The leaf anatomy of a broad-leaved evergreen allows an increase in leaf nitrogen content in winter.

In temperate regions, evergreen species are exposed to large seasonal changes in air temperature and irradiance. They change photosynthetic characteristics of leaves responding to such environmental changes. Recent studies have suggested that photosynthetic acclimation is strongly constrained by leaf anatomy such as leaf thickness, mesophyll and chloroplast surface facing the intercellular space, and the chloroplast volume. We studied how these parameters of leaf anatomy are related with photosynthetic seasonal acclimation. We evaluated differential effects of winter and summer irradiance on leaf anatomy and photosynthesis. Using a broad-leaved evergreen Aucuba japonica, we performed a transfer experiment in which irradiance regimes were changed at the beginning of autumn and of spring. We found that a vacant space on mesophyll surface in summer enabled chloroplast volume to increase in winter. The leaf nitrogen and Rubisco content were higher in winter than in summer. They were correlated significantly with chloroplast volume and with chloroplast surface area facing the intercellular space. Thus, summer leaves were thicker than needed to accommodate mesophyll surface chloroplasts at this time of year but this allowed for increases in mesophyll surface chloroplasts in the winter. It appears that summer leaf anatomical characteristics help facilitate photosynthetic acclimation to winter conditions. Photosynthetic capacity and photosynthetic nitrogen use efficiency were lower in winter than in summer but it appears that these reductions were partially compensated by higher Rubisco contents and mesophyll surface chloroplast area in winter foliage.

[1]  K. Noguchi,et al.  The chloroplast avoidance response decreases internal conductance to CO2 diffusion in Arabidopsis thaliana leaves. , 2008, Plant, cell & environment.

[2]  K. Hikosaka,et al.  Costs and benefits of photosynthetic light acclimation by tree seedlings in response to gap formation , 2008, Oecologia.

[3]  K. Otsuki,et al.  Decrease in the capacity for RuBP carboxylation and regeneration with the progression of cold-induced photoinhibition during winter in evergreen broadleaf tree species in a temperate forest. , 2007, Functional plant biology : FPB.

[4]  K. Noguchi,et al.  Effects of internal conductance on the temperature dependence of the photosynthetic rate in spinach leaves from contrasting growth temperatures. , 2006, Plant & cell physiology.

[5]  K. Hikosaka,et al.  Leaf anatomy and light acclimation in woody seedlings after gap formation in a cool-temperate deciduous forest , 2006, Oecologia.

[6]  M. Kimura,et al.  Matter-economical roles of evergreen leaves inAucuba japonica, an understory shrub in the warm-temperate region of Japan , 1992, The botanical magazine = Shokubutsu-gaku-zasshi.

[7]  K. Hikosaka,et al.  Temperature acclimation of photosynthesis: mechanisms involved in the changes in temperature dependence of photosynthetic rate. , 2006, Journal of experimental botany.

[8]  Ichiro Terashima,et al.  Irradiance and phenotype: comparative eco-development of sun and shade leaves in relation to photosynthetic CO2 diffusion. , 2006, Journal of experimental botany.

[9]  N. Livingston,et al.  Stomatal development in new leaves is related to the stomatal conductance of mature leaves in poplar (Populus trichocarpaxP. deltoides). , 2006, Journal of experimental botany.

[10]  A. Makino,et al.  The photosynthetic properties of rice leaves treated with low temperature and high irradiance. , 2005, Plant & cell physiology.

[11]  K. Hikosaka Nitrogen partitioning in the photosynthetic apparatus of Plantago asiatica leaves grown under different temperature and light conditions: similarities and differences between temperature and light acclimation. , 2005, Plant & cell physiology.

[12]  K. Hikosaka,et al.  Leaf anatomy as a constraint for photosynthetic acclimation: differential responses in leaf anatomy to increasing growth irradiance among three deciduous trees , 2005 .

[13]  K. Noguchi,et al.  Temperature acclimation of photosynthesis in spinach leaves: analyses of photosynthetic components and temperature dependencies of photosynthetic partial reactions , 2005 .

[14]  M. Naramoto,et al.  Photosynthetic acclimation to dynamic changes in environmental conditions associated with deciduous overstory phenology in Daphniphyllum humile, an evergreen understory shrub. , 2005, Tree physiology.

[15]  K. Hikosaka,et al.  Seasonal changes in light and temperature affect the balance between light harvesting and light utilisation components of photosynthesis in an evergreen understory shrub , 2005, Oecologia.

[16]  K. Kikuzawa,et al.  Winter photosynthesis by saplings of evergreen broad-leaved trees in a deciduous temperate forest. , 2004, The New phytologist.

[17]  K. Hikosaka Interspecific difference in the photosynthesis–nitrogen relationship: patterns, physiological causes, and ecological importance , 2004, Journal of Plant Research.

[18]  K. Hikosaka,et al.  Photosynthetic rates and partitioning of absorbed light energy in photoinhibited leaves , 2004 .

[19]  Takashi Nakano,et al.  Spatial and seasonal variability of temperature responses of biochemical photosynthesis parameters and leaf nitrogen content within a Pinus densiflora crown. , 2004, Tree physiology.

[20]  M. Adams,et al.  Evergreen trees do not maximize instantaneous photosynthesis. , 2004, Trends in plant science.

[21]  C. Osmond,et al.  Contrasting patterns of photosynthetic acclimation and photoinhibition in two evergreen herbs from a winter deciduous forest , 1996, Oecologia.

[22]  C. Field,et al.  Allocating leaf nitrogen for the maximization of carbon gain: Leaf age as a control on the allocation program , 1983, Oecologia.

[23]  J. R. Evans Photosynthesis and nitrogen relationships in leaves of C3 plants , 2004, Oecologia.

[24]  W. W. Adams,et al.  Photoprotective Strategies of Overwintering Evergreens , 2004 .

[25]  Tadaki Hirose,et al.  Does the photosynthetic light-acclimation need change in leaf anatomy? , 2003 .

[26]  Masahiro Kasahara,et al.  Chloroplast avoidance movement reduces photodamage in plants , 2002, Nature.

[27]  I. Terashima,et al.  Separate localization of light signal perception for sun or shade type chloroplast and palisade tissue differentiation in Chenopodium album. , 2001, Plant & cell physiology.

[28]  D. Zak,et al.  Photosynthetic adaptation and acclimation to exploit seasonal periods of direct irradiance in three temperate, deciduous-forest herbs , 2001 .

[29]  M. Adams,et al.  Distribution of N, Rubisco and photosynthesis in Pinus pinaster and acclimation to light , 2001 .

[30]  M. Weih,et al.  Growth response of Mountain birch to air and soil temperature: is increasing leaf‐nitrogen content an acclimation to lower air temperature? , 2001 .

[31]  I. Terashima,et al.  Why are Sun Leaves Thicker than Shade Leaves? — Consideration based on Analyses of CO2 Diffusion in the Leaf , 2001, Journal of Plant Research.

[32]  I. Terashima,et al.  Acclimation of leaf characteristics of Fagus species to previous-year and current-year solar irradiances. , 2000, Tree physiology.

[33]  I. E. Woodrow,et al.  Modelling the role of Rubisco activase in limiting non-steady-state photosynthesis. , 2000, Journal of experimental botany.

[34]  K. Hikosaka,et al.  Balancing carboxylation and regeneration of ribulose‐1,5‐ bisphosphate in leaf photosynthesis: temperature acclimation of an evergreen tree, Quercus myrsinaefolia , 1999 .

[35]  K. Hikosaka,et al.  Photosynthetic nitrogen‐use efficiency in leaves of woody and herbaceous species , 1998 .

[36]  G. Öquist,et al.  Energy balance and acclimation to light and cold , 1998 .

[37]  J. R. Evans,et al.  The Relationship Between CO2 Transfer Conductance and Leaf Anatomy in Transgenic Tobacco With a Reduced Content of Rubisco , 1994 .

[38]  D. Sims,et al.  Response of leaf anatomy and photosynthetic capacity in Alocasia macrorrhiza (Araceae) to a transfer from low to high light. , 1992 .

[39]  John R. Evans,et al.  Determination of the Average Partial Pressure of CO2 in Chloroplasts From Leaves of Several C3 Plants , 1991 .

[40]  J. Thain Curvature Correction Factors in the Measurement of Cell Surface Areas in Plant Tissues1 , 1983 .

[41]  O. Björkman Responses to Different Quantum Flux Densities , 1981 .

[42]  J. Berry,et al.  Photosynthetic Response and Adaptation to Temperature in Higher Plants , 1980 .

[43]  S. Tsunoda,et al.  Effect of low temperature on chloroplast structure in cultivars of rice , 1979 .