Priming and memory of stress responses in organisms lacking a nervous system

Abstract

Experience and memory of environmental stimuli that indicate future stress can prepare (prime) organismic stress responses even in species lacking a nervous system. The process through which such organisms prepare their phenotype for an improved response to future stress has been termed 'priming'. However, other terms are also used for this phenomenon, especially when considering priming in different types of organisms and when referring to different stressors. Here we propose a conceptual framework for priming of stress responses in bacteria, fungi and plants which allows comparison of priming with other terms, e.g. adaptation, acclimation, induction, acquired resistance and cross protection. We address spatial and temporal aspects of priming and highlight current knowledge about the mechanisms necessary for information storage which range from epigenetic marks to the accumulation of (dormant) signalling molecules. Furthermore, we outline possible patterns of primed stress responses. Finally, we link the ability of organisms to become primed for stress responses (their 'primability') with evolutionary ecology aspects and discuss which properties of an organism and its environment may favour the evolution of priming of stress responses.

The effect of cold priming on the fitness of Arabidopsis thaliana accessions under natural and controlled conditions

“…1). Consistent with the definition of priming74 and with the previous hypothesis that priming acts independently from cold acclimation and is of importance in nature in spring10, the cold pretreatment resulted in higher Φ PS-II in the intermediate cold-adapted accessions WS, Col-0 and Van-0 than in the most cold-adapted accessions N13, Ms-0 and Kas-1 (Fig. 4).…”

Epigenetic and chromatin-based mechanisms in environmental stress adaptation and stress memory in plants

“…Such conditions may be caused, for example, by extreme temperatures, too little or too much water (drought or flooding, respectively), or pathogen and herbivore attack. Priming of organismal responses to stress describes the phenomenon by which a temporally limited environmental stimulus (a ‘priming stress cue’) modifies a plant for future stress exposure (a ‘triggering stress cue’) [5, 6]. The term priming was originally coined in the context of immunity against pathogens (biotic stress), but was later also applied to responses to abiotic environmental conditions.…”

“…1). Priming acts at the phenotypic level and does not introduce changes in DNA sequence and is thus reversible eventually [5, 6]. Generally, such priming is evidenced by a stronger or faster response pattern, as can be exemplified by the modified activation kinetics of defense gene expression.

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The Arabidopsis DNA Methylome Is Stable under Transgenerational Drought Stress

“…This ability is relayed by various intricate intercellular and intracellular mechanisms, including hormone signaling and organelle-nuclear retrograde pathways that allow plants to perceive and respond to biotic and abiotic stresses (Karpinski et al, 1999;Fernández and Strand, 2008;Cutler et al, 2010;Goodger and Schachtman, 2010;Chan et al, 2016;Martín et al, 2016). Additionally, repeated exposure to stress can lead to plant stress priming, whereby prior stress exposure conveys an enhanced ability to respond to future events (Conrath et al, 2006;Ding et al, 2012;Gordon et al, 2013;Sani et al, 2013;Wang et al, 2014;Virlouvet and Fromm, 2015;Hilker et al, 2016;Wibowo et al, 2016). This notion has been extended to numerous considerations of the formation of plant stress memory, in which a state of altered stress responsivity is mitotically or meiotically transmissible (Bruce et al, 2007;Hauser et al, 2011b;Probst and Mittelsten Scheid, 2015;Crisp et al, 2016;van Loon, 2016).…”