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Chloroplast Signaling and LESION SIMULATING DISEASE1 Regulate Crosstalk between Light Acclimation and Immunity in Arabidopsis^[W]

Per Mühlenbock^a, Magdalena Szechyska-Hebda^a, Marian Paszczyca^a, Marcela Baudo^a, Alfonso Mateo^a, Philip M. Mullineaux^b, Jane E. Parker^c, Barbara Karpiska^d,1 and Stanisaw Karpiski^e,1

^a Department of Botany, Stockholm University, 106 91 Stockholm, Sweden
^b University of Essex, Colchester CO4 3SQ, United Kingdom
^c Department of Plant–Microbe Interactions, Max-Planck Institute for Breeding Research, D-50892 Cologne, Germany
^d Department of Life Sciences, Södertörn University College, 141 89 Huddinge, Sweden
^e Department of Plant Genetics, Breeding, and Biotechnology, University of Life Sciences, 02-776 Warszawa, Poland

¹ Address correspondence to barbara.karpinska{at}sh.se or stanislaw_karpinski{at}sggw.pl.

Plants are simultaneously exposed to abiotic and biotic hazards. Here, we show that local and systemic acclimation in Arabidopsis thaliana leaves in response to excess excitation energy (EEE) is associated with cell death and is regulated by specific redox changes of the plastoquinone (PQ) pool. These redox changes cause a rapid decrease of stomatal conductance, global induction of ASCORBATE PEROXIDASE2 and PATHOGEN RESISTANCE1, and increased production of reactive oxygen species (ROS) and ethylene that signals through ETHYLENE INSENSITIVE2 (EIN2). We provide evidence that multiple hormonal/ROS signaling pathways regulate the plant's response to EEE and that EEE stimulates systemic acquired resistance and basal defenses to virulent biotrophic bacteria. In the Arabidopsis LESION SIMULATING DISEASE1 (lsd1) null mutant that is deregulated for EEE acclimation responses, propagation of EEE-induced programmed cell death depends on the plant defense regulators ENHANCED DISEASE SUSCEPTIBILITY1 (EDS1) and PHYTOALEXIN DEFICIENT4 (PAD4). We find that EDS1 and PAD4 operate upstream of ethylene and ROS production in the EEE response. The data suggest that the balanced activities of LSD1, EDS1, PAD4, and EIN2 regulate signaling of programmed cell death, light acclimation, and holistic defense responses that are initiated, at least in part, by redox changes of the PQ pool.

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