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Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Stomatal aperture can compensate altered stomatal density in Arabidopsis thaliana at growth light conditions

Dirk Büssis A D , Uritza von Groll B C , Joachim Fisahn B and Thomas Altmann A
+ Author Affiliations
- Author Affiliations

A Institute of Biochemistry and Biology — Genetics, University of Potsdam, D-14415 Potsdam, Germany.

B Max-Planck-Institute of Molecular Plant Physiology, Am Mühlenberg 1, D-14476 Golm, Germany.

C Present address: Qiagen GmbH, Max-Vollmer-Str 4, D-40724 Hilden, Germany.

D Corresponding author. Email: buessis@mpimp-golm.mpg.de

Functional Plant Biology 33(11) 1037-1043 https://doi.org/10.1071/FP06078
Submitted: 4 April 2006  Accepted: 24 August 2006   Published: 1 November 2006

Abstract

Stomatal density of transgenic Arabidopsis thaliana plants over-expressing the SDD1 (stomatal density and distribution) gene was reduced to 40% and in the sdd1-1 mutant increased to 300% of the wild type. CO2 assimilation rate and stomatal conductance of over-expressers and the sdd1-1 mutant were unchanged compared with wild types when measured under the light conditions the plants were exposed to during growth. Lower stomatal density was compensated for by increased stomatal aperture and conversely, increased stomatal density was compensated for by reduced stomatal aperture. At high light intensities the assimilation rates and stomatal conductance of SDD1 over-expressers were reduced to 80% of those in wild type plants. Areas beneath stomata and patches lacking stomata were analysed separately. In areas without stomata, maximum fluorescence yield (Fv / Fm) and quantum yield of photosystem II (Φ PSII) were significantly lower than in areas beneath stomata. In areas beneath stomata, Fv / Fm and Φ PSII were identical to levels measured in wild type leaves. At high light intensities over-expressers showed decreased photochemical quenching (qP) compared with wild types. However, the decrease of qP was significantly stronger in areas without stomata than in mesophyll areas beneath stomata. At high CO2 partial pressures and high light intensities CO2 assimilation rates of SDD1 over-expressers did not reach wild type levels. These results indicate that photosynthesis in SDD1 over-expressers was reduced because of limiting CO2 in areas furthest from stomata at high light.

Keywords: chlorophyll fluorescence, gas exchange, lateral diffusion, photosynthesis.


Acknowledgments

This work was supported by a grant from the DFG in the framework of the SFB 429 to TA. We thank the anonymous reviewers for their helpful and constructive comments.


References


Aalto T, Juurola E (2002) A three-dimensional model of CO2 transport in airspaces and mesophyll cells of a silver birch leaf. Plant, Cell & Environment 25, 1399–1409.
Crossref | GoogleScholarGoogle Scholar | open url image1

Araus JL, Alegre L, Tapia L, Calafell R, Serret MD (1986) Relationship between photosynthetic capacity and leaf structure in several shade plants. American Journal of Botany 73, 1760–1770.
Crossref | GoogleScholarGoogle Scholar | open url image1

Berger D, Altmann T (2000) A subtilisin-like protease involved in the regulation of stomatal density and distribution in Arabidopsis thaliana. Genes & Development 14, 1119–1131.
PubMed |
open url image1

Bergmann DC, Lukowitz W, Somerville CR (2004) Stomatal development and pattern controlled by a MAPKK kinase. Science 304, 1494–1497.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Coupe SA, Palmer BG, Lake JA, Overy SA, Oxborough K, Woodward FI, Gray JE, Quick WP (2006) Systemic signalling of environmental cues in Arabidopsis leaves. Journal of Experimental Botany 57, 329–341.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Cowan IR , Farquhar GD (1977) Stomatal function in relation to leaf metabolism and environment: stomatal function in the regulation of gas exchange. In ‘Symposium of the Society of Experimental Botany. Vol. 31’. (Ed. DH Jennings) pp. 471–505. (Cambridge University Press: Cambridge, UK)

Cummins WR, Kende H, Raschke K (1971) Specificity and reversibility of rapid stomatal response to abscisic acid. Planta 99, 347–351.
Crossref | GoogleScholarGoogle Scholar | open url image1

Evans JR (1999) Leaf anatomy enables more equal access to light and CO2 between chloroplasts. New Phytologist 143, 93–104.
Crossref | GoogleScholarGoogle Scholar | open url image1

Evans JR, von Caemmerer S (1996) Carbon dioxide diffusion inside leaves. Plant Physiology 110, 339–346.
PubMed |
open url image1

Farquhar GD, Sharkey TD (1982) Stomatal conductance and photosynthesis. Annual Review of Plant Physiology 33, 317–345.
Crossref | GoogleScholarGoogle Scholar | open url image1

Gay AP, Hurd RG (1975) The influence on light intensity on stomatal density in the tomato. New Phytologist 75, 37–46.
Crossref | GoogleScholarGoogle Scholar | open url image1

Gray JE, Holroyd GH, van der Lee FM, Bahrami AR, Sijmons PC, Woodward FI, Schuch W, Hetherington AM (2000) The HIC signalling pathway links CO2 perception to stomatal development. Nature 408, 713.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Heichel GH (1971) Stomatal movements, frequencies and resistances in two maize varieties differing in photosynthetic capacity. Journal of Experimental Botany 22, 644–649. open url image1

Jones HG (1987) Breeding for stomatal characters. In ‘Stomatal function’. (Eds E Zeiger, GD Farquhar, IR Cowan) pp. 431–443. (Stanford University Press: Palo Alto)

Jones HG (1998) Stomatal control of photosynthesis and transpiration. Journal of Experimental Botany 49, 387–398.
Crossref | GoogleScholarGoogle Scholar | open url image1

Kundu SK, Tigerstedt PMA (1998) Variation in net photosynthesis, stomatal characteristics, leaf area and whole-plant phytomass production among ten provenances of neem (Azadirachta indica). Tree Physiology 19, 47–52. open url image1

Marchi S, Tognetti R, Vaccari FP, Lanini M, Kaligaric M, Miglietta F, Raschi A (2004) Physiological and morphological responses of grassland species to elevated atmospheric CO2 concentrations in FACE-systems and natural CO2 springs. Functional Plant Biology 31, 181–194.
Crossref | GoogleScholarGoogle Scholar | open url image1

Miskin KE, Rasmussen DC (1970) Frequency and distribution of stomata in barley. Crop Science 10, 575–578. open url image1

Miskin KE, Rasmussen DC, Moss DN (1972) Inheritance and physiological effects of stomatal frequency in barley. Crop Science 12, 780–783. open url image1

Morison JIL, Gallouët E, Lawson T, Cornic G, Herbin R, Baker NR (2005) Lateral diffusion of CO2 in leaves is not sufficient to support photosynthesis. Plant Physiology 139, 254–266.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Muschak M, Hoffmann-Benning S, Fuss H, Koßmann J, Willmitzer L, Fisahn J (1997) Gas exchange and ultrastructural analysis of transgenic potato plants expressing a mRNA antisense construct targeted to the cp-fructose-1,6-bisphosphate phosphatase. Photosynthetica 33, 455–465. open url image1

Penuelas J, Matamala R (1990) Changes in N and S leaf content, stomatal density and specific leaf area of 14 plant species during the last three centuries of CO2 increase. Journal of Experimental Botany 41, 1119–1124. open url image1

Raschke K, Hedrich R (1985) Simultaneous and independent effects of abscisic acid on stomata and the photosynthetic apparatus in whole leaves. Planta 163, 105–118.
Crossref | GoogleScholarGoogle Scholar | open url image1

Schlüter U, Muschak M, Berger D, Altmann T (2003) Photosynthetic performance of an Arabidopsis mutant with elevated stomatal density (sdd1-1) under different light regimes. Journal of Experimental Botany 54, 867–874.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Schoch P-G, Zinsou C, Sibu M (1980) Dependence of the stomatal index on environmental factors during stomatal differentiation in leaves of Vigna sinensis L. Journal of Experimental Botany 31, 1211–1216. open url image1

Teare ID, Peterson CJ, Law AG (1971) Size and frequency of leaf stomata in cultivars of Triticum species. Crop Science 11, 496–498. open url image1

von Caemmerer S, Farquhar GD (1981) Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 153, 376–387.
Crossref | GoogleScholarGoogle Scholar | open url image1

von Groll U, Berger D, Altmann T (2002) The subtilisin-like serine protease SDD1 mediates cell-to-cell signalling during Arabidopsis stomatal development. The Plant Cell 14, 1527–1539.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Walton PD (1974) The genetics of stomatal length and frequency in clones of Bromus inermis and the relationships between these traits and yield. Canadian Journal of Plant Science 54, 749–754. open url image1

Willmer C , Fricker M (1996) ‘Topics in plant functional biology, 2. Stomata.’ 2nd edn. (Chapman and Hall Ltd.: London)

Woodward FI (1987) Stomatal numbers are sensitive to increases in CO2 from preindustrial levels. Nature 327, 617–618.
Crossref | GoogleScholarGoogle Scholar | open url image1

Woodward FI, Kelly CK (1995) The influence of CO2 concentration on stomatal density. New Phytologist 131, 311–327.
Crossref | GoogleScholarGoogle Scholar | open url image1