Priming and Memory of Stress Responses in Organisms Lacking a Nervous System

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Priming and Memory of Stress Responses in Organisms Lacking a Nervous System See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/281171559 Priming and memory of stress responses in organisms lacking a nervous system Article in Biological Reviews · August 2015 DOI: 10.1111/brv.12215 · Source: PubMed CITATIONS READS 13 614 19 authors, including: Jens Rolff Anke Steppuhn Freie Universität Berlin Freie Universität Berlin 84 PUBLICATIONS 2,635 CITATIONS 42 PUBLICATIONS 1,004 CITATIONS SEE PROFILE SEE PROFILE Joost T van Dongen Sarah J Whitcomb RWTH Aachen University Max Planck Institute of Molecular Plant Physi… 86 PUBLICATIONS 3,782 CITATIONS 3 PUBLICATIONS 118 CITATIONS SEE PROFILE SEE PROFILE Some of the authors of this publication are also working on these related projects: NUMEX - the Ecuadorian NUtrient Manipulation EXperiment View project Micro- and nanoplastics, glyphosate and impacts on soil biodiversity: Identifying effects from enzymes to microbiomes in multi-stressed systems View project All content following this page was uploaded by Jens Rolff on 26 August 2015. The user has requested enhancement of the downloaded file. All in-text references underlined in blue are added to the original document and are linked to publications on ResearchGate, letting you access and read them immediately. Biol. Rev. (2015), pp. 000–000. 1 doi: 10.1111/brv.12215 Priming and memory of stress responses in organisms lacking a nervous system Monika Hilker1,2∗, Jens Schwachtje3, Margarete Baier4, Salma Balazadeh5, Isabel Baurle¨ 5, Sven Geiselhardt1,DirkK.Hincha6, Reinhard Kunze7, Bernd Mueller-Roeber5, Matthias C. Rillig2,8, Jens Rolff9, Tina Romeis10, Thomas Schm¨ulling11, Anke Steppuhn12, Joost van Dongen13, Sarah J. Whitcomb3, Susanne Wurst14, Ellen Zuther6 and Joachim Kopka3 1Applied Zoology/Animal Ecology, Dahlem Centre of Plant Sciences (DCPS), Institute of Biology, Freie Universit¨at (FU) Berlin, Haderslebener Straße 9, 12163 Berlin, Germany 2Berlin-Brandenburg Institute of Advanced Biodiversity Research (BBIB), Altensteinstr. 6, 14195 Berlin, Germany 3Applied Metabolome Analysis, Department of Molecular Physiology, Max-Planck-Institute of Molecular Plant Physiology, Am M¨uhlenberg 1, 14476 Potsdam-Golm, Germany 4Plant Physiology, DCPS, Institute of Biology, FU Berlin, K¨onigin-Luise-Straße 12-16, 14195 Berlin, Germany 5Institute for Biochemistry and Biology, Universit¨at Potsdam, Karl-Liebknecht-Straße 24-25, Haus 20, 14476 Potsdam-Golm, Germany 6Central Infrastructure Group Transcript Profiling, Max-Planck-Institute of Molecular Plant Physiology, Am M¨uhlenberg 1, 14476 Potsdam-Golm, Germany 7Applied Genetics/Molecular Plant Genetics, DCPS, Institute of Biology, FU Berlin, Albrecht-Thaer-Weg 6, 14195 Berlin, Germany 8Plant Ecology, DCPS, Institute of Biology, FU Berlin, Altensteinstraße 6, 14195 Berlin, Germany 9Evolutionary Biology, Institute of Biology, FU Berlin, K¨onigin-Luise-Straße 1-3, 14195 Berlin, Germany 10Plant Biochemistry, DCPS, Institute of Biology, FU Berlin, K¨onigin-Luise-Straße 12-16, 14195 Berlin, Germany 11Applied Genetics, DCPS, Institute of Biology, FU Berlin, Albrecht-Thaer-Weg 6, 14195 Berlin, Germany 12Molecular Ecology, DCPS, Institute of Biology, FU Berlin, Haderslebener Straße 9, 12163 Berlin, Germany 13Rhizosphere Molecular Ecology, Institute of Biology, RWTH Aachen, Worringerweg 1, 52074 Aachen, Germany 14Functional Ecology, DCPS, Institute of Biology, FU Berlin, K¨onigin-Luise-Straße 1-3, 14195 Berlin, Germany 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. Key words: priming, stress signalling, epigenetics, memory, fitness, stress tolerance, defence, bet hedging. CONTENTS I. Introduction ................................................................................................ 2 II. A general concept of priming of stress responses in organisms without a nervous system ................... 3 * Address for correspondence (Tel: +49 (0)30 838 55913; E-mail: [email protected]). Biological Reviews (2015) 000–000 © 2015 Cambridge Philosophical Society 2 Monika Hilker and others III. Spatial aspects of priming: spreading the information ...................................................... 4 IV. Temporal aspects of priming: memory of the primed state ................................................. 4 V. Molecular mechanisms of priming and memory ........................................................... 6 VI. Patterns of primed stress responses ......................................................................... 8 VII. Priming and other terms: adaptation, acclimation, induction, acquired resistance and cross protection .... 9 (1) Priming and adaptation ................................................................................ 9 (2) Priming and acclimation ............................................................................... 9 (3) Priming and induction ................................................................................. 9 (4) Priming and acquired resistance ....................................................................... 10 (5) Trans-priming and cross protection, cross talk of plant defence signalling and cross stress memory .... 10 VIII. Evolutionary ecology aspects of priming and memory of stress responses .................................. 10 (1) Age of the organism .................................................................................... 11 (2) Nutritional state of the organism and resource availability ............................................. 11 (3) Life strategy of the organism ........................................................................... 11 (4) Reliability and specificity of the priming stimulus and predictability of stress .......................... 12 (5) Community ecology and priming ...................................................................... 12 IX. Conclusions ................................................................................................ 12 X. Acknowledgements ......................................................................................... 12 XI. References .................................................................................................. 12 I. INTRODUCTION hardening or cold acclimation are used when referring to improved cold or frost tolerance of plants after pre-exposure Successful and efficient processing of information is essential to cold (e.g. Thomashow, 1999; Guy, 2003; Hannah, Heyer for the survival of organisms. Memory of environmental & Hincha, 2005; Stavang, Hansen & Olsen, 2008; Hincha stimuli may affect the response of an individual to future & Zuther, 2014). However, it is not only the experience environmental conditions. Memory of an event experienced of a mild stress that ‘warns’ a plant of future stress that is in a certain life stage, i.e. the capacity to retain information considered as a priming stimulus which improves a plant’s on this event, is not necessarily permanent, but may be response to impending threats. Colonization of plant roots short-lived or long-lasting. Evidence is growing that not only by beneficial rhizobacteria is also studied in the context of animals, but also organisms lacking a dedicated nervous priming since it may result in so-called induced systemic system, namely bacteria, fungi and plants, can ‘remember’ resistance (ISR) which positively affects the response to phytopathogens infecting the leaves (e.g. Heil & Bostock, a past experience (e.g. Casades´us & D´Ari, 2002; Bruce 2002; Van Loon, 2007; Van der Ent, van Wees & Pieterse, et al., 2007; Galis et al., 2009; Rensing, Koch & Becker, 2009; 2009). Similarly, plants can be primed by association with Thellier & L¨uttge, 2013). Memory of a past event may shape symbiotic fungi (e.g. Pozo et al., 2009). Improved resistance or ‘prime’ the response to future environmental stimuli, against phytopathogens is also achieved by priming plants resulting in phenotypic and stimulus-dependent plasticity with natural or synthetic compounds. For example, treatment of response traits. Such plasticity allows an individual to of plants with salicylic acid, 2,6-dichloroisonicotinic acid adjust its physiological or developmental phenotype to its (INA), benzo-(1,2,3)-thiadiazole-7-carbothioic acid S-methyl environmental experience (Sultan, 2000; Agrawal, 2001; ester (BTH) or β-aminobutyric acid (BABA) can
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