Abstract
Aim:
Each cell is the production of multiple signal transduction programs involving the expression of thousands of genes. This study aims to gain insights into the gene regulation mechanisms of stomatal development and will investigate the relationships among some signaling transduction pathways.
Methods:
Nail enamel printing was conducted to observe the stomatal indices of wild type and 10 mutants (plant hormone mutants, Pi-starvation induced CaM mutants and Pi-starvation-response mutant) in Arabidopsis, and their stomatal indices were analyzed by ANOVA. We analyzed the stomatal indices of 10 Arabidopsis mutants were analyzed by a model PRGE (potential relative effect of genes) to research relations among these genes.
Results:
In wild type and 10 mutants, the stomatal index didn't differ with respect to location on the lower epidermis. Compared with wild type, the stomatal indices of 10 mutants all decreased significantly. Moreover, significant changes and interactions might exist between some mutant genes.
Conclusion:
It was the stomatal intensity in Arabidopsis might be highly sensitive to most mutations in genome. While the effect of many gene mutations on the stomatal index might be negative, we also could assume the stomatal development was regulated by a signal network in which one signal transduction change might influence the stomatal development more or less, and the architecture might be reticulate. Furthermore, we could speculate that calcium was a hub in stomatal development signal regulation network, and other signal transduction pathways regulated stomtal development by influencing or being influenced by calcium signal transduction pathways.
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References
Hetherington AM, Woodward FI . The role of stomata in sensing and drivingenvironmental change. Nature 2003; 424: 1–8.
Webb AAR, Baker AJ . Commentary stomatal biology: new techniques, new challenge. New Phytol 2002; 153: 365–75.
Pääkkönen E, Günthardt-Goerg MS, Holopainen T . Responses of leaf processes in a sensitive birch (Betula pendula Roth) clone to ozone combined with drought. Ann Bot 1998; 82: 49–59.
Li CY, Wang KY . Differences in drought responses of three contrasting Eucalyptus microtheca F. Muell. population. Forest Ecol Manag 2003; 179: 377–85.
Gitz DC, Lan Liu-Gitz, Britz SJ, Sullivan JH . Ultraviolet-B effects on stomatal density, water-use efficiency, and stable carbon isotope discrimination in four glasshouse-grown soybean (Glyicine max) cultivars. Environ Exp Bot 2005; 53: 343–55.
Beerling DJ, Osborne CP, Chaloner WG . Evolution of leaf-form in land plants linked to atmospheric CO2 decline in the Late Palaeozoic era. Nature 2001; 410: 352–4.
Beerling DJ, McElwain JC, Osborne CP . Stomatal responses of the “living fossil” Ginkgo biloba L. To changes in atmospheric CO2 concentrations. J Exp Bot 1998; 49: 1603–7.
Kürschner WM van der Burgh J, Visscher H, Dilcher DL . Oak leaves as biosensors of late Neogene and early Pleistocene paleoatmospheric CO2 concentrations. Micropaleont 1996; 27: 299–312.
Yang HM, Zhang JH, Zhang XY . Regulation mechanisms of stomatal oscillation. J Integr Plant Biol 2005; 47: 1159–72.
Mansfleld, Mansfield TA, Hetherlngton AM, Atkinson CJ . Some current aspects of stomatal physiology. Annu Rev Plant Physiol Plant MOI Biol 1990; 41: 55–75.
Pei ZM, Kuchitsu K, Ward JM, Schwarz M, Schroeder L . Differnential abscisic acid regulation of guard cell slow anion channels in Arabidopsis wild-type and abi1 and abi2 mutants. Plant Cell 1997; 9: 409–23.
Ward JM, Pei ZM, Schroeder J . Roles of ion channels in initiation of signal transduction in higher plants. Plant Cell 1995; 7: 833–44.
Allen GJ, Chu SP, Schumacher K, Shimazaki C, Vafeados D . Alteration of stimulus-specific guard cell calcium oscillatioins and stomatal closing in Arabidopsis det3 mutant. Science 2000; 289: 2338–42.
McAinsh MR, Webb AAR, Talor JE, Hetherington AM . Stimulus-induces oscillations in guars cell cytoplasmic free calcium. Plant Cell 1995; 7: 1207–19.
Staxen I, Pical C, Montgomery LT, Gray JE, Hetherington AM, McAinsh MR . Abscisic acid induces oscillations in guard-cell cytosolic free calcium that involve phosphoinositide-specific phospholipase C. Proc Natl Acad Sci USA 1999; 96: 1779–84.
McAinsh MR, Brownlee C, Herherington AM . Calcium ions as second messengers in guard cell signal transduction. Physiol Planta 1997; 100: 16–29.
McAinsh MR, Hetherington AM . Encoding specificity in Ca2+ signaling systems. Trends Plant Sci 1997; 3: 32–6.
Schroeder JI, Kwak JM, Allen GJ . Guard cell abscisic acid signaling and engineering drought hardiness in plants. Nature 2001; 410: 327–330.
Allen GJ, Chu SP, Harrington CL, Schumacher K, Hoffmann T, Tang YY, et al. A defined range of guard cell calcium oscillation parameters encodes stomatal movements. Nature 2001; 411: 1053–7.
Wang GX, Zhang J, Liao JX, Wang JL . Hydropassive evidence and effective factors in stomatal oscillations of Glycyrrhiza inflate under desert conditions. Plant Sci 2001; 160: 1007–13.
Wang GX, Zhao SL . RLC circuit simulation of stomatal oscillation of Glycyrrhiza inflata under atmospheric drought condition, Chin J Appl Ecol 1993; 4: 131–5.
Yang HM, Li Y, Wang GX . Functions and roles of the channels in broad bean stomatal movements. Acta Phytoecol Sin 2002; 26: 656–60.
Yang HM, Zhang XY, Wang GX, Li Y, Wei XP . Cytosolic calcium oscillation may induce stomatal oscillation in Vicia faba. Plant Sci 2003; 165: 1117–22.
Yang HM, Zhang XY, Wang GX . Effects of heavy metals on stomatal movements in broad bean. Russ J Plant Physiol 2004; 51: 464–8.
Roelfsema MRG, Hedrich R . Research review Studying guard cells in the intact plant: modulation of stomatal movement by apoplastic factors. New Phytol 2002; 153: 425–31.
Dodd IC . Hormonal interactions and stomatal responses. J Plant growth Regul 2003; 22: 32–46.
Biddington NI, Thomas TH . The influence of different cytokinins on the transpiration and senescence of excised oat leaves. Physiol Plant 1978; 42: 369–74.
Incoll LD, Jewer PC . Cytokinins and stomata. In: Zeiger E, Farquhar GD, Cowan IR Stomatal Function. Stanford: Stanford University Press. 1987; 281–92.
Blackman PG, Davies WJ . Age-regulated changes in stomatal response to cytokinins and abscisic acid. Ann Bot 1984; 54: 121–5.
Irving HR, Gehring CA, Parish RW . Changes in cytosolic pH and calcium of guard cells precede stomatal movements. Proc Natl Acad Sci USA 1992; 89: 1790–4.
Marschner H Mineral nutrition of higher plants. San Diego (CA): Academic Press; 1995.
Bates TR, Lynch JP . Stimulation of root hair elongation in Arabidopsis thaliana by low phosphorus availability. Plant Cell Environ 1996; 21: 529–38.
Rubio V, Linhares F, Solano R, Martín AC, Iglesias J, Leyva A, et al. A conserved MYB transcription factor involved in phosphate starvation signaling both in vascular plants and in unicellular algae. Genes Dev 2001; 15: 2122–33.
Wu P, Ma LG, Hou XL, Wang MY, Wu YR, Liu FY, et al. Phosphate starvation triggers distinct alterations of genome expression in Arabidopsis roots and leaves. Plant Physiol 2003; 132: 1260–71.
Saunders MJ . Calcium and plant hormone action. Symp Soc Exp Biol 1990; 44: 2 71–83.
Sun DY, Guo YL, Ma LG, Cui Sj . Cell signal transduction. 3rd ed. Beijing: Science Press; 2003.
Schroeder JI, Allen GJ, Hugouvieux V, Kwak JM, Waner D . Guard cell signal transduction. Annu Rev Plant Physiol Plant Mol Biol 2001; 52: 627–58.
Gilroy S, Read ND, Trewavas AJ . Elevation of cytoplasmic Ca2+ by caged calcium or caged inositol triphosphate initiates stomatal closure. Nature 1990; 346: 769–71.
Clayton H, Knight MR, Knight H, McAinsh MR, Hetherington AM . Dissection of the ozone-induced calcium signature. Plant J 1999; 17: 575–9.
Blatt MR . Ca2+ signalling and control of guard-cell volumein stomatal movements. Curr Opin Plant Biol 2000; 3: 196–204.
MacRobbie EAC . ABA activates multiple Ca2+fluxes in stomatal guard cells, triggering vacuolar K+ (Rb+) release. Proc Natl Acad Sci USA 2000; 97: 12361–8.
McAinsh MR, Gray JE, Hetherington AM, Leckie CP, Ng CKY . Ca2+ signalling in stomatal guard cells. Biochem Soc Trans 2000; 28: 476–81.
Yang HM, Wang GX . The relationships between the variations of cytosolic Ca2+ concentration in guard cells and the stomatal movements. Plant Physiol Commun 2001; 37: 269–73. Chinese.
Zhang X, Zhang L, Dong F, Gao J, Galbraith DW, Song CP . Hydrogen peroxide is involved in abscisic acid-induced stomatal closure in Vicia faba. Plant Physiol 2001; 126: 1438–48.
Luan S . Signalling drought in guard cells. Plant Cell Environ 2002; 25: 229–37.
Evans NH, Hetherington AM . Plant physiology: The ups and downs of guard cell signalling. Curr Biol 2001; 11: R92–4.
Grabov A, Blatt MR . Membrane voltage initiates Ca2+ waves and potentiates Ca2+ increases with abscisic acid in stomatal guard cells. Proc Natl Acad Sci USA 1998; 95: 4778–83.
Yang M, Sack FD . The too many mouths and four lips mutations affect stomatal production in Arabidopsis. Plant Cell 1995; 7: 2227–39.
Larkin JC, Marks MD, Nadeau J, Sackc F . Epidermal cell fate and patterning in leaves. Plant Cell 1997; 9: 1109–20.
Zhao XZ, Dai XF, Wang GX, Shen ZX, Zhang H, Qiu MQ . Developmental mechanism and distribution pattern of stomatal clusters in Cinnamomum camphora. Russ J Plant Physl. 2006; 53: 310–15.
Vogel JP, Schuerman P, Woeste K, Brandstatter I, Kieber JJ . Isolation and characterization of Arabidopsis mutants defective in the induction of ethylene biosynthesis by cytokinin. Genetics 1998; 149: 417–27.
Chao Q, Rothenberg M, Solano R, Roman G, Terzaghi W, Ecker JR . Activation of the ethylene gas response pathway in Arabidopsis by the nuclear protein ETHYLENE-INSENSITIVE3 and related proteins. Cell 1997; 89: 1133–44.
Hua J, Sakai H, Nourizadeh S, Chen QG, Bleecker AB, Ecker JR, et al. EIN4 and ERS2 are members of the putative ethylene receptor gene family in Arabidopsis. Plant cell 1998; 10: 1321–32.
Cao YZ . Athaliana. Beijing: Higher Education Press; 2004. Chinese.
Yanagisawa S, Yoo SD, Sheen J . Differential regulation of EIN3 stability by glucose and ethylene signalling in plants. Nature 2003; 425: 521–5.
Allen GJ, Murata Y, Chu SP, Nafisi M, Schroeder JI . Hypersensitivity of abscisic acid-induced cytosolic calcium increases in the Arabidopsis farnesyltransferase mutant era1-2. Plant Cell 2002; 14: 1649–62.
Cutler S, Ghassemian M, Bonetta D, Cooney S, McCourt P . A protein farnesyl transferase involves in abscisic acid signal transduction in Arabidopsis. Science 1996; 273: 1239–41.
Cutler S, Ghassemian M, Cooney S, Bonetta D, McCourt P . Molecular genetic analysis of abscisic acid (ABA) hypersensitive mutants in Arabidopsis Sixth International Conference on Arabidopsis research; 1995; Madison, WI.
Duan RJ, Yi KK, Wu P . The structure and phosphorus or potassium deficiency induced expression of a calmodulin-like protein gene in Arabidopsis. J Plant Physiol Mol Biol 2005; 31: 520–6. Chinese.
Murashige T, Skoog F . A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 1962; 15: 473–97.
Chen DL, Delatorre CA, Bakker A, Abel S . Conditional identification of phosphate-starvation-response mutants in Arabidopsis thaliana. Planta 2000; 211: 13–22.
Tang M, Hu YX, Lin JX, Jin XB . Developmental mechanism and distribution pattern of stomatal clusters in begonia peltatifolia. Acta Bot Sin 2002; 44: 384–90.
Weyers JDB, Meidner H . Methods in stomatal research. 1st ed. Essex (UK): Longman Scientific Technical; 1990.
Liu LX, Cheng HW, Chen WF . Studies on the stomatal distribution and density in rice leaves. J Shenyang Agricul Univ 2000; 31: 313–17. Chinese.
Strickberger MW . Evolution. 3rd ed. Sudbury: Jones and Bartlett publishers; 2002.
Clapham DE . Calcium signalling. Cell 1995; 80: 259–68.
Romanov GA, Getman IA, Schmülling T . Investigation of early cytokinin effects in a rapid Amaranthus seedling test. Plant Grow Regul 2000; 32: 337–44.
Reddy ASN, Reddy VS, Golovkin MA . Calmodulin binding protein from Arabidopsis is induced by ethylene and contains a DNA-binding motif. Biochem Biophys Res Commun 2000; 279: 762–9.
Schumaker KS, Gizinski MJ . 1,4-Dihydropyridine binding sites in moss plasma membranes. Properties of receptors for a calcium channel antagonist. J Biol Chem 1995; 270: 23461–7.
Abel S, Ticconi CA, Delatorre CA . Phosphate sensing in higher plants. Physiol Plant 2002; 115: 1–8.
Saunders MJ, Hepler PK . Calcium antagonists and calmodulin inhibitors block cytokinin-induced bud formation in Funaria. Dev Biol 1983; 99: 41–9.
Elliott DC . Inhibition of cytokinin-regulated responses by calmodulin-binding compounds. Plant Physiol. 1983; 72: 215–18.
Yang HM, Zhang XY, Wang GX . Cytosolic calcium oscillation signaling in guard cell. Plant Sci 2004; 166: 549–56.
Elliott DC . Ionic regulation for cytokinin-dependent betacyanin synthesis in amaranthus seedlings. Plant Physiol. 1979; 63: 264–8.
Ghassemian M, Nambara E, Cutler S, Kawaide H, Kamiya Y, McCourt P . Regulation of abscisic acid signaling by the ethylene response pathway in Arabidopsis. Plant Cell 2000; 12: 1117–26.
Reiss C, Beale SI . External calcium requirements for light induction of chlorophyll accumulation and its enhancement by red light and cytokinin pretreatments in excised etiolated cucumber cotyledons. Planta 1995; 196: 635–41.
Hahm SH, Saunders MJ . Cytokinin increases intracellular Ca2+ in Funaria: detection with Indo-1. Cell Calcium 1991; 12: 675–81.
Schumaker KS, Gizinski MJ . Cytokinin stimulates dihydropyridine-sensitive calcium uptake in moss protoplasts. Proc Natl Acad Sci USA 1993; 90: 10937–41.
Salama AMSE-DA, Wareing PF . Effects of mineral nutrition on endogenous cytokinins in plants of sunflower (Helianthus annuus L). J Exp Bot 1979; 30: 971–98.
Shin H, Shin HS, Chen R, Harrison MJ . Loss of At4 function impacts phosphate distribution between the roots and the shoots during phosphate starvation. Plant J 2006; 45: 712–26.
Chang H, Jones ML, Banowetz GM, Clark DG . Overproduction of Cytokinins in Petunia Flowers Transformed with PSAG12-IPT delays corolla senescence and decreases sensitivity to ethylene. Plant Physiol 2003; 132: 2174–83.
Ludwig AA, Saitoh H, Felix G, Freymark G, Miersch O, Wasternack C, et al. Ethylene-mediated cross-talk between calcium-dependent protein kinase and MAPK signaling controls stress responses in plants. Proc Natl Acad Sci USA 2005; 102: 10736–41.
Hamant O, Nogué F, Enric BB, Jublot D, Grandjean O, Traas J, et al. The KNAT2 Homeodomain Protein Interacts with Ethylene and Cytokinin Signaling. Plant Physiol 2002; 130: 657–65.
Cary AJ, Liu W, Howell SH . Cytokinin action is coupled to ethylene in its effects on the inhibition of root and hypocotyl elongation in Arabidopsis thaliana seedlings. Plant Physiol 1995; 107: 1075–82.
Penninckx IA, Thomma BP, Buchala A, Metraux JP, Broekaert WF . Concomitant activation of jasmonate and ethylene response pathways is required for induction of a plant defensin gene in Arabidopsis. Plant Cell 1998; 10: 2103–13.
Alonso JM, Hirayama T, Roman G, Nourizadeh S, Ecker JR . EIN2, a bifunctional transducer of ethylene and stress responses in Arabidopsis. Science 1999; 284: 2148–52.
Lee TI, Rinaldi NJ, Robert F, Odom DT, Ziv Bar-Joseph Gerber GK, et al. Transcriptional Regulatory Networks in Saccharomyces cerevisiae. Science 2002; 298: 799–804.
Mishra G, Zhang WH, Deng F, Zhao J, Wang XM . A bifurcating pathway directs abscisic acid effects on stomatal closure and opening in Arabidopsis. Science 2006; 312: 264–6.
Lake JA, Woodward FL, Quick WP . Long-distance CO2 signaling in plants. J Exp Bot 2002; 53: 183–93.
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Project supported by the National Natural Science Foundation of China (No 3017016, No 90102015) and by a grant of doctoral discipline from the Ministry of Education of China (No 20030335043).
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Shen, Zx., Wang, Gx., Liu, Zq. et al. Network regulation of calcium signal in stomatal development. Acta Pharmacol Sin 27, 950–958 (2006). https://doi.org/10.1111/j.1745-7254.2006.00400.x
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DOI: https://doi.org/10.1111/j.1745-7254.2006.00400.x