Chloroplast Signaling and<i>LESION SIMULATING DISEASE1</i>Regulate Crosstalk between Light Acclimation and Immunity in<i>Arabidopsis</i>

Mühlenbock, Per; Szechyńska‐Hebda, Magdalena; Płaszczyca, Marian; Baudo, Marcela; Mateo, Alfonso; Mullineaux, Philip M.; Parker, Jane E.; Karpińska, Barbara; Karpiński, Stanisław

doi:10.1105/tpc.108.059618

Cited by 299 publications

(430 citation statements)

References 71 publications

(155 reference statements)

Supporting

Mentioning

412

Contrasting

Unclassified

Order By: Relevance

“…It has been shown that PAD4 and EDS1 participate not only in resistance to pathogens but also in the transduction of photooxidative stress signals resulting in cell death and growth inhibition. Cell death and growth inhibition phenotypes of lsd1, acd6-1, cpr1, and cpr6 mutants require the presence of PAD4 and EDS1, as demonstrated by the rescue of mutant phenotypes in double mutants with pad4 or eds1 (Jirage et al, 2001;Rustérucci et al, 2001;Mateo et al, 2004;Ochsenbein et al, 2006;Mühlenbock et al, 2008;Ng et al, 2011). The SA amplification loop is also crucial for cell death and senescence, increased SA content, and gene expression changes in saul1 mutants challenged by low light (Fig.…”

Section: Discussionmentioning

confidence: 99%

Early Senescence and Cell Death in Arabidopsis saul1 Mutants Involves the PAD4-Dependent Salicylic Acid Pathway

Vogelmann

Drechsel²,

Bergler³

et al. 2012

Plant Physiology

View full text Add to dashboard Cite

Age-dependent leaf senescence and cell death in Arabidopsis (Arabidopsis thaliana) requires activation of the transcription factor ORESARA1 (ORE1) and is not initiated prior to a leaf age of 28 d. Here, we investigate the conditional execution of events that regulate early senescence and cell death in senescence-associated ubiquitin ligase1 (saul1) mutants, deficient in the PLANT U-BOX-ARMADILLO E3 ubiquitin ligase SAUL1. In saul1 mutants challenged with low light, the switch of age-dependent cell death was turned on prematurely, as indicated by the accumulation of ORE1 transcripts, induction of the senescence marker gene SENESCENCE-ASSOCIATED GENE12, and cell death. However, ORE1 accumulation by itself was not sufficient to cause saul1 phenotypes, as demonstrated by double mutant analysis. Exposure of saul1 mutants to low light for only 24 h did not result in visible symptoms of senescence; however, the senescence-promoting transcription factor genes WRKY53, WRKY6, and NAC-LIKE ACTIVATED BY AP3/PI were up-regulated, indicating that senescence in saul1 seedlings was already initiated. To resolve the time course of gene expression, microarray experiments were performed at narrow intervals. Differential expression of the genes involved in salicylic acid and defense mechanisms were the earliest events detected, suggesting a central role for salicylic acid in saul1 senescence and cell death. The salicylic acid content increased in low-light-treated saul1 mutants, and application of exogenous salicylic acid was indeed sufficient to trigger saul1 senescence in permissive light conditions. Double mutant analyses showed that PHYTOALEXIN DEFICIENT4 (PAD4) but not NONEXPRESSER OF PR GENES1 (NPR1) is essential for saul1 phenotypes. Our results indicate that saul1 senescence depends on the PAD4-dependent salicylic acid pathway but does not require NPR1 signaling.

show abstract

Section: Discussionmentioning

confidence: 99%

Early Senescence and Cell Death in Arabidopsis saul1 Mutants Involves the PAD4-Dependent Salicylic Acid Pathway

Vogelmann

Drechsel²,

Bergler³

et al. 2012

Plant Physiology

View full text Add to dashboard Cite

show abstract

“…EDS1, in response to chloroplast-sourced ROS, also activates SA and other hormone-controlled signaling, which produces intercellular signal(s) that stimulate a further burst of ROS, leading to cell death and the development of lesions (Mü hlenbock et al, 2008;Straus et al, 2010). However, at some point, the spread of lesions is contained and the signaling changes to produce a response that pushes the cell into defense mode.…”

Section: Ros Signaling In Cells Neighboring Cell Death Lesionsmentioning

confidence: 99%

“…For both systemic acquired acclimation to excess light and systemic acquired resistance to biotrophic pathogens, the underlying responses seem to predominantly involve reiteration of the events in challenged leaves, but with much less intensity (Alvarez et al, 1998;Karpinski et al, 1999;Rossel et al, 2007;Mü hlenbock et al, 2008). The reduced intensity of the response may represent a raised threshold that pushes cells more into acclimation or resistance and away from cell death at an earlier stage.…”

Section: Systemic Signalingmentioning

confidence: 99%

“…These observations may reflect a convergence of ROS signaling pathways from the chloroplasts that feed into another dynamic antagonistically regulated system that is now considered. Under excess light conditions that would produce a strong burst of 1 O 2 and other ROS in the chloroplast, there is now good evidence of the activation of SA-and ethylene-induced defenses that confer resistance to biotrophic pathogens and are associated with ROSinduced local lesions, similar to those produced in the hypersensitive response (HR) to avirulent biotrophic pathogens (Mü hlenbock et al, 2008;Straus et al, 2010). One of the key genes emerging from such studies is ENHANCED DISEASE SUSCEPTIBILITY1 (EDS1), which plays a role in development of the HR and mediates EXE1/EXE2 1 O 2 -regulated cell death (Ochsenbein et al, 2006).…”

Section: O 2 Signalingmentioning

confidence: 99%

See 1 more Smart Citation

Oxidative Stress: Antagonistic Signaling for Acclimation or Cell Death?

2010

Self Cite

View full text Add to dashboard Cite

Severe environmental stress imposed on plant tissues induces changes in oxygen (O 2 ) metabolism that cause oxidative stress. Oxidative stress occurs when reactive oxygen species (ROS) are not rapidly scavenged and the rate of repair of damaged cell components fails to keep pace with the rate of damage. If this situation persists, irreversible damage results in a loss of physiological competence and eventual cell death. However, ROS production in leaves resulting from moderate environmental stresses, within the adaptive range of the plant, also has important local and systemic signaling roles. In these circumstances, ROS production induces defense mechanisms that protect the plant but do not result in oxidative stress. We shall illustrate ROS involvement in signaling in both of these situations by considering the role of chloroplasts in initiating cellular responses to environmental perturbations, choosing examples where this organelle interacts with specific signaling pathways.

show abstract

“…Oxidative signals arising from photorespiration make an important contribution to immunity towards pathogens [40,41]. Cysteine residues on proteins such as peroxiredoxins, and thioredoxins and on low molecular weight thiols such as GSH mediate signal transduction leading to the activation of defence responses [13,14,29,40].…”

Section: (A) Chloroplast Redox Signalsmentioning

confidence: 99%

The functions of WHIRLY1 and REDOX-RESPONSIVE TRANSCRIPTION FACTOR 1 in cross tolerance responses in plants: a hypothesis

Foyer

Karpińska

Krupinska

2014

Phil. Trans. R. Soc. B

113

107

View full text Add to dashboard Cite

Chloroplasts are important sensors of environment change, fulfilling key roles in the regulation of plant growth and development in relation to environmental cues. Photosynthesis produces a repertoire of reductive and oxidative (redox) signals that provide information to the nucleus facilitating appropriate acclimation to a changing light environment. Redox signals are also recognized by the cellular innate immune system allowing activation of non-specific, stress-responsive pathways that underpin cross tolerance to biotic–abiotic stresses. While these pathways have been intensively studied in recent years, little is known about the different components that mediate chloroplast-to-nucleus signalling and facilitate cross tolerance phenomena. Here, we consider the properties of the WHIRLY family of proteins and the REDOX-RESPONSIVE TRANSCRIPTION FACTOR 1 (RRTF1) in relation to chloroplast redox signals that facilitate the synergistic co-activation of gene expression pathways and confer cross tolerance to abiotic and biotic stresses. We propose a new hypothesis for the role of WHIRLY1 as a redox sensor in chloroplast-to-nucleus retrograde signalling leading to cross tolerance, including acclimation and immunity responses. By virtue of its association with chloroplast nucleoids and with nuclear DNA, WHIRLY1 is an attractive candidate coordinator of the expression of photosynthetic genes in the nucleus and chloroplasts. We propose that the redox state of the photosynthetic electron transport chain triggers the movement of WHIRLY1 from the chloroplasts to the nucleus, and draw parallels with the regulation of NONEXPRESSOR OF PATHOGENESIS-RELATED GENES 1 (NPR1).

show abstract

Chloroplast Signaling andLESION SIMULATING DISEASE1Regulate Crosstalk between Light Acclimation and Immunity inArabidopsis

Cited by 299 publications

References 71 publications

Early Senescence and Cell Death in Arabidopsis saul1 Mutants Involves the PAD4-Dependent Salicylic Acid Pathway

Early Senescence and Cell Death in Arabidopsis saul1 Mutants Involves the PAD4-Dependent Salicylic Acid Pathway

Oxidative Stress: Antagonistic Signaling for Acclimation or Cell Death?

The functions of WHIRLY1 and REDOX-RESPONSIVE TRANSCRIPTION FACTOR 1 in cross tolerance responses in plants: a hypothesis

Contact Info

Product

Resources

About