Ecological stress memory and cross stress tolerance in plants in the face of climate extremes

https://doi.org/10.1016/j.envexpbot.2012.02.009Get rights and content

Abstract

Under climate change, not only the magnitude, but also the frequency of extreme weather events is predicted to increase. Such repeated climate stress events may cause fundamental shifts in species compositions or ecosystem functioning. Yet, few studies document such shifts. One reason for higher stability of ecosystems than previously expected may be ecological stress memory at the single plant level. Ecological stress memory is defined here as any response of a single plant after a stress experience that modifies the response of the plant towards future stress events including the mode of interaction with other ecological units. Ecological stress memory is assessed on a whole plant level in ecological relevant parameters. It is therefore one important aspect of the broader concept of ecological memory that refers to whole communities and ecosystems. Here, we present studies which indicate the existence of ecological stress memory within single plants after drought, frost or heat stress. Possible mechanisms underlying an ecological stress memory are the accumulation of proteins, transcription factors or protective metabolites, as well as epigenetic modifications or morphological changes. In order to evaluate the importance of stress memory for stabilizing whole ecosystems and communities in times of climate change, cooperation between ecologists and molecular biologists is urgently needed, as well as more studies investigating stress memory on a single plant level. Only then the potential of plant stress memory for stabilizing ecosystems in times of intensifying climatic extremes can be evaluated and taken into account for measures of mitigation and adaptation to climate change.

Highlights

► We define the concept of an ecological stress memory. ► Some studies hint towards the existence of an ecological stress memory after climate extremes (drought, heat, frost). ► Possible mechanisms are e.g. epigenetic modifications. ► Further work and co-operations between ecologist and molecular biologist are urgently needed.

Introduction

The increase of climatic variability due to global climate change exerts climatic stress on plants that is novel in magnitude and frequency (IPCC, 2007, Hegerl et al., 2011, Min et al., 2011). Extreme weather events such as drought, heat waves, heavy rainfall, or frost spells differ from continuous climatic trends (e.g. warming or rising CO2-levels), as their ecological consequences are expected to be out of proportion to their relatively short duration (Easterling et al., 2000, Jentsch et al., 2007, Smith, 2011). Thus, extreme weather events may cause stronger effects on plants and plant communities than gradual shifts in means, as their abruptness gives little time for acclimation processes and as their magnitude may be impossible for single plants to cope with.

Collapsing populations of key species have been reported as direct responses to extreme climatic events (Allen and Breshears, 1998). However, there is also increasing incidence for stabilizing processes of climatic fluctuations for instance stimulated by reduced precipitation or recurrent drought events (Fay et al., 2000, Kahmen et al., 2005, Jentsch et al., 2011, Lloret et al., 2011). Such stabilizing mechanisms may occur already at the species and single plant level and are not yet fully appreciated. Ecological stress memory, dealt with in this article, might be one aspect leading to more stable community compositions in the face of an increasing frequency of extreme climatic events.

An ecological stress memory might emerge as plants reveal modifications, like acclimation, upon stress exposure that might persist after the stress stopped. Thus, when stress frequency increases, plants may not have returned to their previous reference state in the time lag between two stress events, thus affecting the stress response to repeated stress: Such a stress memory that the plant keeps after a stress event may lead to a faster stress response and increased stress tolerance upon a following stress event (Bruce et al., 2007, Walter et al., 2011).

Here, we (1) introduce the concept of an ecological stress memory and (2) present studies indicating the existence of an ecological stress memory after drought, frost or heat stress. We further (3) discuss possible mechanisms underlying an ecological stress memory and we (4) consider research challenges in the field of ecological stress memory research in times of rapid climate change.

Section snippets

Ecological stress memory vs. ecological memory vs. lagged stress effects

The term “memory” is used ambiguously in ecology (Rensing et al., 2009). Here, we focus on ecological stress memory, which we see as one important aspect of the broader concept of “ecological memory”. Ecological stress memory differs from lagged stress effects.

Ecological memory refers to whole communities or ecosystems and addresses the capacity of past states or experiences to influence present or future responses of ecosystems (Padisak, 1992). It is composed of species, their interactions,

Drought tolerance and drought memory

Plants are able to acclimate to drought stress, thereby increasing their drought tolerance. Mechanisms of acclimation include the accumulation of osmoprotective proteins, like dehydrins (Bohnert, 2000, Lambers et al., 2008), the accumulation of soluble sugars (Lambers et al., 2008, Walter et al., 2012), a reduction of the photosynthetic apparatus along with additional mechanisms to prevent damage by reactive oxygen species (Munne-Bosch and Alegre, 2000) and the accumulation of compatible

Frost tolerance and frost memory

In regions where subzero temperatures are reached, perennial plants show the potential to acclimate to frost to reduce frost damage, caused by intracellular ice crystals and dehydration. As apoplastic ice formation leads to cell dehydration, drought acclimation and frost acclimation often involve the same mechanisms, like accumulation of soluble sugars or transcription of dehydrins and LEA-genes (Lambers et al., 2008, Janska et al., 2010). Frost acclimation is triggered by low temperature and

Heat stress tolerance and heat stress memory

On a cell-level, heat stress acclimation is rather well understood: Upon exposure to extremely high temperatures, expression of normal housekeeping genes is stopped and heat shock proteins (HSP), which act to prevent protein damage or photo-oxidation and which repair already denaturated proteins (chaperones) are increasingly synthesized (Parcellier et al., 2003, Baniwal et al., 2004, Kotak et al., 2007). Furthermore, compatible solutes like prolin or betaine act to stabilize proteins (Schulze

Cross-stress memory

As frost, heat and drought stress all involve cell dehydration, acclimation mechanisms are partly the same (Beck et al., 2007). It is thus possible that acclimation and formation of a stress memory to one kind of stress also prevents damage by other stressors, providing cross-stress memory and tolerance. For instance, frost tolerance of local populations or ecotypes, respectively, is related to drought tolerance (Blodner et al., 2005).

More specifically, exposure to an extreme drought event in

Possible mechanisms behind an ecological stress memory

As possible mechanisms for an ecological stress memory, Bruce et al. (2007) suggest the accumulation of transcription factors or proteins to facilitate a fast response upon repeated stress exposure as well as epigenetic mechanisms, such as histone modifications or chemical changes at the DNA (methylation, acetylation) that are inherited through mitotic or even meiotic cell divisions (Bossdorf et al., 2008, Chinnusamy et al., 2008, Boyko and Kovalchuk, 2011). Another possibility is the

Research challenges

Studies investigating ecological stress memory are rare. Most studies on the duration and heritability of plant stress are conducted on a cellular level and focus on genetic or epigenetic aspects. In such studies, time spans between the initial and the repeated stress is usually restricted to only several hours to days (Bruce et al., 2007). More ecologically relevant research and assessments of stress tolerance and ecological stress memory are needed. Furthermore, multigenerational epigenetic

Acknowledgments

We thank two anonymous reviewers for valuable hints and comments to clarify our concepts and improve our manuscript.

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