The Role of Salicylic Acid in the Induction of Cell Death in Arabidopsis <i>acd11</i>

Brodersen, Peter; Malinovsky, Frederikke Gro; Hématy, Kian; Newman, Mari‐Anne; Mundy, John

doi:10.1104/pp.105.059303

Cited by 143 publications

(114 citation statements)

References 60 publications

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“…1). This function has already been shown for the Arabidopsis ICS1 gene (12,35). Here, we provide the genetic evidence that both ICS1 and ICS2 are also required for the synthesis of PhQ.…”

Section: Essential Role Of Phylloquinone In Higher Plants-the Analysimentioning

confidence: 56%

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A Plant Locus Essential for Phylloquinone (Vitamin K1) Biosynthesis Originated from a Fusion of Four Eubacterial Genes

Gross

Cho

Lezhneva

et al. 2006

Journal of Biological Chemistry

136

162

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Phylloquinone is a compound present in all photosynthetic plants serving as cofactor for Photosystem I-mediated electron transport. Newly identified seedling-lethal Arabidopsis thaliana mutants impaired in the biosynthesis of phylloquinone possess reduced Photosystem I activity. The affected gene, called PHYLLO, consists of a fusion of four previously individual eubacterial genes, menF, menD, menC, and menH, required for the biosynthesis of phylloquinone in photosynthetic cyanobacteria and the respiratory menaquinone in eubacteria. The fact that homologous men genes reside as polycistronic units in eubacterial chromosomes and in plastomes of red algae strongly suggests that PHYLLO derived from a plastid operon during endosymbiosis. The principle architecture of the fused PHYLLO locus is conserved in the nuclear genomes of plants, green algae, and the diatom alga Thalassiosira pseudonana. The latter arose from secondary endosymbiosis of a red algae and a eukaryotic host indicating selective driving forces for maintenance and/or independent generation of the composite gene cluster within the nuclear genomes. Besides, individual menF genes, encoding active isochorismate synthases (ICS), have been established followed by splitting of the essential 3 region of the menF module of PHYLLO only in genomes of higher plants. This resulted in inactivation of the ICS activity encoded by PHYLLO and enabled a metabolic branch from the phylloquinone biosynthetic route to independently regulate the synthesis of salicylic acid required for plant defense. Therefore, gene fusion, duplication, and fission events adapted a eubacterial multienzymatic system to the metabolic requirements of plants.

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“…1). This function has already been shown for the Arabidopsis ICS1 gene (12,35). Here, we provide the genetic evidence that both ICS1 and ICS2 are also required for the synthesis of PhQ.…”

Section: Essential Role Of Phylloquinone In Higher Plants-the Analysimentioning

confidence: 56%

“…suggesting that PhQ or its intermediates could trigger cell death responses associated with plant defense against phytopathogens (35). In any case, a metabolic link between photosynthesis and plant resistance has now been established that provokes further investigations.…”

Section: Essential Role Of Phylloquinone In Higher Plants-the Analysimentioning

confidence: 99%

A Plant Locus Essential for Phylloquinone (Vitamin K1) Biosynthesis Originated from a Fusion of Four Eubacterial Genes

Gross

Cho

Lezhneva

et al. 2006

Journal of Biological Chemistry

136

162

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“…These studies have shown that catalase deficiency in tobacco and Arabidopsis mimics many of the effects of environmental stresses on gene expression and on redox homeostasis (Willekens et al, 1997;Chamnongpol et al, 1998;Mittler et al, 1999;Vandenabeele et al, 2004;Vanderauwera et al, 2005;. While many mutants that show spontaneous lesion formation have been described (Dietrich et al, 1994;Lorrain et al, 2003;Brodersen et al, 2005;Meng et al, 2009), questions remain concerning the relationship of the affected genes to changes in ROS availability, which are known to be important in the responses of plants to stress. Unlike many lesion-mimic mutants, increased H 2 O 2 availability is unambiguously the initiating signal of responses in catalase-deficient plants.…”

Section: Discussionmentioning

confidence: 99%

“…In some lesion-mimic mutants, a link with SA has been demonstrated, although in several cases the role of SA itself is less clear (Hunt et al, 1997;Lorrain et al, 2003;Brodersen et al, 2005;Meng et al, 2009). Previous studies showed that SA accumulates in catalase-deficient tobacco (Takahashi et al, 1997;Chamnongpol et al, 1998).…”

Section: Discussionmentioning

confidence: 99%

Peroxisomal Hydrogen Peroxide Is Coupled to Biotic Defense Responses by ISOCHORISMATE SYNTHASE1 in a Daylength-Related Manner

et al. 2010

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While it is well established that reactive oxygen species can induce cell death, intracellularly generated oxidative stress does not induce lesions in the Arabidopsis (Arabidopsis thaliana) photorespiratory mutant cat2 when plants are grown in short days (SD). One interpretation of this observation is that a function necessary to couple peroxisomal hydrogen peroxide (H 2 O 2 )-triggered oxidative stress to cell death is only operative in long days (LD). Like lesion formation, pathogenesis-related genes and camalexin were only induced in cat2 in LD, despite less severe intracellular redox perturbation compared with SD. Lesion formation triggered by peroxisomal H 2 O 2 was modified by introducing secondary mutations into the cat2 background and was completely absent in cat2 sid2 double mutants, in which ISOCHORISMATE SYNTHASE1 (ICS1) activity is defective. In addition to H 2 O 2 -induced salicylic acid (SA) accumulation, the sid2 mutation in ICS1 abolished a range of LD-dependent pathogen responses in cat2, while supplementation of cat2 with SA in SD activated these responses. Nontargeted transcript and metabolite profiling identified clusters of genes and small molecules associated with the daylength-dependent ICS1-mediated relay of H 2 O 2 signaling. The effect of oxidative stress in cat2 on resistance to biotic challenge was dependent on both growth daylength and ICS1. We conclude that (1) lesions induced by intracellular oxidative stress originating in the peroxisomes can be genetically reverted; (2) the isochorismate pathway of SA synthesis couples intracellular oxidative stress to cell death and associated disease resistance responses; and (3) camalexin accumulation was strictly dependent on the simultaneous presence of both H 2 O 2 and SA signals.

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“…The basal level of SA can vary between species and even within the same plant family (Raskin et al, 1990). For Arabidopsis, basal levels of SA between 2 mmol and 8 mmol g 21 FW have been reported (Brodersen et al, 2005;Klessig et al, 2016;Nawrath and Métraux, 1999;Wildermuth et al, 2001), with SA rising to ;40 mmol g 21 FW during infection, which has been equated to ;70 mM inside infected plant cells (Bi et al, 1995). The importance of SA in response to biotic and abiotic stress and its involvement in the transcriptional regulation of defense genes has been extensively studied and reviewed (Herrera-Vásquez et al, 2015).…”

Section: Low Concentrations Of Sa Increase Sqr Activitymentioning

confidence: 99%

Salicylic Acid-Dependent Plant Stress Signaling via Mitochondrial Succinate Dehydrogenase

et al. 2017

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Mitochondria are known for their role in ATP production and generation of reactive oxygen species, but little is known about the mechanism of their early involvement in plant stress signaling. The role of mitochondrial succinate dehydrogenase (SDH) in salicylic acid (SA) signaling was analyzed using two mutants: disrupted in stress response1 (dsr1), which is a point mutation in SDH1 identified in a loss of SA signaling screen, and a knockdown mutant (sdhaf2) for SDH assembly factor 2 that is required for FAD insertion into SDH1. Both mutants showed strongly decreased SA-inducible stress promoter responses and low SDH maximum capacity compared to wild type, while dsr1 also showed low succinate affinity, low catalytic efficiency, and increased resistance to SDH competitive inhibitors. The SA-induced promoter responses could be partially rescued in sdhaf2, but not in dsr1, by supplementing the plant growth media with succinate. Kinetic characterization showed that low concentrations of either SA or ubiquinone binding site inhibitors increased SDH activity and induced mitochondrial H 2 O 2 production. Both dsr1 and sdhaf2 showed lower rates of SA-dependent H 2 O 2 production in vitro in line with their low SA-dependent stress signaling responses in vivo. This provides quantitative and kinetic evidence that SA acts at or near the ubiquinone binding site of SDH to stimulate activity and contributes to plant stress signaling by increased rates of mitochondrial H 2 O 2 production, leading to part of the SA-dependent transcriptional response in plant cells.

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The Role of Salicylic Acid in the Induction of Cell Death in Arabidopsis acd11

Cited by 143 publications

References 60 publications

A Plant Locus Essential for Phylloquinone (Vitamin K1) Biosynthesis Originated from a Fusion of Four Eubacterial Genes

A Plant Locus Essential for Phylloquinone (Vitamin K1) Biosynthesis Originated from a Fusion of Four Eubacterial Genes

Peroxisomal Hydrogen Peroxide Is Coupled to Biotic Defense Responses by ISOCHORISMATE SYNTHASE1 in a Daylength-Related Manner

Salicylic Acid-Dependent Plant Stress Signaling via Mitochondrial Succinate Dehydrogenase

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