Light acclimation of photosynthesis in two closely related firs (Abies pinsapo Boiss. and Abies alba Mill.): the role of leaf anatomy and mesophyll conductance to CO2.

Leaves growing in the forest understory usually present a decreased mesophyll conductance (gm) and photosynthetic capacity. The role of leaf anatomy in determining the variability in gm among species is known, but there is a lack of information on how the acclimation of gm to shade conditions is driven by changes in leaf anatomy. Within this context, we demonstrated that Abies pinsapo Boiss. experienced profound modifications in needle anatomy to drastic changes in light availability that ultimately led to differential photosynthetic performance between trees grown in the open field and in the forest understory. In contrast to A. pinsapo, its congeneric Abies alba Mill. did not show differences either in needle anatomy or in photosynthetic parameters between trees grown in the open field and in the forest understory. The increased gm values found in trees of A. pinsapo grown in the open field can be explained by occurrence of stomata at both needle sides (amphistomatous needles), increased chloroplast surface area exposed to intercellular airspace, decreased cell wall thickness and, especially, decreased chloroplast thickness. To the best of our knowledge, the role of such drastic changes in ultrastructural needle anatomy in explaining the response of gm to the light environment has not been demonstrated in field conditions.

[1]  T. Sharkey,et al.  The arc mutants of Arabidopsis with fewer large chloroplasts have a lower mesophyll conductance , 2015, Photosynthesis Research.

[2]  J. Flexas,et al.  Diffusional limitations explain the lower photosynthetic capacity of ferns as compared with angiosperms in a common garden study. , 2015, Plant, cell & environment.

[3]  Lea Hallik,et al.  A worldwide analysis of within-canopy variations in leaf structural, chemical and physiological traits across plant functional types. , 2015, The New phytologist.

[4]  Coping with low light under high atmospheric dryness: shade acclimation in a Mediterranean conifer (Abies pinsapo Boiss.). , 2014, Tree physiology.

[5]  J. Flexas,et al.  Leaf mesophyll conductance and leaf hydraulic conductance: an introduction to their measurement and coordination. , 2013, Journal of experimental botany.

[6]  J. Gago,et al.  Leaf responses to drought stress in Mediterranean accessions of Solanum lycopersicum: anatomical adaptations in relation to gas exchange parameters. , 2013, Plant, cell & environment.

[7]  J. Flexas,et al.  Importance of leaf anatomy in determining mesophyll diffusion conductance to CO2 across species: quantitative limitations and scaling up by models , 2013, Journal of experimental botany.

[8]  J. Flexas,et al.  Leaf anatomical properties in relation to differences in mesophyll conductance to CO(2) and photosynthesis in two related Mediterranean Abies species. , 2012, Plant, cell & environment.

[9]  B. Genty,et al.  Variable mesophyll conductance revisited: theoretical background and experimental implications. , 2012, Plant, cell & environment.

[10]  J. Flexas,et al.  Mesophyll diffusion conductance to CO2: an unappreciated central player in photosynthesis. , 2012, Plant science : an international journal of experimental plant biology.

[11]  Ü. Niinemets,et al.  Anatomical basis of vari tion in mesophyll resistance in eastern Australian sclero hylls : news of a long and winding path , 2012 .

[12]  P. Mullineaux,et al.  Photosynthetic Adaptation to Length of Day Is Dependent on S-Sulfocysteine Synthase Activity in the Thylakoid Lumen1[W] , 2012, Plant Physiology.

[13]  U. Niinemets,et al.  Developmental changes in mesophyll diffusion conductance and photosynthetic capacity under different light and water availabilities in Populus tremula: how structure constrains function. , 2012, Plant, cell & environment.

[14]  Shiwei Guo,et al.  Chloroplast downsizing under nitrate nutrition restrained mesophyll conductance and photosynthesis in rice (Oryza sativa L.) under drought conditions. , 2012, Plant & cell physiology.

[15]  H. Cochard,et al.  Hydraulic traits are associated with the distribution range of two closely related Mediterranean firs, Abies alba Mill. and Abies pinsapo Boiss. , 2011, Tree physiology.

[16]  K. Tu,et al.  Spatial variation in photosynthetic CO(2) carbon and oxygen isotope discrimination along leaves of the monocot triticale (Triticum × Secale) relates to mesophyll conductance and the Péclet effect. , 2011, Plant, cell & environment.

[17]  J. Galmés,et al.  Automated flow-based anion-exchange method for high-throughput isolation and real-time monitoring of RuBisCO in plant extracts. , 2011, Talanta.

[18]  Xin-Guang Zhu,et al.  The Mechanistic Basis of Internal Conductance: A Theoretical Analysis of Mesophyll Cell Photosynthesis and CO2 Diffusion1[W][OA] , 2011, Plant Physiology.

[19]  Ü. Niinemets,et al.  Leaf Functional Anatomy in Relation to Photosynthesis1 , 2010, Plant Physiology.

[20]  F. Morales,et al.  Self-shading in cork oak seedlings: Functional implications in heterogeneous light environments , 2010 .

[21]  Ü. Niinemets A review of light interception in plant stands from leaf to canopy in different plant functional types and in species with varying shade tolerance , 2010, Ecological Research.

[22]  J. Flexas,et al.  Role of mesophyll diffusion conductance in constraining potential photosynthetic productivity in the field. , 2009, Journal of experimental botany.

[23]  A. Granier,et al.  Seasonal time-course of gradients of photosynthetic capacity and mesophyll conductance to CO2 across a beech (Fagus sylvatica L.) canopy. , 2009, Journal of experimental botany.

[24]  Jaume Flexas,et al.  Mesophyll conductance to CO2: current knowledge and future prospects. , 2008, Plant, cell & environment.

[25]  A. Mori,et al.  Morphological acclimation to understory environments in Abies amabilis, a shade- and snow-tolerant conifer species of the Cascade Mountains, Washington, USA. , 2008, Tree physiology.

[26]  J. Flexas,et al.  Rapid variations of mesophyll conductance in response to changes in CO2 concentration around leaves. , 2007, Plant, cell & environment.

[27]  A. Sparrow,et al.  Plasticity in mesophyll volume fraction modulates light-acclimation in needle photosynthesis in two pines. , 2007, Tree physiology.

[28]  J. Flexas,et al.  Mesophyll conductance to CO2 in Arabidopsis thaliana. , 2007, The New phytologist.

[29]  Robert W. Pearcy,et al.  Responses of Plants to Heterogeneous Light Environments , 2007 .

[30]  T. Brodribb,et al.  Leaf Maximum Photosynthetic Rate and Venation Are Linked by Hydraulics1[W][OA] , 2007, Plant Physiology.

[31]  A. Abadı́a,et al.  Physiological performance of silver-fir (Abies alba Mill.) populations under contrasting climates near the south-western distribution limit of the species , 2007 .

[32]  J. Berry,et al.  Analysis of leakage in IRGA's leaf chambers of open gas exchange systems: quantification and its effects in photosynthesis parameterization. , 2007, Journal of experimental botany.

[33]  M. Tausz,et al.  Internal conductance to CO2 transfer of adult Fagus sylvatica: Variation between sun and shade leaves and due to free-air ozone fumigation , 2007 .

[34]  J. Flexas,et al.  Mesophyll conductance to CO 2 in Arabidopsis thaliana , 2007 .

[35]  T. Black,et al.  Low stomatal and internal conductance to CO2 versus Rubisco deactivation as determinants of the photosynthetic decline of ageing evergreen leaves. , 2006, Plant, cell & environment.

[36]  E. Dreyer,et al.  Temperature response of photosynthesis and internal conductance to CO2: results from two independent approaches. , 2006, Journal of experimental botany.

[37]  Ü. Niinemets,et al.  Structural determinants of leaf light-harvesting capacity and photosynthetic potentials , 2006 .

[38]  A. Cescatti,et al.  Leaf internal diffusion conductance limits photosynthesis more strongly in older leaves of Mediterranean evergreen broad‐leaved species , 2005 .

[39]  F. Magnani,et al.  Stomatal, mesophyll conductance and biochemical limitations to photosynthesis as affected by drought and leaf ontogeny in ash and oak trees , 2005 .

[40]  N. Holbrook,et al.  Leaf hydraulic capacity in ferns, conifers and angiosperms: impacts on photosynthetic maxima. , 2004, The New phytologist.

[41]  N. Holbrook,et al.  Diurnal depression of leaf hydraulic conductance in a tropical tree species , 2004 .

[42]  Nigel J. Livingston,et al.  On the need to incorporate sensitivity to CO2 transfer conductance into the Farquhar–von Caemmerer–Berry leaf photosynthesis model , 2004 .

[43]  J. Berry,et al.  A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species , 1980, Planta.

[44]  V. Vallejo,et al.  Cavitation, stomatal conductance, and leaf dieback in seedlings of two co-occurring Mediterranean shrubs during an intense drought. , 2003, Journal of experimental botany.

[45]  Ü. Niinemets,et al.  Controls on the emission of plant volatiles through stomata: A sensitivity analysis , 2003 .

[46]  P. Montpied,et al.  Plasticity of morphological and physiological traits in response to different levels of irradiance in seedlings of silver fir (Abies alba Mill) , 2003, Trees.

[47]  R. Zorer,et al.  Structural acclimation and radiation regime of silver fir (Abies alba Mill.) shoots along a light gradient , 2003 .

[48]  A. Bosabalidis,et al.  The relationships between CO2 transfer mesophyll resistance and photosynthetic efficiency in grapevine cultivars , 2003 .

[49]  Susanne von Caemmerer,et al.  Temperature Response of Mesophyll Conductance. Implications for the Determination of Rubisco Enzyme Kinetics and for Limitations to Photosynthesis in Vivo , 2002, Plant Physiology.

[50]  I. Terashima,et al.  The effect of growth irradiance on leaf anatomy and photosynthesis in Acer species differing in light demand , 2002 .

[51]  D. Ellsworth,et al.  Dependence of needle architecture and chemical composition on canopy light availability in three North American Pinus species with contrasting needle length. , 2002, Tree physiology.

[52]  P. Montpied,et al.  Temperature response of photosynthesis of silver fir (Abies alba Mill.) seedlings , 2002 .

[53]  Ü. Niinemets,et al.  Site fertility and the morphological and photosynthetic acclimation of Pinus sylvestris needles to light. , 2001, Tree physiology.

[54]  G. Grassi,et al.  Foliar morphological and physiological plasticity in Picea abies and Abies alba saplings along a natural light gradient. , 2001, Tree physiology.

[55]  V. Lieffers,et al.  Photosynthesis and carbon allocation of six boreal tree species grown in understory and open conditions. , 2001, Tree physiology.

[56]  T. Brodribb,et al.  Stem hydraulic supply is linked to leaf photosynthetic capacity: evidence from New Caledonian and Tasmanian rainforests , 2000 .

[57]  R. Valentini,et al.  In situ estimation of net CO2 assimilation, photosynthetic electron flow and photorespiration in Turkey oak (Q. cerris L.) leaves: diurnal cycles under different levels of water supply , 1995 .

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

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

[60]  G. Edwards,et al.  Relationship between photosystem II activity and CO2 fixation in leaves , 1992 .

[61]  T. Sharkey,et al.  Theoretical Considerations when Estimating the Mesophyll Conductance to CO(2) Flux by Analysis of the Response of Photosynthesis to CO(2). , 1992, Plant physiology.

[62]  M. Abrams,et al.  Leaf structural characteristics of 31 hardwood and conifer tree species in central Wisconsin: influence of light regime and shade-tolerance rank. , 1990 .

[63]  J. Briantais,et al.  The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence , 1989 .

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

[65]  S. B. Carpenter,et al.  A comparative study of leaf thickness among southern Appalachian hardwoods , 1981 .

[66]  M. M. Bradford A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. , 1976, Analytical biochemistry.

[67]  G. Aussenac Effets de conditions microclimatiques différentes sur la morphologie et la structure anatomique des aiguilles de quelques résineux , 1973 .

[68]  L. Leyton,et al.  Method for Measuring the Leaf Surface Area of Complex Shoots , 1971, Nature.