The geometry of light interception by shoots of Heteromeles arbutifolia: morphological and physiological consequences for individual leaves

Abstract The influence of leaf orientation and position within shoots on individual leaf light environments, carbon gain, and susceptibility to photoinhibition was studied in the California chaparral shrub Heteromeles arbutifolia with measurements of gas exchange and chlorophyll fluorescence, and by application of a three-dimensional canopy architecture model. Simulations of light absorption and photosynthesis revealed a complex pattern of leaf light environments and resulting leaf carbon gain within the shoots. Upper, south-facing leaves were potentially the most productive because they intercepted greater daily photon flux density (PFD) than leaves of any other orientation. North-facing leaves intercepted less PFD but of this, more was received on the abaxial surface because of the steep leaf angles. Leaves differed in their response to abaxial versus adaxial illumination depending on their orientation. While most had lower photosynthetic rates when illuminated on their abaxial as compared to adaxial surface, the photosynthetic rates of north-facing leaves were independent of the surface of illumination. Because of the increasing self-shading, there were strong decreases in absorbed PFD and daily carbon gain in the basipetal direction. Leaf nitrogen per unit mass also decreased in the basipetal direction but on a per unit area basis was nearly constant along the shoot. The decrease in leaf N per unit mass was accounted for by an increase in leaf mass per unit area (LMA) rather than by movement of N from older to younger leaves during shoot growth. The increased LMA of older lower leaves may have contributed directly to their lower photosynthetic capacities by increasing the limitations to diffusion of CO2 within the leaf to the sites of carboxylation. There was no evidence for sun/shade acclimation along the shoot. Upper leaves and especially south-facing upper leaves had a potential risk for photoinhibition as demonstrated by the high PFDs received and the diurnal decreases in the fluorescence ratio Fv/Fm. Predawn Fv/Fm ratios remained high (>0.8) indicating that when in their normal orientations leaves sustained no photoinhibition. Reorientation of the leaves to horizontal induced a strong sustained decrease in Fv/Fm and CO2 exchange that slowly recovered over the next 10–15 days. If leaves were also inverted so that the abaxial surface received the increased PFDs, then the reduction in Fv/Fm and CO2 assimilation was much greater with no evidence for recovery. The heterogeneity of responses was due to a combination of differences between leaves of different orientation, differences between responses on their abaxial versus adaxial surfaces, and differences along the shoot due to leaf age and self-shading effects.

[1]  Ichiro Terashima,et al.  Dorsiventrality in Photosynthetic Light Response Curves of a Leaf , 1986 .

[2]  R. W. Pearcy,et al.  Interactions between Acclimation and Photoinhibition of Photosynthesis of a Tropical Forest Understorey Herb, Alocasia macrorrhiza, during Simulated Canopy Gap Formation , 1992 .

[3]  M. A. Wolf,et al.  Portable monitor for solar radiation that accumulates irradiance histograms for 32 leaf-mounted sensors , 1985 .

[4]  C. Ascaso,et al.  Past, present and future methods of quantification in anatomical and ultrastructural studies of lichens , 1994 .

[5]  D. F. Parkhurst,et al.  Intercellular Diffusion Limits to CO(2) Uptake in Leaves : Studies in Air and Helox. , 1990, Plant physiology.

[6]  I. Terashima.  Productive structure of a leaf , 1989 .

[7]  Robert W. Pearcy,et al.  Interactions between water stress, sun-shade acclimation, heat tolerance and photoinhibition in the sclerophyll Heteromeles arbutifolia , 1997 .

[8]  Robert W. Pearcy,et al.  The functional ecology of shoot architecture in sun and shade plants of Heteromeles arbutifolia M. Roem., a Californian chaparral shrub , 1998, Oecologia.

[9]  I. E. Woodrow,et al.  A Model Predicting Stomatal Conductance and its Contribution to the Control of Photosynthesis under Different Environmental Conditions , 1987 .

[10]  Fernando Valladares,et al.  Tradeoffs Between Irradiance Capture and Avoidance in Semi-arid Environments Assessed with a Crown Architecture Model , 1999 .

[11]  D. R. Causton,et al.  Use of the chlorophyll a/b ratio as a bioassay for the light environment of a plant , 1992 .

[12]  Thomas J. Givnish,et al.  Adaptation to Sun and Shade: a Whole-Plant Perspective , 1988 .

[13]  B. Demmig‐Adams,et al.  The role of xanthophyll cycle carotenoids in the protection of photosynthesis , 1996 .

[14]  S. von Caemmerer,et al.  Carbon Dioxide Diffusion inside Leaves , 1996, Plant physiology.

[15]  Paul G. Falkowski,et al.  Photoinhibition of Photosynthesis in Nature , 1994 .

[16]  R. W. Pearcy,et al.  Seasonal progressions of tissue and cell water relations parameters in evergreen and deciduous perennials , 1984 .

[17]  Arana,et al.  Progress in Photosynthesis Research , 1987, Springer Netherlands.

[18]  D. Hollinger.  Leaf and Simulated Whole‐Canopy Photosynthesis in Two Co‐Occurring Tree Species , 1992 .

[19]  John R. Evans,et al.  Partitioning of Nitrogen Between and Within Leaves Grown Under Different Irradiances , 1989 .

[20]  J. Gamon,et al.  Photoinhibition in Vitis californica: The Role of Temperature during High-Light Treatment. , 1990, Plant physiology.

[21]  G. Farquhar,et al.  On the relationship between leaf anatomy and CO2 diffusion through the mesophyll of hypostomatous leaves , 1995 .

[22]  Ü. Niinemets,et al.  Acclimation to low irradiance in Picea abies: influences of past and present light climate on foliage structure and function. , 1997, Tree physiology.

[23]  Fernando Valladares,et al.  THE ROLE OF CROWN ARCHITECTURE FOR LIGHT HARVESTING AND CARBON GAIN IN EXTREME LIGHT ENVIRONMENTS ASSESSED WITH A REALISTIC 3-D MODEL , 2000 .

[24]  J. Tenhunen,et al.  Ecological implications of sun/shade-leaf differentiation in sclerophyllous canopies: Assessment by canopy modeling , 1987 .