The heterogeneity and spatial patterning of structure and physiology across the leaf surface in giant leaves of Alocasia macrorrhiza.

Tobias Isaac Baskin,Shuai Li,Lawren Sack,Christine Scoffoni,Ya-Jun Chen,Atsushi Ishida,Kun-Fang Cao,Yong-Jiang Zhang

doi:10.1371/journal.pone.0066016

Abstract

Leaf physiology determines the carbon acquisition of the whole plant, but there can be considerable variation in physiology and carbon acquisition within individual leaves. Alocasia macrorrhiza (L.) Schott is an herbaceous species that can develop very large leaves of up to 1 m in length. However, little is known about the hydraulic and photosynthetic design of such giant leaves. Based on previous studies of smaller leaves, and on the greater surface area for trait variation in large leaves, we hypothesized that A. macrorrhiza leaves would exhibit significant heterogeneity in structure and function. We found evidence of reduced hydraulic supply and demand in the outer leaf regions; leaf mass per area, chlorophyll concentration, and guard cell length decreased, as did stomatal conductance, net photosynthetic rate and quantum efficiency of photosystem II. This heterogeneity in physiology was opposite to that expected from a thinner boundary layer at the leaf edge, which would have led to greater rates of gas exchange. Leaf temperature was 8.8°C higher in the outer than in the central region in the afternoon, consistent with reduced stomatal conductance and transpiration caused by a hydraulic limitation to the outer lamina. The reduced stomatal conductance in the outer regions would explain the observed homogeneous distribution of leaf water potential across the leaf surface. These findings indicate substantial heterogeneity in gas exchange across the leaf surface in large leaves, greater than that reported for smaller-leafed species, though the observed structural differences across the lamina were within the range reported for smaller-leafed species. Future work will determine whether the challenge of transporting water to the outer regions can limit leaf size for plants experiencing drought, and whether the heterogeneity of function across the leaf surface represents a particular disadvantage for large simple leaves that might explain their global rarity, even in resource-rich environments.

Highlights

Leaves first appeared in terrestrial plants about 400 million years ago and arose independently multiple times in a number of plant lineages, eventually evolving an enormous diversity in shape, size, internal structure and longevity across environments [1,2,3,4,5]
Leaf dry mass per area, chlorophyll concentration per leaf area, minor vein length per area and the ratio of palisade- to spongy- tissue thickness remained stable from the leaf base to leaf tip
From the midrib to the margin, chlorophyll concentration per leaf area decreased by 24%, leaf dry mass per area decreased by 12%, and stomatal density by 7%, and guard cell length 3% (Fig. 3)

Summary

Introduction

Leaves first appeared in terrestrial plants about 400 million years ago and arose independently multiple times in a number of plant lineages, eventually evolving an enormous diversity in shape, size, internal structure and longevity across environments [1,2,3,4,5]. Previous studies have shown variable patterns, e.g., that abaxial stomatal density increases continuously from the leaf base to tip in wheat [14], and that stomatal density decreases from the leaf center to edges in some eudicotyledons, including other monocots [16,17]. These results suggest nonuniform water loss rates over a leaf surface [18]. There is a marked heterogeneity of stomatal conductance and gas exchange rate across the leaf surface in tobacco leaves [16], corresponding with a greater vein density (i.e., vein length per leaf area) near the leaf tip than at the leaf base [16]

Methods

Results

Conclusion