Cold-priming causes dampening of oxylipin biosynthesis and signalling during the early cold- and light-triggering response of Arabidopsis thaliana.

Andras Bittner,Bettina Hause,Margarete Baier

doi:10.1093/jxb/erab314

Andras Bittner, Bettina Hause + Show 1 more

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https://doi.org/10.1093/jxb/erab314

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Abstract

Cold-priming uncouples cold and light regulation of otherwise tightly co-regulated genes. In this study, we focused on the early regulatory processes in Arabidopsis within the first 2 h in cold and in high light after a 5-d lag-phase at 20 °C and 24 h cold-priming at 4 °C. Priming quickly modified gene expression in a trigger-specific manner. In the early stress-response phase during cold and high-light triggering, it reduced the regulatory amplitudes of many up- and down-regulated genes. A third of the priming-regulated genes were jasmonate-sensitive, including the full set of genes required for oxylipin biosynthesis. Analysis of wild-type and mutant plants based on qPCR demonstrated that biosynthesis of the jasmonic acid (JA) precursor 12-oxo phytenoic acid (OPDA) relative to the availability of JA dampened the response of the genes for oxylipin biosynthesis. In oxylipin biosynthetic mutants, cold-priming more strongly affected genes involved in the biosynthesis of OPDA than in its conversion to JA. In addition, priming-dependent dampening of the triggering response was more linked to OPDA than to regulation of the JA concentration. Spray application of OPDA prior to triggering counteracted the priming effect. Regulation of the oxylipin hub was controlled by modulation of the oxylipin-sensitivity of the genes for OPDA biosynthesis, but it was insensitive to priming-induced accumulation of thylakoid ascorbate peroxidase, thus identifying a parallel-acting cold-priming pathway.

Highlights

Priming is a highly versatile process that prepares plants to specific response to occur (Crisp et al, 2016; Hilker et al, 2016; respond more effectively to changes in conditions, whether Avramova, 2019; Baier et al, 2019)
To gain further insights into the early mechanisms of priming-dependent regulation of gene expression, we have refined our previous experiments and investigated the impact of cold-priming on regulation of gene expression by cold and heat-filtered, high light across 2-h time-courses.We show that the priming memory quickly dampens the response of genes that are essential for activation of biosynthesis of the jasmonic acid precursor oxylipin under stressful conditions and causes trigger-specific regulation of gene expression
To begin our examination of the mechanisms behind the strong jasmonic acid (JA) imprint, we evaluated the regulation of transcript abundance of genes in the CL-cluster 4 for the JA biosynthetic enzymes LOX2, LOX3, AOC2, and allene oxide synthase (AOS), together with the JA-sensitive genes MYC2, JR1, JR2, and VSP2 after 60 min in either cold or high light. quantitative PCR (qPCR) analysis of 3–4 independently grown and treated biological replicates confirmed that the genes are regulated by priming-dependent dampening (Fig. 5)

Summary

Introduction

Priming is a highly versatile process that prepares plants to specific response to occur (Crisp et al, 2016; Hilker et al, 2016; respond more effectively to changes in conditions, whether Avramova, 2019; Baier et al, 2019). Epigenetic regulation by DNA and/or histone acetylation or methylation can mediate priming (Hilker et al, 2016; Avramova, 2019; Baier et al, 2019; Friedrich et al, 2019), the majority of shifts in gene expression after short abiotic priming events result from transcriptional regulation, for example after 2 h of dehydration stress, 60 min of excess light, or 24 h of cold (Ding et al, 2013; Ganguly et al, 2019; van Buer et al, 2019; Bittner et al, 2020). Based on results such as these, we have hypothesized that the priming memory integrates into trigger-specific signalling and modifies it (Bittner et al, 2020)

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