Plasticity in bundle sheath extensions of heterobaric leaves

Douglas J Lynch,Francesca A Mcinerney,Lenny L.R Kouwenberg,Miquel A Gonzalez‐Meler

doi:10.3732/ajb.1100525

Abstract

Leaf venation is linked to physiological performance, playing a critical role in ecosystem function. Despite the importance of leaf venation, associated bundle sheath extensions (BSEs) remain largely unstudied. Here, we quantify plasticity in the spacing of BSEs over irradiance and precipitation gradients. Because physiological function(s) of BSEs remain uncertain, we additionally explored a link between BSEs and water use efficiency (WUE). We sampled leaves of heterobaric trees along intracrown irradiance gradients in natural environments and growth chambers and correlated BSE spacing to incident irradiance. Additionally, we sampled leaves along a precipitation gradient and correlated BSE spacing to precipitation and bulk δ(13)C, a proxy for intrinsic WUE. BSE spacing was quantified using a novel semiautomatic method on fresh leaf tissue. With increased irradiance or decreased precipitation, Liquidambar styraciflua decreased BSE spacing, while Acer saccharum showed little variation in BSE spacing. Two additional species, Quercus robur and Platanus occidentalis, decreased BSE spacing with increased irradiance in growth chambers. BSE spacing correlated with bulk δ(13)C, a proxy for WUE in L. styraciflua, Q. robur, and P. occidentalis leaves but not in leaves of A. saccharum. We demonstrated that BSE spacing is plastic with respect to irradiance or precipitation and independent from veins, indicating BSE involvement in leaf adaptation to a microenvironment. Plasticity in BSE spacing was correlated with WUE only in some species, not supporting a function in water relations. We discuss a possible link between BSE plasticity and life history, particularly canopy position.

Highlights

Premise of the study: Leaf venation is linked to physiological performance, playing a critical role in ecosystem function
Plasticity in bundle sheath extensions (BSEs) spacing within tree crown—Irradiance received by leaves varied based on cardinal orientation and peripheral, intermediate or interior canopy position due to self-shading
Increased intracrown irradiance resulted in decreases in BSE spacing of ca. 200% in L. styraciflua and ca. 50% in the growth chambergrown Q. robur and P. occidentalis (Fig. 2, Table 3)

Summary

Introduction

Premise of the study: Leaf venation is linked to physiological performance, playing a critical role in ecosystem function. We quantify plasticity in the spacing of BSEs over irradiance and precipitation gradients. Because physiological function(s) of BSEs remain uncertain, we explored a link between BSEs and water use efficiency (WUE). We sampled leaves along a precipitation gradient and correlated BSE spacing to precipitation and bulk δ13C, a proxy for intrinsic WUE. Quercus robur and Platanus occidentalis, decreased BSE spacing with increased irradiance in growth chambers. BSE spacing correlated with bulk δ13C, a proxy for WUE in L. styraciflua, Q. robur, and P. occidentalis leaves but not in leaves of A. saccharum. Conclusions: We demonstrated that BSE spacing is plastic with respect to irradiance or precipitation and independent from veins, indicating BSE involvement in leaf adaptation to a microenvironment. Plasticity in BSE spacing was correlated with WUE only in some species, not supporting a function in water relations. The evolution of vascular tissue networks was a critical trait for early plant evolution (Niklas, 1997), and dramatic increases in vein density greatly improved photosynthetic capacity during angiosperm evolution (Brodribb and Feild, 2010) Because plant branching in general

Methods

Results

Conclusion