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Genetic and Molecular Mechanisms Controlling Reactive Oxygen Species and Hormonal Signalling of Cell Death in Response to Environmental Stresses in Arabidopsis thaliana
Stockholm University, Faculty of Science, Department of Botany.
2006 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

In the present work the regulation of environmentally induced cell death and signaling of systemic acquired acclimation (SAA) in Arabidopsis thaliana is characterized. We used the lesion simulating disease1 (lsd1) mutant as a model system that is deregulated in light acclimation and programmed cell death (PCD). In this system we identify that redox status controlling SAA and cell death is controlled by the genes LSD1, EDS1, EIN2 and PAD4 which regulate cellular homeostasis of salicylic acid (SA), ethylene (ET), auxin (IAA) and reactive oxygen species (ROS). Furthermore we propose that the roles of LSD1 in light acclimation and in biotic stress are functionally linked. The influence of SA on plant growth, short-term acclimation to high light (HL), and on the redox homeostasis of Arabidopsis leaves was also assessed. SA impaired acclimation of wild-type plants to prolonged conditions of excess excitation energy (EEE). This indicates an essential role of SA in acclimation and regulation of cellular redox homeostasis. We also show that cell death in response to EEE is controlled by specific redox changes of photosynthetic electron transport carriers that normally regulate EEE acclimation. These redox changes cause production of ET that signals through the EIN2 gene and regulon. In the lsd1 mutant, we found that propagation of cell death depends on the plant defence regulators EDS1 and PAD4 operating upstream of ET production. We conclude that the balanced activities of LSD1, EDS1, PAD4 and EIN2 regulate chloroplast dependent acclimatory and defence responses. Furthermore, we show that Arabidopsis hypocotyls form lysigenous aerenchyma in response to hypoxia and that this process involves H2O2 and ET signalling. We found that formation of lysigenous aerenchyma depends on LSD1, EDS1 and PAD4. Conclusively we show that LSD1, EDS1 and PAD4, in their functions as major plant redox and hormone regulators provide a basis for fundamental plant survival in natural contitions.

Place, publisher, year, edition, pages
Stockholm: Botaniska institutionen , 2006. , 50 p.
National Category
Botany
Identifiers
URN: urn:nbn:se:su:diva-1358ISBN: 91-7155-344-4 (print)OAI: oai:DiVA.org:su-1358DiVA: diva2:189947
Public defence
2006-12-14, föreläsningssalen, Botanicum, Lilla Frescativägen 5, Stockholm, 10:00
Opponent
Supervisors
Available from: 2006-11-23 Created: 2006-11-23 Last updated: 2013-12-10Bibliographically approved
List of papers
1. LESION SIMULATING DISEASE 1 is required for acclimation to conditions that promote excess excitation energy
Open this publication in new window or tab >>LESION SIMULATING DISEASE 1 is required for acclimation to conditions that promote excess excitation energy
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2004 (English)In: Plant Physiology, ISSN 0032-0889, E-ISSN 1532-2548, Vol. 136, no 1, 2818-2830 p.Article in journal (Refereed) Published
Abstract [en]

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.

National Category
Botany
Identifiers
urn:nbn:se:su:diva-23644 (URN)10.1104/pp.104.043646 (DOI)000223962100034 ()
Available from: 2005-03-23 Created: 2005-03-23 Last updated: 2014-10-02Bibliographically approved
2. Controlled levels of salicylic acid are required for optimal photosynthesis and redox homeostasis
Open this publication in new window or tab >>Controlled levels of salicylic acid are required for optimal photosynthesis and redox homeostasis
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2006 (English)In: Journal of Experimental Botany, ISSN 0022-0957, E-ISSN 1460-2431, Vol. 57, no 8, 1795-1807 p.Article in journal (Refereed) Published
Abstract [en]

Sudden exposure of plants to high light (HL) leads to metabolic and physiological disruption of the photosynthetic cells. Changes in ROS content, adjustment of photosynthetic processes and the antioxidant pools and, ultimately, gene induction are essential components for a successful acclimation to the new light conditions. The influence of salicylic acid (SA) on plant growth, short-term acclimation to HL, and on the redox homeostasis of Arabidopsis thaliana leaves was assessed here. The dwarf phenotype displayed by mutants with high SA content (cpr1-1, cpr5-1, cpr6-1, and dnd1-1) was less pronounced when these plants were grown in HL, suggesting that the inhibitory effect of SA on growth was partly overcome at higher light intensities. Moreover, higher SA content affected energy conversion processes in low light, but did not impair short-term acclimation to HL. On the other hand, mutants with low foliar SA content (NahG and sid2-2) were impaired in acclimation to transient exposure to HL and thus predisposed to oxidative stress. Low and high SA levels were strictly correlated to a lower and higher foliar H2O2 content, respectively. Furthermore high SA was also associated with higher GSH contents, suggesting a tight correlation between SA, H2O2 and GSH contents in plants. These observations implied an essential role of SA in the acclimation processes and in regulating the redox homeostasis of the cell. Implications for the role of SA in pathogen defence signalling are also discussed.

Place, publisher, year, edition, pages
Oxford University Press, 2006
Keyword
Arabidopsis cross tolerance defence reactions glutathione hydrogen peroxide light acclimation photo-oxidative stress photosynthesis redox signalling salicylic acid
National Category
Botany
Identifiers
urn:nbn:se:su:diva-24370 (URN)10.1093/jxb/erj196 (DOI)000238768200020 ()
Available from: 2005-10-20 Created: 2005-10-20 Last updated: 2013-12-10Bibliographically approved
3. Redox changes in the chloroplast initiate ethylene dependent signaling controlled by LESION SIMULATING DISEASE1 in Arabidopsis
Open this publication in new window or tab >>Redox changes in the chloroplast initiate ethylene dependent signaling controlled by LESION SIMULATING DISEASE1 in Arabidopsis
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Article in journal (Refereed) Submitted
Identifiers
urn:nbn:se:su:diva-23033 (URN)
Note
Part of urn:nbn:se:su:diva-1358Available from: 2006-11-23 Created: 2006-11-23Bibliographically approved
4. Lysigenous aerenchyma formation in Arabidopsis thaliana in response to hypoxia is controlled by LESION SIMULATING DISEASE1
Open this publication in new window or tab >>Lysigenous aerenchyma formation in Arabidopsis thaliana in response to hypoxia is controlled by LESION SIMULATING DISEASE1
2006 Article in journal (Refereed) Submitted
Identifiers
urn:nbn:se:su:diva-23034 (URN)
Note
Part of urn:nbn:se:su:diva-1358Available from: 2006-11-23 Created: 2006-11-23Bibliographically approved

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