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Roles of LESIONS SIMULATING DISEASE1 and Salicylic Acid in Acclimation of Plants to Environmental Cues: Redox Homeostasis and physiological processes underlying plants responses to biotic and abiotic challenges
Stockholm University, Faculty of Science, Department of Botany.
2005 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

In the natural environment plants are confronted to a multitude of biotic and abiotic stress factors that must be perceived, transduced, integrated and signaled in order to achieve a successful acclimation that will secure survival and reproduction. Plants have to deal with excess excitation energy (EEE) when the amount of absorbed light energy is exceeding that needed for photosynthetic CO2 assimilation. EEE results in ROS formation and can be enhanced in low light intensities by changes in other environmental factors.

The lesions simulating disease resistance (lsd1) mutant of Arabidopsis spontaneously initiates spreading lesions paralleled by ROS production in long day photoperiod and after application of salicylic acid (SA) and SA-analogues that trigger systemic acquired resistance (SAR). Moreover, the mutant fails to limit the boundaries of hypersensitive cell death (HR) after avirulent pathogen infection giving rise to the runaway cell death (rcd) phenotype. This ROS-dependent phenotype pointed towards a putative involvement of the ROS produced during photosynthesis in the initiation and spreading of the lesions.

We report here that the rcd has a ROS-concentration dependent phenotype and that the light-triggered rcd is depending on the redox-state of the PQ pool in the chloroplast. Moreover, the lower stomatal conductance and catalase activity in the mutant suggested LSD1 was required for optimal gas exchange and ROS scavenging during EEE. Through this regulation, LSD1 can influence the effectiveness of photorespiration in dissipating EEE. Moreover, low and high SA levels are strictly correlated to lower and higher foliar H2O2 content, respectively. This implies an essential role of SA in regulating the redox homeostasis of the cell and suggests that SA could trigger rcd in lsd1 by inducing H2O2 production.

LSD1 has been postulated to be a negative regulator of cell death acting as a ROS rheostat. Above a certain threshold, the pro-death pathway would operate leading to PCD. Our data suggest that LSD1 may be subjected to a turnover, enhanced in an oxidizing milieu and slowed down in a reducing environment that could reflect this ROS rheostat property. Finally, the two protein disulphide isomerase boxes (CGHC) present in the protein and the down regulation of the NADPH thioredoxin reductase (NTR) in the mutant connect the rcd to a putative impairment in the reduction of the cytosolic thioredoxin system. We propose that LSD1 suppresses the cell death processes through its control of the oxidation-reduction state of the TRX pool. An integrated model considers the role of LSD1 in both light acclimatory processes and in restricting pathogen-induced cell death.

Place, publisher, year, edition, pages
Stockholm: Botaniska institutionen , 2005. , 46 p.
Keyword [en]
LSD1, Photooxidative stress, Reactive oxygen species, Light acclimation, Photorespiration, Salicylic acid
National Category
Botany
Identifiers
URN: urn:nbn:se:su:diva-698ISBN: 91-7155-144-1 (print)OAI: oai:DiVA.org:su-698DiVA: diva2:197397
Public defence
2005-11-11, föreläsningssalen, Botanicum, Lilla Frescativägen 5, Stockholm, 10:00
Opponent
Supervisors
Available from: 2005-10-20 Created: 2005-10-20 Last updated: 2014-10-02Bibliographically approved
List of papers
1. Light perception in plant disease defence signalling
Open this publication in new window or tab >>Light perception in plant disease defence signalling
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2003 (English)In: Current opinion in plant biology, ISSN 1369-5266, E-ISSN 1879-0356, Vol. 6, no 4, 390-396 p.Article in journal (Refereed) Published
Abstract [en]

Light is a predominant factor in the control of plant growth, development and stress responses. Many biotic stress responses in plants are therefore specifically adjusted by the prevailing light conditions. The plant cell is equipped with sophisticated light-sensing mechanisms that are localised inside and outside of the chloroplast and the nucleus. Recent progress has provided models of how the signalling pathways that are involved in light perception and in defence could operate and interact to form a plant defence network. Such a signalling network includes systems to sense light and regulate gene expression. Photo-produced H2O2 and other reactive oxygen species in the cell also play an essential role in this regulatory network, controlling biotic and abiotic stress responses

National Category
Botany
Identifiers
urn:nbn:se:su:diva-24367 (URN)10.1016/S1369-5266(03)00061-X (DOI)
Note

Part of urn:nbn:se:su:diva-698

Available from: 2005-10-20 Created: 2005-10-20 Last updated: 2017-12-13Bibliographically approved
2. 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: 2017-12-13Bibliographically approved
3. Cellular processes underlying the runaway cell death phenotype in lesions simulating disease1
Open this publication in new window or tab >>Cellular processes underlying the runaway cell death phenotype in lesions simulating disease1
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Manuscript (Other academic)
Identifiers
urn:nbn:se:su:diva-24369 (URN)
Note
Part of urn:nbn:se:su:diva-698Available from: 2005-10-20 Created: 2005-10-20 Last updated: 2010-01-13Bibliographically approved
4. 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: 2017-12-13Bibliographically approved
5. On the isolation of photooxidative-stress resistant mutants
Open this publication in new window or tab >>On the isolation of photooxidative-stress resistant mutants
Manuscript (Other academic)
Identifiers
urn:nbn:se:su:diva-24371 (URN)
Note
Part of urn:nbn:se:su:diva-698Available from: 2005-10-20 Created: 2005-10-20 Last updated: 2010-01-13Bibliographically approved

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