Leaf shrinkage with dehydration has attracted attention for over 100 years, especially as it becomes visibly extreme during drought. However, little has been known of its correlation with physiology. Computer simulations of the leaf hydraulic system showed that a reduction of hydraulic conductance of the mesophyll pathways outside the xylem would cause a strong decline of leaf hydraulic conductance (K leaf ). For 14 diverse species, we tested the hypothesis that shrinkage during dehydration (i.e. in whole leaf, cell and airspace thickness, and leaf area) is associated with reduction in K leaf at declining leaf water potential (C leaf ). We tested hypotheses for the linkage of leaf shrinkage with structural and physiological water relations parameters, including modulus of elasticity, osmotic pressure at full turgor, turgor loss point (TLP), and cuticular conductance. Species originating from moist habitats showed substantial shrinkage during dehydration before reaching TLP, in contrast with species originating from dry habitats. Across species, the decline of K leaf with mild dehydration (i.e. the initial slope of the K leaf versus C leaf curve) correlated with the decline of leaf thickness (the slope of the leaf thickness versus C leaf curve), as expected based on predictions from computer simulations. Leaf thickness shrinkage before TLP correlated across species with lower modulus of elasticity and with less negative osmotic pressure at full turgor, as did leaf area shrinkage between full turgor and oven desiccation. These findings point to a role for leaf shrinkage in hydraulic decline during mild dehydration, with potential impacts on drought adaptation for cells and leaves, influencing plant ecological distributions.
One of the most striking ecological trends is the association of small leaves with dry and cold climates, described 2400 years ago by Theophrastus, and recently recognized for eudicotyledonous plants at the global scale 1-3 . For eudicotyledons, this pattern is attributed 24 to small leaves having a thinner boundary layer to avoid extreme leaf temperatures 4 , and 25 their developing vein traits that improve water transport under cold or dry climates 5,6 . Yet, 26 the global distribution of leaf size and its mechanisms have not been tested in grasses, an 27 extraordinarily diverse lineage, distinct in leaf morphology, which contributes 33% of 28 terrestrial primary productivity, including the bulk of crop production 7 . Here we demonstrate that grasses have shorter and narrower leaves under colder and drier climates worldwide. We show that small grass leaves have thermal advantages and vein development that contrast with those of eudicotyledons, but that also explain the abundance of small leaves in cold and dry climates. The worldwide distribution of grass leaf size exemplifies how biophysical and developmental processes result in convergence across major lineages in adaptation to climate globally, and highlights the importance of leaf size and venation architecture for grass performance in past, present and future ecosystems. Data Fig. 1, SupplementaryTable 3). We tested whether developmental scaling would confer 64 small leaves with potential climatic advantages. 65 4 66 Box 1. Synthetic model of grass leaf vein development based on published data for 20 species (Supplementary Tables 5-6), conferring small leaves with traits advantageous under cold and dry climates Grass leaf development includes five phases based on developmental zones: Phase P (formation and expansion of the primordium, P): "Founder cells" in the periphery of the shoot apical meristem generate the leaf primordium. Cell divisions drive growth of a hood-like structure, in which the central 1° vein (midvein) and the large 2° veins are initiated early and extend acropetally, enabling their prolonged diameter growth (Box 1 Fig. 1a, c, e). Henceforth, discrete spatial growth zones develop at the leaf base and drive leaf expansion laterally and longitudinally. Phase D (formation of the cell division zone, DZ):The basal cell division zone (DZ) expands slightly, driving minimal growth (Box 1 Fig. 1a, b). The 1° and 2° vein orders (major veins) complete their patterning basipetally along the leaf blade and increase in diameter (Box 1 Fig. 1c, e). Meanwhile, beginning at the lamina tip, C 3 species form a single order of small longitudinal minor veins, i.e., 3° veins, as do most C 4 species, i.e., C 4-3L species. Some C 4 species of the subfamily Panicoideae additionally form smaller 4° veins, i.e., C 4-4L species 15 (Box 1 Fig. 1c). Phase D-E (DZ, and formation of the expansion zone, EZ):Cells from the DZ transition to a distinct, distal expansion zone (EZ).In the EZ, cell expansion in width and length spaces apart the 1° and 2° veins, resulting in th...
SummaryLeaf hydraulic conductance (K leaf ) quantifies the capacity of a leaf to transport liquid water and is a major constraint on light-saturated stomatal conductance (g s ) and photosynthetic rate (A max ). Few studies have tested the plasticity of K leaf and anatomy across growth light environments. These provided conflicting results.The Hawaiian lobeliads are an excellent system to examine plasticity, given the striking diversity in the light regimes they occupy, and their correspondingly wide range of A max , allowing maximal carbon gain for success in given environments. We measured K leaf , A max , g s and leaf anatomical and structural traits, focusing on six species of lobeliads grown in a common garden under two irradiances (300/800 lmol photons m À2 s À1). We tested hypotheses for light-induced plasticity in each trait based on expectations from optimality.K leaf , A max , and g s differed strongly among species. Sun/shade plasticity was observed in K leaf , A max, and numerous traits relating to lamina and xylem anatomy, venation, and composition, but g s was not plastic with growth irradiance. Species native to higher irradiance showed greater hydraulic plasticity.Our results demonstrate that a wide set of leaf hydraulic, stomatal, photosynthetic, anatomical, and structural traits tend to shift together during plasticity and adaptation to diverse light regimes, optimizing performance from low to high irradiance.
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