Hydraulically based stomatal oscillations and stomatal patchiness in Gossypium hirsutum
Ricardo A. Marenco A C , Katharina Siebke B , Graham D. Farquhar A D and Marilyn C. Ball BA Environmental Biology Group, Research School of Biological Sciences, The Australian National University, Canberra, ACT 0200, Australia.
B Ecosystem Dynamics Group, Research School of Biological Sciences, The Australian National University, Canberra, ACT 0200, Australia.
C Coordenação de Pesquisas em Silvicultura Tropical, Instituto Nacional de Pesquisas da Amazônia — INPA-CPST. Bolsista do CNPq. PO Box 478, Manaus, AM, Brazil 69010-970.
D Corresponding author. Email: Graham.Farquhar@anu.edu.au
Functional Plant Biology 33(12) 1103-1113 https://doi.org/10.1071/FP06115
Submitted: 9 May 2006 Accepted: 21 September 2006 Published: 1 December 2006
Abstract
Slow stomatal oscillations (70–95 min), associated with feedback within the plant hydraulic systems, were studied in cotton (Gossypium hirsutum L.). Oscillations were only evident when the whole plant was exposed to light, and were not influenced by reductions in intercellular CO2 concentrations (Ci) in intact, attached leaves. Oscillations were synchronised among different leaves of the same plant, even when the leaf-to-air vapour pressure difference (VPD) was reduced in a cuvette enclosing one of the leaves. In the trough phase of stomatal oscillations the apparent Ci was higher than expected from the combination of the observed assimilation rate and the A(Ci) relationship measured in the absence of oscillations. Using chlorophyll fluorescence imaging we found evidence of stomatal heterogeneity in this phase. Finally, we found that stomatal oscillations appeared to be correlated with xylem embolism, with more vessels filled with gas at the peak than at the troughs of stomatal oscillations.
Keywords: chlorophyll fluorescence, photosynthesis, stomatal conductance, xylem embolism.
Acknowledgments
We thank Drs Chen Huang and Roger Heady for technical support at the Electron Microscopy Unit, RSBS, ANU, and Prof. Martin Canny, Dr Dan Bruhn, Dr John Evans, Jack Egerton and Katherine Martin for constructive advice. RAM is deeply grateful to The Australian National University, the Instituto Nacional de Pesquisas da Amazônia and the Conselho Nacional de Desenvolvimento Científico e Tecnológico — INPA / CNPq, Brazil for their support.
Barrs HD
(1971) Cyclic variations in stomatal aperture, transpiration, and leaf water potential under constant environmental conditions. Annual Review of Plant Physiology 22, 223–236.
| Crossref | GoogleScholarGoogle Scholar |
Barrs HD, Klepper B
(1968) Cyclic variations in plant properties under constant environmental conditions. Physiologia Plantarum 21, 711–730.
| Crossref | GoogleScholarGoogle Scholar |
Beator J, Kloppstech K
(1996) Significance of circadian gene expression in higher plants. Chronobiology International 13, 319–339.
| PubMed |
Beyschlag W, Eckstein J
(2001) Towards a causal analysis of stomatal patchiness: the role of stomatal size variability and hydrological heterogeneity. Acta Oecologica 22, 161–173.
| Crossref | GoogleScholarGoogle Scholar |
Canny MJ
(1998) Applications of the compensating pressure theory of water transport. American Journal of Botany 85, 897–909.
| Crossref | GoogleScholarGoogle Scholar |
Cardon ZG,
Mott KA, Berry JA
(1994) Dynamics of patchy stomatal movements, and their contribution to steady-state and oscillating stomatal conductance calculated using gas-exchange techniques. Plant, Cell & Environment 17, 995–1007.
| Crossref | GoogleScholarGoogle Scholar |
Clarkson DT,
Carvajal M,
Henzler T,
Waterhouse RN,
Smyth AJ,
Cooke DT, Steudle E
(2000) Root hydraulic conductance: diurnal aquaporin expression and the effects of nutrient stress. Journal of Experimental Botany 51, 61–70.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Cowan IR
(1972) Oscillations in stomatal conductance and plant functioning associated with stomatal conductance. Observations and a model. Planta 106, 185–219.
| Crossref |
Cowan IR, Farquhar GD
(1977) Stomatal function in relation to leaf metabolism and environment. Symposia of the Society for Experimental Biology 31, 471–505.
| PubMed |
Cox EF
(1968) Cyclic exchanges in transpiration of sunflower leaves in a steady environment. Journal of Experimental Botany 19, 167–175.
Downton JW,
Loveys BR, Grant WJR
(1988) Stomatal closure fully accounts for the inhibition of photosynthesis by abscisic acid. New Phytologist 108, 263–266.
| Crossref | GoogleScholarGoogle Scholar |
Farquhar GD
(1989) Models of integrated photosynthesis of cells and leaves. Philosophical Transactions of the Royal Society (Series B) 323, 357–368.
Farquhar GD, Cowan IR
(1974) Oscillations in stomatal conductance. Plant Physiology 54, 769–772.
| PubMed |
Farquhar GD,
Dubbe DR, Raschke K
(1978) Gain of the feedback loop involving carbon dioxide and stomata. Theory and measurement. Plant Physiology 62, 406–412.
| PubMed |
Henzler T,
Waterhouse RN,
Smyth AJ,
Carvajal M,
Cooke DT,
Schaffner AR,
Steudle E, Clarkson DT
(1999) Diurnal variations in hydraulic conductivity and root pressure can be correlated with the expression of putative aquaporins in the roots of Lotus japonicus. Planta 210, 50–60.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Holbrook NM, Zwieniecki MA
(1999) Embolism repair and xylem tension: do we need a miracle? Plant Physiology 120, 7–10.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Iwanoff L
(1928) Zur Methodik der Transpirations-bestimmung am Standort. Berichte Deutsche Botanische Gesellschaft 46, 306–310.
Jarvis AJ,
Young PC,
Taylor CJ, Davies WJ
(1999) An analysis of the dynamic response of stomatal conductance to a reduction in humidity over leaves of Cedrella odorata. Plant, Cell & Environment 22, 913–924.
| Crossref | GoogleScholarGoogle Scholar |
Kanemasu ET, Tanner CB
(1969) Stomatal diffusion resistance of snap bean. II. Effect of light. Plant Physiology 44, 1542–1546.
| PubMed |
Laisk A
(1983) Calculation of leaf photosynthetic parameters considering the statistical distribution of stomatal apertures. Journal of Experimental Botany 34, 1627–1635.
Laisk A,
Oja V, Kull K
(1980) Statistical distribution of stomatal apertures of Vicia faba and Hordeum vulgare and the Spannungsphase of stomatal opening. Journal of Experimental Botany 31, 49–58.
Lopez M,
Bousser A,
Sissoeff I,
Gaspar M,
Lachaise B,
Hoarau J, Mahe A
(2003) Diurnal regulation of water transport and aquaporin gene expression in maize roots: contribution of PIP2 proteins. Plant & Cell Physiology 44, 1384–1395.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Martin ES, Meidner H
(1971) Endogenous stomatal movements in Tradescantia virginiana. New Phytologist 70, 923–928.
| Crossref | GoogleScholarGoogle Scholar |
Meidner H, Willmer CM
(1993) Circadian rhythm of stomatal movements in epidermal strips. Journal of Experimental Botany 44, 1649–1652.
Mott KA
(1988) Do stomata respond to CO2 concentrations other than intercellular? Plant Physiology 86, 200–203.
| PubMed |
Nardini A, Salleo S
(2000) Limitation of stomatal conductance by hydraulic traits: sensing or preventing xylem cavitation? Trees — Structure and Function 15, 14–24.
| Crossref | GoogleScholarGoogle Scholar |
Omasa K, Takayama K
(2003) Simultaneous measurement of stomatal conductance, non-photochemical quenching, and photochemical yield of photosystem II in intact leaves by thermal and chlorophyll fluorescence imaging. Plant & Cell Physiology 44, 1290–1300.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Raschke K, Kühl U
(1969) Stomatal responses to change in atmospheric humidity and water supply: Experiment with leaf sections of Zea mays in CO2-free air. Planta 87, 36–48.
| Crossref | GoogleScholarGoogle Scholar |
Salleo S,
Lo Gullo MA,
Trifilò P, Nardini A
(2004) New evidence for a role of vessel-associated cells and phloem in the rapid refilling of cavitated stems of Laurus nobilis L. Plant, Cell & Environment 27, 1065–1076.
| Crossref | GoogleScholarGoogle Scholar |
Stålfelt MG
(1929) Die Abhngigkeit der Spaltoffnungsreaktionen von der Wasserbilanz. Planta 8, 287–296.
| Crossref | GoogleScholarGoogle Scholar |
Teoh CT, Palmer JH
(1971) Nonsynchronized oscillations in stomatal resistance among sclerophylls of Eucalyptus umbra. Plant Physiology 47, 409–411.
| PubMed |
Terashima I,
Wong SC,
Osmond CB, Farquhar GD
(1988) Characterization of non-uniform photosynthesis induced by abscisic acid in leaves having different mesophyll anatomies. Plant & Cell Physiology 29, 385–394.
Troughton JH
(1969) Plant water status and carbon dioxide exchange of cotton leaves. Australian Journal of Biological Sciences 22, 289–302.
Tyree M, Sperry J
(1988) Do woody-plants operate near the point of catastrophic xylem dysfunction caused by dynamic water-stress? Plant Physiology 88, 574–580.
| PubMed |
Wang GX,
Zhang J,
Liao JX, Wang JL
(2001) Hydropassive evidence and effective factors in stomatal oscillations of Glycyrrhiza inflata under desert conditions. Plant Science 160, 1007–1013.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
West JD,
Peak D,
Peterson JQ, Mott KA
(2005) Dynamics of stomatal patches for a single surface of Xanthium strumarium L. leaves observed with fluorescence and thermal images. Plant, Cell & Environment 28, 633–641.
| Crossref | GoogleScholarGoogle Scholar |
Williams WE, Gorton HL
(1998) Circadian rhythms have insignificant effects on plant gas exchange under field conditions. Physiologia Plantarum 103, 247–256.
| Crossref | GoogleScholarGoogle Scholar |
Zipperlen SW, Press MC
(1997) Photosynthetic induction and stomatal oscillations in relation to the light environment of two dipterocarp rain forest tree species. Journal of Ecology 85, 491–503.
| Crossref | GoogleScholarGoogle Scholar |
