Photosynthesis-dependent and -independent responses of stomata to blue, red and green monochromatic light: differences between the normally oriented and inverted leaves of sunflower.

The effects of growth light environment on stomatal light responses were analyzed. We inverted leaves of sunflower (Helianthus annuus) for 2 weeks until their full expansion, and measured gas exchange properties of the adaxial and abaxial sides separately. The sensitivity to light assessed as the increase in stomatal conductance was generally higher in the abaxial stomata than in the adaxial stomata, and these differences could not be completely changed by the inversion treatment. We also treated the leaves with DCMU to inhibit photosynthesis and evaluated the photosynthesis-dependent and -independent components of stomatal light responses. The red light response of stomata in both normally oriented and inverted leaves relied only on the photosynthesis-dependent component. The blue light response involved both the photosynthesis-dependent and photosynthesis-independent components, and the relative contributions of the two components differed between the normally oriented and inverted leaves. A green light response was observed only in the abaxial stomata, which also involved the photosynthesis-dependent and photosynthesis-independent components, strongly suggesting the existence of a green light receptor in sunflower leaves. Moreover, acclimation of the abaxial stomata to strong direct light eliminated the photosynthesis-independent component in the green light response. The results showed that stomatal responses to monochromatic light change considerably in response to growth light environment, although some of these responses appear to be determined inherently.

[1]  S. Driscoll,et al.  Specification of adaxial and abaxial stomata, epidermal structure and photosynthesis to CO2 enrichment in maize leaves. , 2006, Journal of experimental botany.

[2]  M. Ahmad,et al.  Expression of an Arabidopsis cryptochrome gene in transgenic tobacco results in hypersensitivity to blue, UV-A, and green light. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[3]  K. Shimazaki,et al.  The Stomata of the Fern Adiantum capillus-veneris Do Not Respond to CO 2 in the Dark and Open by Photosynthesis , 2008 .

[4]  T. Sharkey,et al.  Separation and measurement of direct and indirect effects of light on stomata. , 1981, Plant physiology.

[5]  T. Lawson,et al.  Stomatal conductance does not correlate with photosynthetic capacity in transgenic tobacco with reduced amounts of Rubisco. , 2004, Journal of experimental botany.

[6]  L. D. Talbott,et al.  Green light reversal of blue-light-stimulated stomatal opening is found in a diversity of plant species. , 2002, American journal of botany.

[7]  G. Farquhar,et al.  Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves , 1981, Planta.

[8]  L. D. Talbott,et al.  The guard cell chloroplast: a perspective for the twenty-first century. , 2002, The New phytologist.

[9]  S. Driscoll,et al.  Adaxial/abaxial specification in the regulation of photosynthesis and stomatal opening with respect to light orientation and growth with CO2 enrichment in the C4 species Paspalum dilatatum. , 2007, The New phytologist.

[10]  K. Folta,et al.  Green light: a signal to slow down or stop. , 2007, Journal of experimental botany.

[11]  Ichiro Terashima,et al.  Comparative ecophysiology of leaf and canopy photosynthesis , 1995 .

[12]  M. A. Pemadasa DIFFERENTIAL ABAXIAL AND ADAXIAL STOMATAL RESPONSES TO INDOLE‐3‐ACETIC ACID IN COMMELINA COMMUNIS L. , 1982 .

[13]  T. Kinoshita,et al.  Guard-cell chloroplasts provide ATP required for H(+) pumping in the plasma membrane and stomatal opening. , 2001, Plant & cell physiology.

[14]  A. Travis,et al.  Light Saturation of Stomatal Opening on the Adaxial and Abaxial Epidermis of Commelina communis , 1981 .

[15]  I. R. Cowan,et al.  Leaf Conductance in Relation to Rate of CO(2) Assimilation: I. Influence of Nitrogen Nutrition, Phosphorus Nutrition, Photon Flux Density, and Ambient Partial Pressure of CO(2) during Ontogeny. , 1985, Plant physiology.

[16]  Toshinori Kinoshita,et al.  Blue light activates the plasma membrane H+‐ATPase by phosphorylation of the C‐terminus in stomatal guard cells , 1999, The EMBO journal.

[17]  Susanne von Caemmerer,et al.  The Contribution of Photosynthesis to the Red Light Response of Stomatal Conductance1[OA] , 2007, Plant Physiology.

[18]  Tracy Lawson,et al.  Guard cell photosynthesis and stomatal function. , 2009, The New phytologist.

[19]  K. Shimazaki,et al.  Cyclic and Noncyclic Photophosphorylation in Isolated Guard Cell Chloroplasts from Vicia faba L. , 1985, Plant physiology.

[20]  Harry Smith,et al.  THE FUNCTION OF PHYTOCHROME IN THE NATURAL ENVIRONMENT—II. THE INFLUENCE OF VEGETATION CANOPIES ON THE SPECTRAL ENERGY DISTRIBUTION OF NATURAL DAYLIGHT , 1977 .

[21]  K. Noguchi,et al.  Distinct light responses of the adaxial and abaxial stomata in intact leaves of Helianthus annuus L. , 2008, Plant, cell & environment.

[22]  Tracy Lawson,et al.  Responses of photosynthetic electron transport in stomatal guard cells and mesophyll cells in intact leaves to light, CO2, and humidity. , 2002, Plant physiology.

[23]  K. Shimazaki,et al.  Photosynthetic Properties of Guard Cell Protoplasts from Vicia faba L. , 1982 .

[24]  J. E. Dale Investigations into the Stomatal Physiology of Upland Cotton 2. Calibration of the Infiltration Method against Leaf and Stomatal Resistances , 1961 .

[25]  N. Turner RESPONSE OF ADAXIAL AND ABAXIAL STOMATA TO LIGHT , 1970 .

[26]  A. Melis,et al.  Fluorescence Properties of Guard Cell Chloroplasts: EVIDENCE FOR LINEAR ELECTRON TRANSPORT AND LIGHT-HARVESTING PIGMENTS OF PHOTOSYSTEMS I AND II. , 1981, Plant physiology.

[27]  E. Zeiger,et al.  Light quality and osmoregulation in vicia guard cells : evidence for involvement of three metabolic pathways. , 1988, Plant physiology.

[28]  L. D. Talbott,et al.  The role of sucrose in guard cell osmoregulation , 1998 .

[29]  A. Schwartz,et al.  Metabolic energy for stomatal opening. Roles of photophosphorylation and oxidative phosphorylation , 1984, Planta.

[30]  S. Davis,et al.  Responses of Adaxial and Abaxial Stomata of Normally Oriented and Inverted Leaves of Vicia faba L. to Light. , 1986, Plant physiology.

[31]  K. Mott,et al.  Do Stomata Respond to CO(2) Concentrations Other than Intercellular? , 1988, Plant physiology.

[32]  Chentao Lin,et al.  Photoexcited CRY2 Interacts with CIB1 to Regulate Transcription and Floral Initiation in Arabidopsis , 2008, Science.

[33]  L. D. Talbott,et al.  Reversal by green light of blue light-stimulated stomatal opening in intact, attached leaves of Arabidopsis operates only in the potassium-dependent, morning phase of movement. , 2006, Plant & cell physiology.

[34]  Alain Vavasseur,et al.  Guard cell metabolism and CO2 sensing. , 2005, The New phytologist.

[35]  T. Sharkey,et al.  Effect of Light Quality on Stomatal Opening in Leaves of Xanthium strumarium L. , 1981, Plant physiology.

[36]  M. Quiñones,et al.  Abaxial and adaxial stomata from Pima cotton (Gossypium barbadense L.) differ in their pigment content and sensitivity to light quality , 1993 .

[37]  G. Tallman The chemiosmotic model of stomatal opening revisited , 1992 .

[38]  Ken-ichiro Shimazaki,et al.  phot1 and phot2 mediate blue light regulation of stomatal opening , 2001, Nature.

[39]  K. Mott,et al.  Evidence for Involvement of Photosynthetic Processes in the Stomatal Response to CO21 , 2006, Plant Physiology.

[40]  R. Klein EFFECTS OF GREEN LIGHT ON BIOLOGICAL SYSTEMS , 1992, Biological reviews of the Cambridge Philosophical Society.

[41]  S. Assmann,et al.  Is ATP Required for K+ Channel Activation in Vicia Guard Cells? , 1995, Plant physiology.

[42]  K. Shimazaki,et al.  The Stomata of the Fern Adiantum capillus-veneris Do Not Respond to CO2 in the Dark and Open by Photosynthesis in Guard Cells1[OA] , 2008, Plant Physiology.

[43]  R. Bogomolni,et al.  Reversal of blue light-stimulated stomatal opening by green light. , 2000, Plant & cell physiology.

[44]  J. E. Dale,et al.  Investigations into the Stornatal Physiology of Upland Cotton I. The Effects of Hour of Day, Solar Radiation, Temperature and Leaf Water-Content on Stomatal Behaviour , 1961 .

[45]  M. Ahmad,et al.  Association of flavin adenine dinucleotide with the Arabidopsis blue light receptor CRY1 , 1995, Science.

[46]  R. Pratt,et al.  Red light activates a chloroplast-dependent ion uptake mechanism for stomatal opening under reduced CO2 concentrations in Vicia spp. , 2002, The New phytologist.

[47]  M. A. Pemadasa MOVEMENTS OF ABAXIAL AND ADAXIAL STOMATA , 1979 .

[48]  R. Hedrich,et al.  CO2 provides an intermediate link in the red light response of guard cells. , 2002, The Plant journal : for cell and molecular biology.

[49]  J. Miller,et al.  Effect of Colored Light on Stomatal Opening Rates of Vicia faba L. , 1977, Plant Physiology.

[50]  S. Assmann,et al.  Light regulation of stomatal movement. , 2007, Annual review of plant biology.

[51]  N. Turner,et al.  RESPONSES OF ADAXIAL AND ABAXIAL STOMATA TO LIGHT AND WATER DEFICITS IN SUNFLOWER AND SORGHUM , 1984 .

[52]  S. Anagnostakis,et al.  Stomatal Response to Light of Solanum pennellii, Lycopersicon esculentum, and a Graft-induced Chimera. , 1978, Plant physiology.

[53]  J. Berry,et al.  Effects of O(2) and CO(2) Concentration on the Steady-State Fluorescence Yield of Single Guard Cell Pairs in Intact Leaf Discs of Tradescantia albiflora: Evidence for Rubisco-Mediated CO(2) Fixation and Photorespiration in Guard Cells. , 1992, Plant physiology.

[54]  T. Lawson,et al.  Reductions in mesophyll and guard cell photosynthesis impact on the control of stomatal responses to light and CO2 , 2008, Journal of experimental botany.

[55]  T. Oku,et al.  Properties of Proton Pumping in Response to Blue Light and Fusicoccin in Guard Cell Protoplasts Isolated from Adaxial Epidermis of Vicia Leaves , 1995, Plant physiology.

[56]  H. Nam,et al.  Parallel recordings of photosynthetic electron transport and K+-channel activity in single guard cells. , 2002, The Plant journal : for cell and molecular biology.

[57]  Takeshi Inoue,et al.  Green light drives leaf photosynthesis more efficiently than red light in strong white light: revisiting the enigmatic question of why leaves are green. , 2009, Plant & cell physiology.

[58]  K. Shimazaki,et al.  Photosynthetic properties of adaxial guard cells from Vicia leaves , 1997 .