Quantitative Leaf Anatomy of C3 and C4 Grasses (Poaceae): Bundle Sheath and Mesophyll Surface Area Relationships

Abstract

Quantitative anatomical characteristics, including cross-sectional areas (volumes) of all tissues and perimeters (surface areas) of chlorenchymatous tissues, were measured in transverse sections of leaf blades of 125 species of grasses (Poaceae). The species sample represents the major taxonomic groups and the range of photosynthetic pathway variation, including the 'classical' anatomical-biochemical types (the NADP-malic enzymic type, NADP-ME; the NAD-malic enzyme type, NAD-ME; and the PEP carboxykinase type, PCK) and species of Eragrostis, Panicum and Enneapogon that are PCK-like structurally, but NAD-ME biochemically. We found new evidence that both mesophyll and bundle sheath tissues of C4 species have less surface area exposed to intercellular space and lower surface: volume ratios than in C3 species and, in C4 species, the ratio of PCR (bundle sheath) tissue surface adjacent to intercellular space:tissue volume ratio is strikingly lower than the comparable value for PCA tissue. Additionally, the 'classical' NAD-ME type differs from the structurally similar PCK type in reduced exposure of bundle sheath tissue surface to intercellular space and in lower surface: volume ratios of both mesophyll and bundle sheath tissues. Multivariate analysis reinforces this discrimination of the 'classical' NAD-ME type from the PCK type, lending support to the hypothesis that certain anatomical features reduce apoplastic leakage of CO2 from bundle sheath to intercellular space. Overall, the pattern of variation in quantitative leaf blade anatomy is complex, reflecting correlations with both taxonomic group and photosynthetic type, and no new diagnostic characters emerge that can be used to distinguish one biochemical type from another a priori.