Effects of Foliar Redox Status on Leaf Vascular Organization Suggest Avenues for Cooptimization of Photosynthesis and Heat Tolerance

Jared Stewart,William Adams,Stephanie Polutchko,Christopher Baker,Barbara Demmig-Adams,Shannon Wong-Michalak,Carlie Sharpes

doi:10.3390/ijms19092507

Abstract

The interaction of heat stress with internal signaling networks was investigated through Arabidopsis thaliana mutants that were deficient in either tocopherols (vte1 mutant) or non-photochemical fluorescence quenching (NPQ; npq1, npq4, and npq1 npq4 mutants). Leaves of both vte1 and npq1 npq4 mutants that developed at a high temperature exhibited a significantly different leaf vascular organization compared to wild-type Col-0. Both mutants had significantly smaller water conduits (tracheary elements) of the xylem, but the total apparent foliar water-transport capacity and intrinsic photosynthetic capacity were similarly high in mutants and wild-type Col-0. This was accomplished through a combination of more numerous (albeit narrower) water conduits per vein, and a significantly greater vein density in both mutants relative to wild-type Col-0. The similarity of the phenotypes of tocopherol-deficient and NPQ-deficient mutants suggests that leaf vasculature organization is modulated by the foliar redox state. These results are evaluated in the context of interactions between redox-signaling pathways and other key regulators of plant acclimation to growth temperature, such as the C-repeat binding factor (CBF) transcription factors, several of which were upregulated in the antioxidant-deficient mutants. Possibilities for the future manipulation of the interaction between CBF and redox-signaling networks for the purpose of cooptimizing plant productivity and plant tolerance to extreme temperatures are discussed.

Highlights

Today’s changing climate threatens crop productivity through unpredictable weather events and warmer, drier summers in many regions [1]
The maintenance of photosynthetic productivity requires a vascular system with a sufficient capacity for water transport and resistance to the introduction of air bubbles when evaporative demand exceeds water supply [4] or during freeze–thaw cycles [5]
We have recently focused on leaves of herbaceous species, for which we reported concomitant adjustments in leaf vascular anatomy and photosynthetic capacity in response to growth temperature

Summary

Introduction

Today’s changing climate threatens crop productivity through unpredictable weather events and warmer, drier summers in many regions [1]. The maintenance of photosynthetic productivity requires a vascular system with a sufficient capacity for water transport and resistance to the introduction of air bubbles (embolisms) when evaporative demand exceeds water supply [4] or during freeze–thaw cycles [5]. We have recently focused on leaves of herbaceous species, for which we reported concomitant adjustments in leaf vascular anatomy and photosynthetic capacity in response to growth temperature (see, e.g., [6]). Leaves of Arabidopsis thaliana that were grown under hot versus cool temperature exhibited a foliar vascular network with more numerous veins and an increased proportion of water conduits relative to sugar conduits [7,8]. Summer annuals that germinate in the spring and grow over the summer exhibited a foliar vasculature with constitutively more numerous veins and a greater ratio of water-to-sugar conduits compared to winter annuals that germinate in the fall, overwinter, and set seed in the spring before being subjected to the heat of summer [8,9]

Methods

Results

Conclusion