Abstract
Key message
Transcriptomes of solanaceous plants expressing a plastid-targeted antioxidant protein were analysed to identify chloroplast redox networks modulating the expression of nuclear genes associated with stress acclimation.
Abstract
Plastid functions depend on the coordinated expression of nuclear genes, many of them associated to developmental and stress response pathways. Plastid-generated signals mediate this coordination via retrograde signaling, which includes sensing of chloroplast redox state and levels of reactive oxygen species (ROS), although it remains a poorly understood process. Chloroplast redox poise and ROS build-up can be modified by recombinant expression of a plastid-targeted antioxidant protein, i.e., cyanobacterial flavodoxin, with the resulting plants displaying increased tolerance to multiple environmental challenges. Here we analysed the transcriptomes of these flavodoxin-expressing plants to study the coordinated transcriptional responses of the nucleus to the chloroplast redox status and ROS levels during normal growth and stress responses (drought or biotic stress) in tobacco and potato, members of the economically important Solanaceae family. We compared their transcriptomes against those from stressed and mutant plants accumulating ROS in different subcellular compartments and found distinct ROS-related imprints modulated by flavodoxin expression and/or stress. By introducing our datasets in a large-scale interaction network, we identified transcriptional factors related to ROS and stress responses potentially involved in flavodoxin-associated signaling. Finally, we discovered identical cis elements in the promoters of many genes that respond to flavodoxin in the same direction as in wild-type plants under stress, suggesting a priming effect of flavodoxin before stress manifestation. The results provide a genome-wide picture illustrating the relevance of chloroplast redox status on biotic and abiotic stress responses and suggest new cis and trans targets to generate stress-tolerant solanaceous crops.
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The authors declare that all the data supporting the findings of this study are publicly available.
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Acknowledgements
NC is Staff Member from the National Research Council (CONICET, Argentina) and Professor at the School of Biochemical and Pharmaceutical Sciences, University of Rosario (Facultad de Ciencias Bioquímicas y Farmacéuticas, UNR, Argentina). JJPK is post-doctoral Fellow of the Fonds Français pour l'Environnement Mondial (FFEM) and RCA is a doctoral Fellow of CONICET.
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The current work was funded by the National Research Council (CONICET, Argentina) and the Fonds Français pour l'Environnement Mondial (FFEM).
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JJPK designed the project. RCA carried out the bioinformatic analysis. RCA, NC, and JJPK analyzed the results and wrote the manuscript.
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Arce, R.C., Carrillo, N. & Pierella Karlusich, J.J. The chloroplast redox-responsive transcriptome of solanaceous plants reveals significant nuclear gene regulatory motifs associated to stress acclimation. Plant Mol Biol 108, 513–530 (2022). https://doi.org/10.1007/s11103-022-01240-5
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DOI: https://doi.org/10.1007/s11103-022-01240-5