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First published online September 3, 2004; 10.1104/pp.104.043646

Plant Physiology 136:2818-2830 (2004)
© 2004 American Society of Plant Biologists

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ENVIRONMENTAL STRESS AND ADAPTATION

LESION SIMULATING DISEASE 1 Is Required for Acclimation to Conditions That Promote Excess Excitation Energy1,2,[w]

Alfonso Mateo, Per Mühlenbock, Christine Rustérucci, Christine Chi-Chen Chang, Zbigniew Miszalski, Barbara Karpinska, Jane E. Parker, Philip M. Mullineaux and Stanislaw Karpinski*

Department of Botany, Stockholm University, Stockholm SE–106 91, Sweden (A.M., P.M., C.C.C., B.K., S.K.); Department of Plant Physiology, Umea University and Umea Plant Science Centre, SE–901 85 Umea, Sweden (S.K.); Department of Biological Sciences, University of Essex, Colchester, CO4 3SQ, United Kingdom (P.M.M.); Department of Plant-Microbe Interactions, Max-Planck Institute for Plant Breeding Research, D–50829 Cologne, Germany (C.R., J.E.P.); and Institute of Plant Physiology, Polish Academy of Sciences, 30–239 Krakow, Poland (Z.M.)

The lsd1 mutant of Arabidopsis fails to limit the boundaries of hypersensitive cell death response during avirulent pathogen infection and initiates unchecked lesions in long day photoperiod giving rise to the runaway cell death (rcd) phenotype. We link here the initiation and propagation of rcd to the activity of photosystem II, stomatal conductance and ultimately to photorespiratory H2O2. A cross of lsd1 with the chlorophyll a/b binding harvesting-organelle specific (designated cao) mutant, which has a reduced photosystem II antenna, led to reduced lesion formation in the lsd1/cao double mutant. This lsd1 mutant also had reduced stomatal conductance and catalase activity in short-day permissive conditions and induced H2O2 accumulation followed by rcd when stomatal gas exchange was further impeded. All of these traits depended on the defense regulators EDS1 and PAD4. Furthermore, nonphotorespiratory conditions retarded propagation of lesions in lsd1. These data suggest that lsd1 failed to acclimate to light conditions that promote excess excitation energy (EEE) and that LSD1 function was required for optimal catalase activity. Through this regulation LSD1 can influence the effectiveness of photorespiration in dissipating EEE and consequently may be a key determinant of acclimatory processes. Salicylic acid, which induces stomatal closure, inhibits catalase activity and triggers the rcd phenotype in lsd1, also impaired acclimation of wild-type plants to conditions that promote EEE. We propose that the roles of LSD1 in light acclimation and in restricting pathogen-induced cell death are functionally linked.

1 This work was supported by the Department of Botany at Stockholm University, by the Swedish Research Councils (VR and FORMAS), by Carl Tryggers Foundation and the Swedish Council for International Cooperation in Research and Higher Education (STINT), and by the Wallenberg Consortium North (to S.K. and B.K.). P.M.M. acknowledges the support of the UK Biotechnology and Biological Sciences Research Council. C.R. and J.E.P. are grateful to The European Commission for a Marie-Curie postdoctoral training fellowship and The Alexander von Humboldt Foundation for funding. Z.M. is grateful to The European Commission for funding from project (QLAM–2001–00424).

2 In memory of Dr. Anna Siedlecka and members of her family who tragically died on May 26, 2004.

[w] The online version of this article contains Web-only data.

Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.104.043646.

* Corresponding author; e-mail stanislaw.karpinski{at}botan.su.se; fax 00–46–8–1625–55.

Received March 27, 2004; returned for revision June 9, 2004; accepted June 9, 2004.




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