Cold priming uncouples light- and cold-regulation of gene expression in Arabidopsis thaliana

Abstract

Background: The majority of stress-sensitive genes responds to cold and high light in the same direction, if plants face the stresses for the first time. As shown recently for a small selection of genes of the core environmental stress response cluster, pre-treatment of Arabidopsis thaliana with a 24 h long 4°C cold stimulus modifies cold regulation of gene expression for up to a week at 20°C, although the primary cold effects are reverted within the first 24 h. Such memory-based regulation is called priming. Here, we analyse the effect of 24 h cold priming on cold regulation of gene expression on a transcriptomewide scale and investigate if and how cold priming affects light regulation of gene expression. Results: Cold-priming affected cold and excess light regulation of a small subset of genes. In contrast to the strong gene coregulation observed upon cold and light stress in non-primed plants, most priming-sensitive genes were regulated in a stressor-specific manner in cold-primed plant. Furthermore, almost as much genes were inversely regulated as co-regulated by a 24 h long 4°C cold treatment and exposure to heat-filtered high light (800 μmol quanta m − 2 s − 1). Gene ontology enrichment analysis revealed that cold priming preferentially supports expression of genes involved in the defence against plant pathogens upon cold triggering. The regulation took place on the cost of the expression of genes involved in growth regulation and transport. On the contrary, cold priming resulted in stronger expression of genes regulating metabolism and development and weaker expression of defence genes in response to high light triggering. qPCR with independently cultivated and treated replicates confirmed the trends observed in the RNASeq guide experiment. Conclusion: A 24 h long priming cold stimulus activates a several days lasting stress memory that controls cold and light regulation of gene expression and adjusts growth and defence regulation in a stressor-specific manner.

Long-Term Waterlogging as Factor Contributing to Hypoxia Stress Tolerance Enhancement in Cucumber: Comparative Transcriptome Analysis of Waterlogging Sensitive and Tolerant Accessions

“…This may indicate that first waterlogging treatment enhanced tolerance to recurring waterlogging stress in the sensitive accession. An increased number of DEGs in primed plants, compared to non-primed plants, was also observed in rice, where salt shock was used as the priming factor [ 64 ] and in radish, where cold priming was applied [ 65 ]. To the best of our knowledge, there is no information on the differential number of regulated genes between plants treated once with hypoxic stress and plants treated again with stress, thus these results are novel and unique in the area of waterlogging tolerance in cucumber.…”

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

“…Subsequent studies have shown that a 24-h temperature shift from 20 °C to 4 °C under short-day conditions does not support cold-activation of CBF s (encoding C-repeat binding factors) or their target genes in Arabidopsis upon cold-triggering at 4 °C after a lag-phase of 5 d at 20 °C in 4-week-old plants ( van Buer et al , 2016 ), but it does result in higher expression of defence-regulated genes ( Bittner et al , 2020 ) and in decreased susceptibility to pathogens ( Griebel et al , 2020 , Preprint). The same genes are not induced in cold-primed plants by heat-filtered, high-light conditions, and some are even inversely regulated by cold-priming in response to the high light, for example the pathogen responsive genes PR4 (At3g04720) and PCC1 (At3g22231) ( Bittner et al , 2020 ). Other genes are only priming-sensitive in the cold, but not in the light, for example the light- and cold-inducible genes for the stress-signalling mediating zinc-finger transcription factors ZAT6 (At5g04340), ZAT10 (At1g27730; STZ ), and ZAT12 (At5g59820) ( Bittner et al , 2020 ).…”

“…The same genes are not induced in cold-primed plants by heat-filtered, high-light conditions, and some are even inversely regulated by cold-priming in response to the high light, for example the pathogen responsive genes PR4 (At3g04720) and PCC1 (At3g22231) ( Bittner et al , 2020 ). Other genes are only priming-sensitive in the cold, but not in the light, for example the light- and cold-inducible genes for the stress-signalling mediating zinc-finger transcription factors ZAT6 (At5g04340), ZAT10 (At1g27730; STZ ), and ZAT12 (At5g59820) ( Bittner et al , 2020 ). Although 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 ).…”

“…Other genes are only priming-sensitive in the cold, but not in the light, for example the light- and cold-inducible genes for the stress-signalling mediating zinc-finger transcription factors ZAT6 (At5g04340), ZAT10 (At1g27730; STZ ), and ZAT12 (At5g59820) ( Bittner et al , 2020 ). Although 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 ). Comparisons of the light and cold responses after cold-priming of plants has demonstrated that priming uncouples otherwise tightly linked transcriptional regulation ( Bittner et al , 2020 ).…”

“…Although 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 ). Comparisons of the light and cold responses after cold-priming of plants has demonstrated that priming uncouples otherwise tightly linked transcriptional regulation ( 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 ).…”