Ultra-fast alterations in mRNA levels uncover multiple players in light stress acclimation in plants

The acclimation of plants to changes in light intensity requires rapid responses at several different levels. These include biochemical and biophysical responses as well as alterations in the steady-state level of different transcripts and proteins. Recent studies utilizing promoter::reporter constructs suggested that transcriptional responses to changes in light intensity could occur within seconds, rates for which changes in mRNA expression are not routinely measured or functionally studied. To identify and characterize rapid changes in the steady-state level of different transcripts in response to light stress we performed RNA sequencing analysis of Arabidopsis thaliana plants subjected to light stress. Here we report that mRNA accumulation of 731 transcripts occurs as early as 20-60 sec following light stress application, and that at least five of these early response transcripts play an important biological role in the acclimation of plants to light stress. More than 20% of transcripts accumulating in plants within 20-60 sec of initiation of light stress are H₂O₂- and ABA-response transcripts, and the accumulation of several of these transcripts is inhibited by transcriptional inhibitors. In accordance with the association of rapid response transcripts with H₂O₂ and ABA signaling, a mutant impaired in ABA sensing (abi-1) was found to be more tolerant to light stress, and the response of several of the rapid response transcripts was altered in mutants impaired in reactive oxygen metabolism. Our findings reveal that transcriptome reprogramming in plants could occur within seconds of initiation of abiotic stress and that this response could invoke known as well as unknown proteins and pathways. Significance Statement Transcriptome reprogramming in plants could occur within seconds of abiotic stress initiation and could invoke known as well as unknown proteins and pathways. Here we use light stress as a case study to show that ultra-fast transcriptional responses can reveal important transcripts for abiotic stress acclimation and/or for pathogen resistance.