Developmental and biophysical determinants of grass leaf size worldwide

Abstract

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...

A clear trade‐off between leaf hydraulic efficiency and safety in an aridland shrub during regrowth

“…Plants have acquired a suite of traits that allow them to adapt to the environmental conditions of their habitats (Baird et al, 2021; Brodribb, Powers, Cochard, & Choat, 2020; Choat et al, 2012; Fu & Meinzer, 2018; Meinzer et al, 2016, 2017; Yao, Nie, et al, 2021). Among them, hydraulic traits related to efficient water transport and resistance to hydraulic dysfunction are of particular importance (Brodribb, Powers, Cochard, & Choat, 2020; Li et al, 2020; Liu et al, 2018; Scoffoni, Sack, & Ort, 2017), and efficient water transport could trade‐off against protecting hydraulic systems from loss of function (Nardini, Pedà, & Rocca, 2012; Scoffoni, Sack, & Ort, 2017) to allow species to adapt to habitats with different precipitation levels (Choat et al, 2012; Ocheltree, Nippert, & Prasad, 2016; Scoffoni, Sack, & Ort, 2017).…”

High Leaf Vein Density Promotes Leaf Gas Exchange by Enhancing Leaf Hydraulic Conductance in Oryza sativa L. Plants

“…VLA and VLA minor showed no varietal differences in the present study, which was perhaps due to the few genotypes used, and their vein traits ranged very narrowly. Rice leaf veins are distributed in parallel, and the leaf vein density is strongly affected by the leaf width (Baird et al, 2021 ). For example, Tabassum et al ( 2016 ) reported that polyethylene glycol–induced water deficit caused rice leaf narrowing and led to an increase in leaf density.…”

“…Simonin et al ( 2012 ) demonstrated that K leaf increased with leaf area. However, a recent study exploring the development and biophysical determinations of grass leaf size worldwide revealed that small leaves have hydraulic benefits due to their higher VLA major (Baird et al, 2021 ). Optimal leaf morphological and anatomical traits for improving K leaf and P N should be defined to provide theories for high photosynthetic capacity rice breeding.…”

Correlational selection and genetic architecture promote the leaf economics spectrum in a perennial grass

“…Short growing seasons may promote a quick return-on-investment strategy of low tissue construction costs and high photosynthetic capacity (Baird et al 2021). In the southern habitat typical of the lowland ecotype, the long growing season may select for longer-lived leaves with higher LMA.…”