Leaf-to-leaf long-distance signaling in response to localized cold stress in Arabidopsis thaliana

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Abstract

The molecular responses of plants to cold stress have been extensively described, leading to the identification of numerous molecular actors, including a role for Ca 2+ -dependent signaling systems. However, the degree to which systemic signaling then integrates the plant’s cold response remains poorly defined. By monitoring the regulation of early cold-responsive genes across Arabidopsis rosettes in response to localized cold stimuli, we confirmed the existence of such systemic signaling. If the plant were simply responding to the lowered ambient temperature, the effect on induction of molecular markers of cold response, such as CRT/DRE BINDING FACTORS 1-3 or MITOGEN ACTIVATED PROTEIN KINASE 6 ( MPK6 ), might be expected to fall with the distance of the different leaves from the cold source. However, although we observed increased expression in CBF1-3 in the coldest area of the rosette that fell sharply in the leaves further from the stimulus, MPK6 expression was uniformly altered throughout the rosette. This systemic regulation was impaired by application of the Ca 2+ -permeable cation channel antagonist La 3+ implying a role for Ca2+ signaling in this response. Using plants expressing GFP-based Ca 2+ biosensors, we show that a localized cold stimulus on a single leaf induces an increase of cytosolic Ca 2+ throughout distal leaves of the plant. Both systemic regulation of early cold responsive genes and propagation of long-distance calcium signals were still observed in the glr3.3/3.6 double mutant that inhibits the propagation of wound-triggered systemic Ca 2+ signals. These observations suggest the existence of a fine-tuned systemic regulation of early cold responsive genes that is driven by a long-distance calcium signaling in a GLR3.3 and GLR3.6 independent manner.
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Leaf-to-leaf long-distance signaling in response to localized cold stress in Arabidopsis thaliana | Authorea try { document.documentElement.classList.add('js'); } catch (e) { } var _gaq = _gaq || []; _gaq.push(['_setAccount', 'G-8VDV14Y67G']); _gaq.push(['_trackPageview']); (function() { var ga = document.createElement('script'); ga.type = 'text/javascript'; ga.async = true; ga.src = ('https:' == document.location.protocol ? 'https://ssl' : 'http://www') + '.google-analytics.com/ga.js'; var s = document.getElementsByTagName('script')[0]; s.parentNode.insertBefore(ga, s); })(); Skip to main content Preprints Collections Wiley Open Research IET Open Research Ecological Society of Japan All Collections About About Authorea FAQs Contact Us Quick Search anywhere Search for preprint articles, keywords, etc. Search Search ADVANCED SEARCH SCROLL This is a preprint and has not been peer reviewed. Data may be preliminary. 30 May 2025 V1 Latest version Share on Leaf-to-leaf long-distance signaling in response to localized cold stress in Arabidopsis thaliana Authors : Arthur Poitout [email protected] , Arkadipta Bakshi , Virginia Protto , Fabrice Bauget , and Simon Gilroy 0000-0001-9597-6839 Authors Info & Affiliations https://doi.org/10.22541/au.174858533.33563576/v1 491 views 165 downloads Contents Abstract Supplementary Material Information & Authors Metrics & Citations View Options References Figures Tables Media Share Abstract The molecular responses of plants to cold stress have been extensively described, leading to the identification of numerous molecular actors, including a role for Ca 2+ -dependent signaling systems. However, the degree to which systemic signaling then integrates the plant’s cold response remains poorly defined. By monitoring the regulation of early cold-responsive genes across Arabidopsis rosettes in response to localized cold stimuli, we confirmed the existence of such systemic signaling. If the plant were simply responding to the lowered ambient temperature, the effect on induction of molecular markers of cold response, such as CRT/DRE BINDING FACTORS 1-3 or MITOGEN ACTIVATED PROTEIN KINASE 6 ( MPK6 ), might be expected to fall with the distance of the different leaves from the cold source. However, although we observed increased expression in CBF1-3 in the coldest area of the rosette that fell sharply in the leaves further from the stimulus, MPK6 expression was uniformly altered throughout the rosette. This systemic regulation was impaired by application of the Ca 2+ -permeable cation channel antagonist La 3+ implying a role for Ca2+ signaling in this response. Using plants expressing GFP-based Ca 2+ biosensors, we show that a localized cold stimulus on a single leaf induces an increase of cytosolic Ca 2+ throughout distal leaves of the plant. Both systemic regulation of early cold responsive genes and propagation of long-distance calcium signals were still observed in the glr3.3/3.6 double mutant that inhibits the propagation of wound-triggered systemic Ca 2+ signals. These observations suggest the existence of a fine-tuned systemic regulation of early cold responsive genes that is driven by a long-distance calcium signaling in a GLR3.3 and GLR3.6 independent manner. Supplementary Material File (poitout et al 2025 main text.docx) Download 21.95 MB Information & Authors Information Version history V1 Version 1 30 May 2025 Copyright This work is licensed under a Non Exclusive No Reuse License. Keywords calcium cold signaling systemic Authors Affiliations Arthur Poitout [email protected] University of Wisconsin-Madison Department of Botany View all articles by this author Arkadipta Bakshi University of Wisconsin-Madison Department of Botany View all articles by this author Virginia Protto Univ Montpellier View all articles by this author Fabrice Bauget Univ Montpellier View all articles by this author Simon Gilroy 0000-0001-9597-6839 University of Wisconsin-Madison Department of Botany View all articles by this author Metrics & Citations Metrics Article Usage 491 views 165 downloads .FvxKWukQNSOunydq8rnd { width: 100px; } Citations Download citation Arthur Poitout, Arkadipta Bakshi, Virginia Protto, et al. Leaf-to-leaf long-distance signaling in response to localized cold stress in Arabidopsis thaliana. Authorea . 30 May 2025. 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