Deacclimation and reacclimation of cold-hardy plants: Current understanding and emerging concepts

Abstract

The abilities of cold-hardy plants to resist deacclimation during transient warm spells and to reacclimate when cold temperatures return are significant for winter survival. Yet compared to the volume of research on the biology of cold acclimation, relatively little is known about how plants maintain and/or reacquire cold hardiness in late winter and spring. This review summarizes the past 40 years of research into deacclimation and reacclimation in herbaceous and woody plants and suggests questions that should be addressed with multi-disciplinary approaches to more comprehensively understand the biology of winter-survival in plants. Deacclimation and reacclimation are highly dependent on exogenous and endogenous factors such as the ambient temperatures, water availability, photoperiod, energy budget and metabolism, growth and development, and the dormancy status of plants. Putative mechanisms of these hardiness transitions are discussed based on the published accounts of changes in carbohydrates (e.g., compatible solutes), membrane lipids, proteins (e.g., dehydrins), antioxidants, photosynthesis, and gene expression. In conclusion, the relationships between environmental determinants, gene expression and regulation, cellular and organismal structure and function, and the consequent cold hardiness transitions in plants are discussed and debated.

Introduction

Survival of plants at freezing temperatures is dependent on their ability to cold acclimate in response to environmental stimuli such as short-days and low temperatures [1], [2]. Plant species in cold climates have evolved adaptations such as dormancy, rapid acclimation, and maintainence of high cold hardiness throughout winter singly or in combination [3], [4], [5]. Although researchers have intensively studied various aspects of acclimation, the processes of cold deacclimation and reacclimation remain less understood. As will be described in this review, deacclimation resistance and reacclimation capacity play a significant role in determining plant hardiness during late winter and early spring when plants are particularly vulnerable to cold-injury due to emergence from dormancy.

Some terms should be defined at the outset. Cold acclimation, also known as cold hardening, is an increase in tolerance over time to cold temperatures and cellular desiccation in response to inductive conditions such as cold temeperature, short photoperiods, mild drought, etc., and that results from changes in gene expression and physiology [1], [2], [5]. Dormancy was defined by Lang et al. as a “temporary suspension of visible growth of any plant structure containing a meristem” [6]. When the dormancy-inducing, environmental or endogenous signals (e.g., low temperature, short photoperiod, hormones, etc.) are specifically perceived within (i.e., “endo”) the affected meristem, it is called endodormancy which is regulated by physiological factors originating inside the affected structure. This is different from paradormancy that involves a dormancy-inducing signal originating in a structure other than (i.e., “para”) the affected structure. Ecodormancy includes all those cases of growth suspension that result from unsuitable environmental (i.e., “eco”) factors (e.g., hot or cold temperatures, dehydration, nutrient deficiencies, etc.) which have a non-targeted effect on all aspects of development and physiology including those of the dormant organ [6].

The term deacclimation has often been defined as a reduction in those levels of hardiness that were originally attained through an earlier acclimation process. However, deacclimation may also refer to mechanisms that mediate reduced hardiness rather than simply the loss of hardiness per se. Additionally, the term deacclimation can be used to describe losses in hardiness due to such diverse factors as environmental stimuli (i.e., warm temperatures), phenological changes, and reactivation of growth. Furthermore, deacclimation may be either reversible by subsequent re-exposure to low temperatures or result in a largely irreversible loss of hardiness.

In this paper, the term deacclimation will refer to a loss of acclimated cold hardiness measured at the cellular, tissue, or whole-plant level, irrespective of the stimulus that initiated deacclimation or the mechanism by which it occurred. Changes in structure, physiology, or gene expression associated with the loss of hardiness represent putative mechanisms that could account for deacclimation. If a deacclimated plant is subsequently exposed to cold temperatures, it may regain some or most of the lost hardiness in a process called reacclimation. Similar considerations apply to the definition of reacclimation as have been stated for deacclimation. The terms deacclimation and reacclimation are used in this paper in preference to the synonymous terms dehardening and rehardening often found in the agronomic, horticultural, and forestry literature.

This review is divided into three subject areas. In Section 2, the general characteristics of deacclimation and reacclimation are introduced with an emphasis on the role of temperature. Section 3 illustrates how growth and development affect deacclimation and reacclimation and how the influence of growth is modulated by photoperiod and dormancy. Section 4 summarizes information on biochemistry, molecular genetics, and physiology associated with deacclimation. Emphasis is placed throughout this review, but particularly in the conclusion, on identifying gaps in our current understanding and suggesting possibilities for future research.