Original Article
Priming and memory of stress responses in organisms lacking a nervous system
Monika Hilker,
Jens Schwachtje,
Margarete Baier,
Salma Balazadeh,
Isabel Bäurle,
Sven Geiselhardt,
Dirk K. Hincha,
Reinhard Kunze,
Bernd Mueller-Roeber,
Matthias C. Rillig,
Jens Rolff,
Tina Romeis,
Thomas Schmülling,
Anke Steppuhn,
Joost van Dongen,
Sarah J. Whitcomb,
Susanne Wurst,
Ellen Zuther,
Joachim Kopka,
Corresponding Author
Monika Hilker
Applied Zoology/Animal Ecology, Dahlem Centre of Plant Sciences (DCPS), Institute of Biology, Freie Universität (FU) Berlin, Haderslebener Straße 9, 12163 Berlin, Germany
Berlin-Brandenburg Institute of Advanced Biodiversity Research (BBIB), Altensteinstr. 6, 14195 Berlin, Germany
Address for correspondence (Tel: +49 (0)30 838 55913; E-mail: [email protected]).Search for more papers by this authorJens Schwachtje
Applied Metabolome Analysis, Department of Molecular Physiology, Max-Planck-Institute of Molecular Plant Physiology, Am Mühlenberg 1, 14476 Potsdam-Golm, Germany
Search for more papers by this authorMargarete Baier
Plant Physiology, DCPS, Institute of Biology, FU Berlin, Königin-Luise-Straße 12-16, 14195 Berlin, Germany
Search for more papers by this authorSalma Balazadeh
Institute for Biochemistry and Biology, Universität Potsdam, Karl-Liebknecht-Straße 24-25, Haus 20, 14476 Potsdam-Golm, Germany
Search for more papers by this authorIsabel Bäurle
Institute for Biochemistry and Biology, Universität Potsdam, Karl-Liebknecht-Straße 24-25, Haus 20, 14476 Potsdam-Golm, Germany
Search for more papers by this authorSven Geiselhardt
Applied Zoology/Animal Ecology, Dahlem Centre of Plant Sciences (DCPS), Institute of Biology, Freie Universität (FU) Berlin, Haderslebener Straße 9, 12163 Berlin, Germany
Search for more papers by this authorDirk K. Hincha
Central Infrastructure Group Transcript Profiling, Max-Planck-Institute of Molecular Plant Physiology, Am Mühlenberg 1, 14476 Potsdam-Golm, Germany
Search for more papers by this authorReinhard Kunze
Applied Genetics/Molecular Plant Genetics, DCPS, Institute of Biology, FU Berlin, Albrecht-Thaer-Weg 6, 14195 Berlin, Germany
Search for more papers by this authorBernd Mueller-Roeber
Institute for Biochemistry and Biology, Universität Potsdam, Karl-Liebknecht-Straße 24-25, Haus 20, 14476 Potsdam-Golm, Germany
Search for more papers by this authorMatthias C. Rillig
Berlin-Brandenburg Institute of Advanced Biodiversity Research (BBIB), Altensteinstr. 6, 14195 Berlin, Germany
Plant Ecology, DCPS, Institute of Biology, FU Berlin, Altensteinstraße 6, 14195 Berlin, Germany
Search for more papers by this authorJens Rolff
Evolutionary Biology, Institute of Biology, FU Berlin, Königin-Luise-Straße 1-3, 14195 Berlin, Germany
Search for more papers by this authorTina Romeis
Plant Biochemistry, DCPS, Institute of Biology, FU Berlin, Königin-Luise-Straße 12-16, 14195 Berlin, Germany
Search for more papers by this authorThomas Schmülling
Applied Genetics, DCPS, Institute of Biology, FU Berlin, Albrecht-Thaer-Weg 6, 14195 Berlin, Germany
Search for more papers by this authorAnke Steppuhn
Molecular Ecology, DCPS, Institute of Biology, FU Berlin, Haderslebener Straße 9, 12163 Berlin, Germany
Search for more papers by this authorJoost van Dongen
Rhizosphere Molecular Ecology, Institute of Biology, RWTH Aachen, Worringerweg 1, 52074 Aachen, Germany
Search for more papers by this authorSarah J. Whitcomb
Applied Metabolome Analysis, Department of Molecular Physiology, Max-Planck-Institute of Molecular Plant Physiology, Am Mühlenberg 1, 14476 Potsdam-Golm, Germany
Search for more papers by this authorSusanne Wurst
Functional Ecology, DCPS, Institute of Biology, FU Berlin, Königin-Luise-Straße 1-3, 14195 Berlin, Germany
Search for more papers by this authorEllen Zuther
Central Infrastructure Group Transcript Profiling, Max-Planck-Institute of Molecular Plant Physiology, Am Mühlenberg 1, 14476 Potsdam-Golm, Germany
Search for more papers by this authorJoachim Kopka
Applied Metabolome Analysis, Department of Molecular Physiology, Max-Planck-Institute of Molecular Plant Physiology, Am Mühlenberg 1, 14476 Potsdam-Golm, Germany
Search for more papers by this author
Monika Hilker,
Jens Schwachtje,
Margarete Baier,
Salma Balazadeh,
Isabel Bäurle,
Sven Geiselhardt,
Dirk K. Hincha,
Reinhard Kunze,
Bernd Mueller-Roeber,
Matthias C. Rillig,
Jens Rolff,
Tina Romeis,
Thomas Schmülling,
Anke Steppuhn,
Joost van Dongen,
Sarah J. Whitcomb,
Susanne Wurst,
Ellen Zuther,
Joachim Kopka,
Corresponding Author
Monika Hilker
Applied Zoology/Animal Ecology, Dahlem Centre of Plant Sciences (DCPS), Institute of Biology, Freie Universität (FU) Berlin, Haderslebener Straße 9, 12163 Berlin, Germany
Berlin-Brandenburg Institute of Advanced Biodiversity Research (BBIB), Altensteinstr. 6, 14195 Berlin, Germany
Address for correspondence (Tel: +49 (0)30 838 55913; E-mail: [email protected]).Search for more papers by this authorJens Schwachtje
Applied Metabolome Analysis, Department of Molecular Physiology, Max-Planck-Institute of Molecular Plant Physiology, Am Mühlenberg 1, 14476 Potsdam-Golm, Germany
Search for more papers by this authorMargarete Baier
Plant Physiology, DCPS, Institute of Biology, FU Berlin, Königin-Luise-Straße 12-16, 14195 Berlin, Germany
Search for more papers by this authorSalma Balazadeh
Institute for Biochemistry and Biology, Universität Potsdam, Karl-Liebknecht-Straße 24-25, Haus 20, 14476 Potsdam-Golm, Germany
Search for more papers by this authorIsabel Bäurle
Institute for Biochemistry and Biology, Universität Potsdam, Karl-Liebknecht-Straße 24-25, Haus 20, 14476 Potsdam-Golm, Germany
Search for more papers by this authorSven Geiselhardt
Applied Zoology/Animal Ecology, Dahlem Centre of Plant Sciences (DCPS), Institute of Biology, Freie Universität (FU) Berlin, Haderslebener Straße 9, 12163 Berlin, Germany
Search for more papers by this authorDirk K. Hincha
Central Infrastructure Group Transcript Profiling, Max-Planck-Institute of Molecular Plant Physiology, Am Mühlenberg 1, 14476 Potsdam-Golm, Germany
Search for more papers by this authorReinhard Kunze
Applied Genetics/Molecular Plant Genetics, DCPS, Institute of Biology, FU Berlin, Albrecht-Thaer-Weg 6, 14195 Berlin, Germany
Search for more papers by this authorBernd Mueller-Roeber
Institute for Biochemistry and Biology, Universität Potsdam, Karl-Liebknecht-Straße 24-25, Haus 20, 14476 Potsdam-Golm, Germany
Search for more papers by this authorMatthias C. Rillig
Berlin-Brandenburg Institute of Advanced Biodiversity Research (BBIB), Altensteinstr. 6, 14195 Berlin, Germany
Plant Ecology, DCPS, Institute of Biology, FU Berlin, Altensteinstraße 6, 14195 Berlin, Germany
Search for more papers by this authorJens Rolff
Evolutionary Biology, Institute of Biology, FU Berlin, Königin-Luise-Straße 1-3, 14195 Berlin, Germany
Search for more papers by this authorTina Romeis
Plant Biochemistry, DCPS, Institute of Biology, FU Berlin, Königin-Luise-Straße 12-16, 14195 Berlin, Germany
Search for more papers by this authorThomas Schmülling
Applied Genetics, DCPS, Institute of Biology, FU Berlin, Albrecht-Thaer-Weg 6, 14195 Berlin, Germany
Search for more papers by this authorAnke Steppuhn
Molecular Ecology, DCPS, Institute of Biology, FU Berlin, Haderslebener Straße 9, 12163 Berlin, Germany
Search for more papers by this authorJoost van Dongen
Rhizosphere Molecular Ecology, Institute of Biology, RWTH Aachen, Worringerweg 1, 52074 Aachen, Germany
Search for more papers by this authorSarah J. Whitcomb
Applied Metabolome Analysis, Department of Molecular Physiology, Max-Planck-Institute of Molecular Plant Physiology, Am Mühlenberg 1, 14476 Potsdam-Golm, Germany
Search for more papers by this authorSusanne Wurst
Functional Ecology, DCPS, Institute of Biology, FU Berlin, Königin-Luise-Straße 1-3, 14195 Berlin, Germany
Search for more papers by this authorEllen Zuther
Central Infrastructure Group Transcript Profiling, Max-Planck-Institute of Molecular Plant Physiology, Am Mühlenberg 1, 14476 Potsdam-Golm, Germany
Search for more papers by this authorJoachim Kopka
Applied Metabolome Analysis, Department of Molecular Physiology, Max-Planck-Institute of Molecular Plant Physiology, Am Mühlenberg 1, 14476 Potsdam-Golm, Germany
Search for more papers by this authorABSTRACT
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.
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