Cell-level anatomical characteristics explain high mesophyll conductance and photosynthetic capacity in sclerophyllous Mediterranean oaks.

Leaf mass per area (LMA) has been suggested to negatively affect the mesophyll conductance to CO2 (gm ), which is the most limiting factor for area-based photosynthesis (AN ) in many Mediterranean sclerophyll species. However, despite their high LMA, these species have similar AN to plants from other biomes. Variations in other leaf anatomical traits, such as mesophyll and chloroplast surface area exposed to intercellular air space (Sm /S and Sc /S), may offset the restrictions imposed by high LMA in gm and AN in these species. Seven sclerophyllous Mediterranean oaks from Europe/North Africa and North America with contrasting LMA were compared in terms of morphological, anatomical and photosynthetic traits. Mediterranean oaks showed specific differences in AN that go beyond the common morphological leaf traits reported for these species (reduced leaf area and thick leaves). These variations resulted mainly from the differences in gm , the most limiting factor for carbon assimilation in these species. Species with higher AN showed increased Sc /S, which implies increased gm without changes in stomatal conductance. The occurrence of this anatomical adaptation at the cell level allowed evergreen oaks to reach AN values comparable to congeneric deciduous species despite their higher LMA.

[1]  J. Flexas,et al.  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. , 2016, Tree physiology.

[2]  A. Escudero,et al.  Costs of leaf reinforcement in response to winter cold in evergreen species. , 2016, Tree physiology.

[3]  J. Flexas,et al.  The photosynthetic capacity in 35 ferns and fern allies: mesophyll CO2 diffusion as a key trait. , 2016, The New phytologist.

[4]  J. Flexas,et al.  Leaf morphological and physiological adaptations of a deciduous oak (Quercus faginea Lam.) to the Mediterranean climate: a comparison with a closely related temperate species (Quercus robur L.). , 2016, Tree physiology.

[5]  J. Flexas,et al.  Leaf functional plasticity decreases the water consumption without further consequences for carbon uptake in Quercus coccifera L. under Mediterranean conditions. , 2016, Tree physiology.

[6]  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.

[7]  U. Niinemets Is there a species spectrum within the world-wide leaf economics spectrum? Major variations in leaf functional traits in the Mediterranean sclerophyll Quercus ilex. , 2015, The New phytologist.

[8]  P. J. Andralojc,et al.  Environmentally driven evolution of Rubisco and improved photosynthesis and growth within the C3 genus Limonium (Plumbaginaceae). , 2014, The New phytologist.

[9]  J. Flexas,et al.  Photosynthetic limitations in Mediterranean plants: A review , 2014 .

[10]  Ü. Niinemets,et al.  Photosynthetic responses to stress in Mediterranean evergreens: Mechanisms and models , 2014 .

[11]  J. Flexas,et al.  Variability of mesophyll conductance in grapevine cultivars under water stress conditions in relation to leaf anatomy and water use efficiency , 2014 .

[12]  D. Sánchez-Gómez,et al.  Effects of drought on mesophyll conductance and photosynthetic limitations at different tree canopy layers. , 2013, Plant, cell & environment.

[13]  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.

[14]  F. Gugerli,et al.  Inter- and intra-specific variability in isoprene production and photosynthesis of Central European oak species. , 2013, Plant biology.

[15]  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.

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

[17]  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.

[18]  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 .

[19]  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.

[20]  Margaret E. Staton,et al.  Genomics of Fagaceae , 2012, Tree Genetics & Genomes.

[21]  J. Flexas,et al.  Terrestrial Photosynthesis in a Changing Environment: Ecophysiology of photosynthesis in semi-arid environments , 2012 .

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

[23]  E. Veneklaas,et al.  Photosynthesis at an extreme end of the leaf trait spectrum: how does it relate to high leaf dry mass per area and associated structural parameters? , 2010, Journal of experimental botany.

[24]  Munir Ozturk,et al.  Ecophysiological responses of some maquis (Ceratonia siliqua L., Olea oleaster Hoffm. & Link, Pistacia lentiscus and Quercus coccifera L.) plant species to drought in the east Mediterranean ecosystem. , 2010, Journal of environmental biology.

[25]  G. Grimm,et al.  Significance of Pollen Characteristics for Infrageneric Classification and Phylogeny in Quercus (Fagaceae) , 2009, International Journal of Plant Sciences.

[26]  J. Flexas,et al.  Differential photosynthetic performance and photoprotection mechanisms of three Mediterranean evergreen oaks under severe drought stress. , 2009, Functional plant biology : FPB.

[27]  E. Veneklaas,et al.  Influence of leaf dry mass per area, CO2, and irradiance on mesophyll conductance in sclerophylls. , 2009, Journal of experimental botany.

[28]  I. Wright,et al.  Leaf mesophyll diffusion conductance in 35 Australian sclerophylls covering a broad range of foliage structural and physiological variation. , 2009, Journal of experimental botany.

[29]  J. Flexas,et al.  Variability in water use efficiency at the leaf level among Mediterranean plants with different growth forms , 2009, Plant and Soil.

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

[31]  D. Baldocchi,et al.  What limits evaporation from Mediterranean oak woodlands The supply of moisture in the soil, physiological control by plants or the demand by the atmosphere? , 2007 .

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

[33]  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.

[34]  J. Camarero,et al.  Crown architecture and leaf habit are associated with intrinsically different light-harvesting efficiencies in Quercus seedlings from contrasting environments , 2006 .

[35]  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.

[36]  William G. Lee,et al.  Modulation of leaf economic traits and trait relationships by climate , 2005 .

[37]  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 .

[38]  J. Flexas,et al.  Modulation of relative growth rate and its components by water stress in Mediterranean species with different growth forms , 2005, Oecologia.

[39]  V. Mosbrugger,et al.  Environmental signals from leaves--a physiognomic analysis of European vegetation. , 2005, The New phytologist.

[40]  A. Abadı́a,et al.  Seasonal changes in photosynthesis and photoprotection in a Quercus ilex subsp. ballota woodland located in its upper altitudinal extreme in the Iberian Peninsula. , 2005, Tree physiology.

[41]  Fernando Valladares,et al.  Photoinhibition and drought in Mediterranean woody saplings: scaling effects and interactions in sun and shade phenotypes. , 2004, Journal of experimental botany.

[42]  Sean C. Thomas,et al.  The worldwide leaf economics spectrum , 2004, Nature.

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

[44]  H. Mooney,et al.  Drought adaptations in two Californian evergreen sclerophylls , 1974, Oecologia.

[45]  A. Escudero,et al.  Stomatal responses to drought at a Mediterranean site: a comparative study of co-occurring woody species differing in leaf longevity. , 2003, Tree physiology.

[46]  A. Escudero,et al.  Stomatal responses to drought of mature trees and seedlings of two co-occurring Mediterranean oaks , 2003 .

[47]  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.

[48]  J. Flexas,et al.  Relationship between maximum leaf photosynthesis, nitrogen content and specific leaf area in balearic endemic and non-endemic mediterranean species. , 2003, Annals of botany.

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

[50]  Jesús Julio Camarero,et al.  Effects of a severe drought on Quercus ilex radial growth and xylem anatomy , 2003, Trees.

[51]  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.

[52]  C. Piel Diffusion du CO2 dans le mésophylle des plantes à métabolisme C3 , 2002 .

[53]  W. Smith,et al.  Mesophyll Architecture and Cell Exposure to Intercellular Air Space in Alpine, Desert, and Forest Species , 2002, International Journal of Plant Sciences.

[54]  J. Camarero,et al.  Functional groups in Quercus species derived from the analysis of pressure–volume curves , 2002, Trees.

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

[56]  D. Whitehead,et al.  Photosynthetic characteristics in canopies of Quercus rubra, Quercus prinus and Acer rubrum differ in response to soil water availability , 2002, Oecologia.

[57]  I. Terashima,et al.  The influence of leaf thickness on the CO2 transfer conductance and leaf stable carbon isotope ratio for some evergreen tree species in Japanese warm‐temperate forests , 1999 .

[58]  K. Nixon,et al.  Phylogeny, biogeography, and processes of molecular differentiation in Quercus subgenus Quercus (Fagaceae). , 1999, Molecular phylogenetics and evolution.

[59]  J. García-Plazaola,et al.  Diurnal changes in antioxidant and carotenoid composition in the Mediterranean schlerophyll tree Quercus ilex (L) during winter , 1999 .

[60]  O. Roupsard,et al.  Limitation of photosynthetic activity by CO2 availability in the chloroplasts of oak leaves from different species and during drought , 1996 .

[61]  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 .

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

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

[64]  D. Epron,et al.  A comparison of photosynthetic responses to water stress in seedlings from 3 oak species: Quercus petraea (Matt) Liebl, Q rubra L and Q cerris L , 1993 .

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

[66]  N. Breda,et al.  Photosynthesis of oak trees [Quercus petraea (Matt.) Liebl.] during drought under field conditions: diurnal course of net CO2 assimilation and photochemical efficiency of photosystem II , 1992 .

[67]  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.

[68]  S. Rhizopoulou,et al.  Water Relations of Evergreen Sclerophylls. I. Seasonal Changes in the Water Relations of Eleven Species from the Same Environment , 1990 .

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

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

[71]  P. Miller,et al.  WATER RELATIONS OF SELECTED SPECIES OF CHAPARRAL AND COASTAL SAGE COMMUNITIES , 1975 .