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Mechanisms and genes controlling the signalling network for biotic and abiotic stress defences in Arabidopsis thaliana (L.) Heyhn: Functional cross-talk between photo-produced reactive oxygen species, photosynthesis and plant disease defence responses
Stockholm University, Faculty of Science, Department of Botany.
2005 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Excess excitation energy, mechanical injury and defence against pathogens, each trigger rapid production of reactive oxygen species (ROS) in Arabidopsis thaliana leaves. ROS, such as hydrogen peroxide (H2O2), are required for the induction of systemic acquired acclimation and may lead to redox changes in photosynthetic electron transport (PET). On one hand, enhanced ROS production during stress can destroy cells, and on the other, ROS can also act as signals for the activation of stress responsive and defensive pathways.

In this work, physiological and molecular analyses of Arabidopsis mutants and transgenic lines were applied to investigate the signalling network controlling biotic and abiotic stress responses. A key enzyme of the antioxidant network is encoded by ASCORBATE PEROXIDASE 2 (APX2). Wounded leaves showed low induction of APX2 expression and when exposed to excess light, APX2 expression was increased synergistically. Signalling pathways dependent upon jasmonic acid, chitosan and abscisic acid were not involved in the wound-induced expression of APX2, but PET was required, and APX2 induction was preceded by a depressed rate of CO2 fixation.

Analysis of lsd1 (LESION SIMULATING DISEASE 1) strongly suggests that light acclimatory processes and pathogen defences are genetically and functionally linked. It is important to know that LSD1 type of mutants have mainly been studied with regard to pathogenesis. From this work, it reveals that association of LSD1 with hypersensitive response may only be supplementary.

GLUTATHIONE PEROXIDASES (GPXs) are another major family of ROS scavenging enzymes. Analysis of the Arabidopsis genome database revealed a new open-reading frame, thus increasing the total number of AtGPX gene family to eight (AtGPX1-AtGPX8). Arabidopsis thaliana transgenic lines with reduced expression of both putative chloroplastic isoforms (AtGPX1 and AtGPX7) and AtGPX7 knock-out mutant (ko-GPX7) were more sensitive to photo-oxidative stress but had a reduced bacterial growth rate when inoculated with virulent strains Pseudomonas syringae pv. tomato DC3000 and P.s.t. maculicola strain ES4326, indicating increased resistance to pathogenesis. This, to our knowledge, is the first functional and genetic analysis of chloroplastic GPXs in plants, and confirms that light and chloroplastic ROS metabolism is important for basal resistance against virulent pathogens.

The above results confirm that light sensing, light acclimatory processes and photo-produced ROS also govern pathogen defence pathways. This has a great ecological relevance for Darwinian fitness of plants growing in the natural environment, where simultaneous pathogen attack and fluctuations in light, temperature and other environmental factors make rapid acclimation a constant necessity. Molecular, biochemical and physiological analysis of pathogen responses in mutants impaired in light sensing, EEE-dissipatory mechanisms, and similar analysis of light acclimatory processes in mutants impaired in pathogen defences may prove to be seminal.

Place, publisher, year, edition, pages
Stockholm: Botaniska institutionen , 2005. , 44 p.
Keyword [en]
reactive oxygen species, Arabidopsis thaliana, signalling work, biotic stress, abiotic stress
National Category
Botany
Identifiers
URN: urn:nbn:se:su:diva-418ISBN: 91-7155-002-X (print)OAI: oai:DiVA.org:su-418DiVA: diva2:193641
Public defence
2005-04-15, föreläsningssalen, Botanicum, Lilla Frescativägen 5, Stockholm, 10:00
Opponent
Supervisors
Available from: 2005-03-23 Created: 2005-03-23Bibliographically approved
List of papers
1. Induction of ASCORBATE PEROXIDASE 2 expression in wounded Arabidopsis leaves does not involve known wound-signalling pathways but is associated with changes in photosynthesis
Open this publication in new window or tab >>Induction of ASCORBATE PEROXIDASE 2 expression in wounded Arabidopsis leaves does not involve known wound-signalling pathways but is associated with changes in photosynthesis
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2004 In: Plant Journal, Vol. 38, no 3, 499-511 p.Article in journal (Refereed) Published
Identifiers
urn:nbn:se:su:diva-23643 (URN)
Note
Part of urn:nbn:se:su:diva-418Available from: 2005-03-23 Created: 2005-03-23Bibliographically 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. Functional characterization of the chloroplastic glutathione peroxidases (cpGPXs) in Arabidopsis thaliana: its role in light acclimatory mechanisms
Open this publication in new window or tab >>Functional characterization of the chloroplastic glutathione peroxidases (cpGPXs) in Arabidopsis thaliana: its role in light acclimatory mechanisms
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Manuscript (Other academic)
Identifiers
urn:nbn:se:su:diva-23645 (URN)
Note
Part of urn:nbn:se:su:diva-418Available from: 2005-03-23 Created: 2005-03-23 Last updated: 2010-01-13Bibliographically approved
4. Functional analysis of chloroplastic glutathione peroxidases (cpGPXs) in Arabidopsis thaliana provides a direct link between photo-oxidative stress and basal pathogen resistance mechanisms
Open this publication in new window or tab >>Functional analysis of chloroplastic glutathione peroxidases (cpGPXs) in Arabidopsis thaliana provides a direct link between photo-oxidative stress and basal pathogen resistance mechanisms
Show others...
Manuscript (Other academic)
Identifiers
urn:nbn:se:su:diva-23646 (URN)
Note
Part of urn:nbn:se:su:diva-418Available from: 2005-03-23 Created: 2005-03-23 Last updated: 2010-01-13Bibliographically approved

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