Developmental control of hypoxia during bud burst in grapevine.

Karlia Meitha,Daniel J Gibbs,Christine H Foyer,Patricia Agudelo‐Romero,Santiago Signorelli,Michael J Considine,John A Considine

doi:10.1111/pce.13141

Abstract

Dormant or quiescent buds of woody perennials are often dense and in the case of grapevine (Vitis vinifera L.) have a low tissue oxygen status. The precise timing of the decision to resume growth is difficult to predict, but once committed, the increase in tissue oxygen status is rapid and developmentally regulated. Here, we show that more than a third of the grapevine homologues of widely conserved hypoxia-responsive genes and nearly a fifth of all grapevine genes possessing a plant hypoxia-responsive promoter element were differentially regulated during bud burst, in apparent harmony with resumption of meristem identity and cell-cycle gene regulation. We then investigated the molecular and biochemical properties of the grapevine ERF-VII homologues, which in other species are oxygen labile and function in transcriptional regulation of hypoxia-responsive genes. Each of the 3 VvERF-VIIs were substrates for oxygen-dependent proteolysis in vitro, as a function of the N-terminal cysteine. Collectively, these data support an important developmental function of oxygen-dependent signalling in determining the timing and effective coordination bud burst in grapevine. In addition, novel regulators, including GASA-, TCP-, MYB3R-, PLT-, and WUS-like transcription factors, were identified as hallmarks of the orderly and functional resumption of growth following quiescence in buds.

Highlights

The transition from heterotrophic to autotrophic metabolism is a defining feature of vegetative organogenesis in higher plants
PHYSIOLOGY AND METABOLITE ANALYSIS Resumption of primary metabolism and tissue oxygenation is largely independent of light Temperate woody perennials such as grapevine are commercially propagated from cuttings of bud-wood bearing dormant proleptic buds, which comprise an embryonic shoot enclosed in layers of bracts and scales
The incidence of light has a strong influence on primary metabolism and tissue oxygen tension in photosynthetic seeds (Borisjuk and Rolletschek, 2009), and as hypoxia was a key focus of this study, we hypothesised that the degree of hypoxia would be directly influenced by light

Summary

Introduction

The transition from heterotrophic to autotrophic metabolism is a defining feature of vegetative organogenesis in higher plants. The initial events during this transition are rapid and accompanied by considerable changes in the cellular and extracellular environment, notably light and oxygen-dependent cues, which function as powerful signals influencing cell function and fate. Bud burst in woody perennial species is an important ecological and agricultural context of this transition. Few studies have investigated the physiology in relation to transcriptional change during the course of bud burst. Few studies have investigated the physiology of tissue oxygen status, and accompanying oxygen-dependent metabolism and signalling. Tissue oxygen status has emerged as an important context for the regulation of developmental transitions (Considine et al, 2017) and acclimation to stress (Voesenek and Bailey-Serres, 2015), as both an essential substrate for aerobic metabolism as well as important medium of post-translational modification and signal transduction

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