOR 2 in Arabidopsis leaves," Plant Cell Physiol., vol. 50(6), pp. 1019-1031, 2009.
C. A. MacAlister, K. Ohashi-Ito and D. C. Bergmann, "Arabidopsis FAMA controls the final proliferation/differentiation switch during stomatal development," Nature, vol. 445, pp. 537–540, February 2007.
J. E. Gray, G. H. Holroyd, F. M. van der Lee, A. R. Bahrami, P. C. Sijmons, F. I. Woodward, W. Schuch and A. M. Hetherington, "The HIC signaling pathway links CO2 perception to stomatal development," Nature, vol. 408, pp. 713–716, December 2000.
U. Schlüter, M. Muschak, D. Berger and T. Altmann, "Photosynthetic performance an Arabidopsis mutant with elevated stomatal density (sdd1-1) under different light regimes," J. Exp. Bot., vol. 54(383), pp. 867–874, February 2003.
B. Luo, X.-Y. Xue, W.-L. Hu, L.-J. Wang and X.-Y. Chen, "An ABC transporter gene of Arabidopsis thaliana, AtWBC11, is involved in cuticle development and prevention of organ fusion," Plant Cell Physiol., vol. 48(12), pp. 1790-1802, December 2007.
D. Panikashvili, S. Savaldi-Goldstein, T. Mandel, T. Yifhar, R. B. Franke, R. Hofer, L. Schreiber, J. Chory and A. Aharoni, The Arabidopsis DESPERADO/AtWBC11 transporter is required for cutin and wax secretion," Plant Physiol., vol. 145(4), pp. 1345-1360, December 2007.
P. J. Seo, S. B. Lee, M. Ch. Suh, M.-J. Park, Y. S. Go and Ch.-M. Parka, "The MYB96 transcription factor regulates cuticular wax biosynthesis under drought conditions in Arabidopsis," Plant Cell, vol. 23, pp. 1138–1152, March 2011.
H. Candela, A. Martinez-Laborda and J. L. Micol, "Venation pattern formation in Arabidopsis thaliana vegetative leaves," Develop. Biol., vol. 205(1), pp. 205-216, 1999.
Y. Kovtun, W. L. Chiu, G. Tena and J. Sheen, "Functional analysis of oxidative stress-activated mitogenactivated protein kinase cascade in plants," Proc. Natl. Acad. Sci. U S A, vol. 97(6), pp. 2940–2945, March 2000.
R. Aloni, "Foliar and axial aspects of vascular differentiation: hypotheses and evidence," J. Plant Growth Regul., vol. 20, pp. 22–34, February 2001.
R. Aloni, M. Langhans, E. Aloni, E. Dreieicher, C. I. Ullrich, "Root-synthesized cytokinin in Arabidopsis is distributed in the shoot by the transpiration stream," J. Exp. Bot., vol. 56(416), pp. 1535–1544, June 2005.
N. K. Clay and T. Nelson, "Arabidopsis thickvein mutation affects vein thickness and organ vascularization, and resides in a provascular cell-specific spermine synthase involved in vein definition and in polar auxin transport," Plant Physiol., vol. 138(2), pp. 767-777, June 2005.
E. Scarpella, D. Marcos, J. Friml and T. Berleth, "Control of leaf vascular patterning by polar auxin transport," Genes Dev., vol. 20(8), pp. 1015-1027, April 2006.
F.I. Woodward, "Stomatal numbers are sensitive to CO2 increases from preindustrial levels," Nature, vol. 327, pp. 617–618, June 1987.
F. I. Woodward and C. K. Kelly, "The influences of CO2 concentration on stomatal density," New Phytologist, vol. 131(3), pp. 311–327, November 1995.
J. A. Lake, W.P. Quick, D. J. Beerling and F.I. Woodward, "Signals from mature to new leaves," Nature, vol. 411, pp. 154, May 2001.
T. Lawson, J. Craigon, C. R. Black, J. J., Colls, G. Landon and J.D. Weyers, "Impact of elevated CO2 and O3 on gas exchange parameters and epidermal characteristics in potato (Solanum tuberosum L.)," J. Exp. Bot., vol. 53(369), pp. 737–746, 2002.
S. Driscoll, A. Prins, E. Olmos, K. Kunert, C. Foyer, "Specification of adaxial and abaxial stomata, epidermal structure and photosynthesis to CO2 enrichment in maize leaves," J. Exp. Bot., vol. 57, pp. 381–390, 2006.
G. J. Retallak, "A 300-million-year record of atmospheric carbon dioxide from fossil plant cuticles," Nature, vol. 411, pp. 287-290, May 2001.
G. Ågren, "Limits to plant production," J. Theor. Biol., vol. 113, pp. 89–92, March 1985.
O. Kossover, Z. Frenkel, A. Korol and E. Nevo, "Genetic diversity and stress of Ricotia lunaria in "Evolution Canyon," Israel," J. Hered. vol. 100(4), pp. 432-440, March 2009.
H. Kazama, H. Dan, H. Imaseki and G. O. Wasteneys, "Transient exposure to ethylene stimulates cell division and alters the fate and polarity of hypocotyl epidermal cells," Plant Physiol., vol. 134(4), pp. 1614–1623, April 2004.
S. Schoch, C. Hehlein and W. Rudiger, "Influence of anaerobiosis on chlorphyll biosynthesis in greening oat seddlings (Avena sativa L.)," Plant Physiol., vol. 66, pp. 576-569, October 1980.
W. D. Teale, I. A. Paponov and K. Palme, "Auxin in action: Signalling, transport and the control of plant growth and development," Nat. Rev. Mol. Cell Biol., vol. 7(11), pp. 847–859, November 2006.
X. Chen, S. M. Goodwin, V. L. Boroff, X. Liu and M. A. Jenks, "Cloning and characterization of the WAX2 gene of Arabidopsis involved in cuticle membrane and wax production," Plant Cell, vol. 15(5), pp. 1170–1185, May 2003.
K .D. Cameron, M. A. Teece and L.B. Smart, "Increased accumulation of cuticular wax and expression of lipid transfer protein in response to periodic drying events in leaves of tree tobacco," Plant Physiol., vol. 140(1), pp. 176–183, January 2006.
Y. Xiang, Y. Huang and L. Xiong, "Characterization of stress-responsive CIPK genes in rice for stress tolerance improvement," Plant Physiol., vol. 144(3), pp. 1416-1428, July 2007.
E. Benková, M. Michniewicz, M. Sauer, T. Teichmann, D. Seifertová, G. Jürgens and J. Friml, "Local, efflux-dependent auxin gradients as a common module for plant organ formation," Cell, vol. 115(5), pp. 591–602, November 2003.
A. Paponov, W. D. Teale, M. Trebar, I. Blilou and K. Palme, "The PIN auxin efflux facilitators: evolutionary and functional perspectives," Trends Plant Sci., vol. 10, pp. 170–177, April 2005.
K. U. Torii, N. Mitsukawa, T. Oosumi, Y. Matsuura, R. Yokoyama, R. F. Whittier and Y. Komeda, "The Arabidopsis ERECTA gene encodes a putative receptor protein kinase with extracellular leucine-rich repeats," Plant Cell, vol. 8(4), pp. 735-746, April 1996.
J. I. Schroeder, J. M. Kwak and G. J. Allen, "Guard cell abscisic acid signalling and engineering drought hardiness in plants," Nature, vol. 410, pp. 327-330, March 2001.
Science Publishing Group
NEW YORK, NY 10018
Tel: (001)347-688-8931