Retrograde signaling and plant stress: plastid signals initiate cellular stress responses

Fernández, Aurora Piñas; Strand, Åsa

doi:10.1016/j.pbi.2008.06.002

Cited by 148 publications

(111 citation statements)

References 42 publications

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“…Therefore, the amount of unfolded plastid precursors must be precisely Regulation of Precursor Levels by Hsc70-4 and CHIP 3997 maintained below a threshold at which nonspecific protein aggregates can form. Retrograde signals from the plastid to the nucleus may help regulate the amount of precursors at the transcriptional level (Ferná ndez and Strand, 2008). Alternatively, if the cellular plastid precursor level exceeds the protein import capacity of plastids, the excess precursors may be actively removed by protein degradation.…”

Section: Discussionmentioning

confidence: 99%

Heat Shock Protein Cognate 70-4 and an E3 Ubiquitin Ligase, CHIP, Mediate Plastid-Destined Precursor Degradation through the Ubiquitin-26S Proteasome System inArabidopsis

et al. 2009

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Plastid-targeted proteins pass through the cytosol as unfolded precursors. If proteins accumulate in the cytosol, they can form nonspecific aggregates that cause severe cellular damage. Here, we demonstrate that high levels of plastid precursors are degraded through the ubiquitin-proteasome system (UPS) in Arabidopsis thaliana cells. The cytosolic heat shock protein cognate 70-4 (Hsc70-4) and E3 ligase carboxy terminus of Hsc70-interacting protein (CHIP) were highly induced in plastid protein import2 plants, which had a T-DNA insertion at Toc159 and showed an albino phenotype and a severe defect in protein import into chloroplasts. Hsc70-4 and CHIP together mediated plastid precursor degradation when import-defective chloroplast-targeted reporter proteins were transiently expressed in protoplasts. Hsc70-4 recognized specific sequence motifs in transit peptides and thereby led to precursor degradation through the UPS. CHIP, which interacted with Hsc70-4, functioned as an E3 ligase in the Hsc70-4-mediated protein degradation. The physiological role of Hsc70-4 was confirmed by analyzing Hsc70-4 RNA interfernce plants in an hsc70-1 mutant background. Plants with lower Hsc70 levels exhibited abnormal embryogenesis, resulting in defective seedlings that displayed high levels of reactive oxygen species and monoubiquitinated Lhcb4 precursors. We propose that Hsc70-4 and CHIP mediate plastid-destined precursor degradation to prevent cytosolic precursor accumulation and thereby play a critical role in embryogenesis. INTRODUCTIONProteins destined for the two endosymbiotic organelles (i.e., plastids and mitochondria) are targeted from the cytoplasm as unfolded precursors (Keegstra and Froehlich, 1999;Koumoto et al., 2001;Jarvis and Soll, 2002;Soll and Schleiff, 2004;Jarvis, 2008). In the cytosol, unfolded proteins have a high tendency to form cytotoxic, life-threatening, and nonspecific aggregates if they accumulate to high levels (Wickner et al., 1999;Esser et al., 2004;Meredith, 2005;Kabashi and Durham, 2006). Therefore, posttranslational targeting to endosymbiotic organelles requires that precursor levels be maintained within limits that do not result in nonspecific aggregate formation. At the same time, the cytosolic regulatory mechanism must not jeopardize the supply of sufficient amounts of proteins to the organelles.Eukaryotic cells have a protein quality control (PQC) mechanism to constantly monitor the quality of newly synthesized proteins and preexisting proteins and to actively remove unfolded or misfolded proteins (Hartl and Hayer-Hartl, 2002;Hatakeyama and Nakayama, 2003;Esser et al., 2004). It is reported that as much as 30% of newly synthesized proteins are immediately degraded by the PQC system because of a problem in protein folding (Schubert et al., 2000). The PQC in the cytosol is achieved by two opposing processes: chaperone-assisted folding and ubiquitin/proteasome-mediated degradation. The molecular chaperones heat shock protein 70 (Hsp70) and heat shock protein cognate 70 (Hsc70), whose levels are ele...

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Section: Discussionmentioning

confidence: 99%

Heat Shock Protein Cognate 70-4 and an E3 Ubiquitin Ligase, CHIP, Mediate Plastid-Destined Precursor Degradation through the Ubiquitin-26S Proteasome System inArabidopsis

et al. 2009

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“…The redox state of PET has been shown to influence a diversity of phenomena from altering the excitation distribution between photosystems through state transitions controlled by STN7, a chloroplast thylakoid protein kinase in Arabidopsis thaliana (Rochaix, 2004;Kargul and Barber, 2008), to changes in organellar gene expression (Pfannschmidt et al, 1999;Pfannschmidt, 2003) and nuclear gene expression through retrograde regulation (Pfannschmidt, 2003;Ferná ndez and Strand, 2008;Woodson and Chory, 2008;Pesaresi et al, 2009;Pfannschmidt et al, 2009), to changes in plant growth habit and morphology (Gray et al, 1997). Furthermore, tobacco (Nicotiana tabacum) plants deficient in ferredoxin-NADP(H) reductase exhibit a yellow-green phenotype due to the overreduction of the intersystem PET chain.…”

Section: Introductionmentioning

confidence: 99%

“…These and additional signals, including the precursor of chlorophyll synthesis, magnesium protoporphyrin (Strand et al, 2003), and reactive oxygen species (ROS) generated by the PET (Meskauskiene et al, 2001;op den Camp et al, 2003), may constitute a complex network of signals involved in the retrograde pathway of communication from the chloroplast to the nucleus (Koussevitzky et al, 2007;Ferná ndez and Strand, 2008;Woodson and Chory, 2008). However, the putative role of Mg-protoporphyrin in retrograde signaling remains equivocal (Mochizuki et al, 2008;Moulin et al, 2008).…”

Section: Introductionmentioning

confidence: 99%

Photosynthetic Redox Imbalance Governs Leaf Sectoring in theArabidopsis thalianaVariegation Mutantsimmutans,spotty,var1, andvar2

et al. 2009

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We hypothesized that chloroplast energy imbalance sensed through alterations in the redox state of the photosynthetic electron transport chain, measured as excitation pressure, governs the extent of variegation in the immutans mutant of Arabidopsis thaliana. To test this hypothesis, we developed a nondestructive imaging technique and used it to quantify the extent of variegation in vivo as a function of growth temperature and irradiance. The extent of variegation was positively correlated (R 2 = 0.750) with an increase in excitation pressure irrespective of whether high light, low temperature, or continuous illumination was used to induce increased excitation pressure. Similar trends were observed with the variegated mutants spotty, var1, and var2. Measurements of greening of etiolated wild-type and immutans cotyledons indicated that the absence of IMMUTANS increased excitation pressure twofold during the first 6 to 12 h of greening, which led to impaired biogenesis of thylakoid membranes. In contrast with IMMUTANS, the expression of its mitochondrial analog, AOX1a, was transiently upregulated in the wild type but permanently upregulated in immutans, indicating that the effects of excitation pressure during greening were also detectable in mitochondria. We conclude that mutations involving components of the photosynthetic electron transport chain, such as those present in immutans, spotty, var1, and var2, predispose Arabidopsis chloroplasts to photooxidation under high excitation pressure, resulting in the variegated phenotype.

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“…Recent studies confirm the important role of plastid retrograde signaling in plant acclimation to a variety of environmental stresses, as proposed in earlier reviews. 10,13 One recent example is the detailed analysis of the role of the metalloprotease AMOS1/EGY1 in plastid retrograde signaling under high-ammonium stress.…”

Section: Possible Plastid Retrograde Signaling Pathways In Ammonium Smentioning

confidence: 99%

“…In particular, the regulation of plastid retrograde signaling in the expression of photosynthesis-associated nuclear genes and those related to chloroplast development has been extensively studied. [2][3][4][5][6][7][8][9][10][11][12][13][14][15][16] More recently, several plastid retrograde signaling pathways have been identified to regulate the expression of stress-related nuclear genes during several stresses such as high light, drought, wounding, heat, and excess ammonium. [17][18][19][20][21][22][23][24][25][26][27][28][29][30][31] Based on the new stress-responsive plastid retrograde signaling pathways just reported in 2012 alone, this review will focus on properties of currently proposed molecular components in the plastid retrograde signaling network under stress.…”

Section: Introductionmentioning

confidence: 99%

Molecular components of stress-responsive plastid retrograde signaling networks and their involvement in ammonium stress

Kronzucker

Shi

2013

Plant Signaling & Behavior

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Retrograde signaling and plant stress: plastid signals initiate cellular stress responses

Cited by 148 publications

References 42 publications

Heat Shock Protein Cognate 70-4 and an E3 Ubiquitin Ligase, CHIP, Mediate Plastid-Destined Precursor Degradation through the Ubiquitin-26S Proteasome System inArabidopsis

Heat Shock Protein Cognate 70-4 and an E3 Ubiquitin Ligase, CHIP, Mediate Plastid-Destined Precursor Degradation through the Ubiquitin-26S Proteasome System inArabidopsis

Photosynthetic Redox Imbalance Governs Leaf Sectoring in theArabidopsis thalianaVariegation Mutantsimmutans,spotty,var1, andvar2

Molecular components of stress-responsive plastid retrograde signaling networks and their involvement in ammonium stress

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