Clp protease complexes and their diversity in chloroplasts

Sokolenko, Anna; Lerbs-Mache, Silvia; Altschmied, Lothar; Herrmann, Reinhold G.

doi:10.1007/s004250050485

Cited by 65 publications

(47 citation statements)

References 44 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…ClpP2 was found in mitochondria by proteomic analyses as well (Millar et al, 2001;Peltier et al, 2004). Other ClpPs and ClpRs were found only in chloroplasts (Sokolenko et al, 1998;Nakabayashi et al, 1999;Peltier et al, 2001Peltier et al, , 2004Zheng et al, 2002). The pea homolog of FtsH3 was detected in mitochondria but not in chloroplasts (Kolodziejczak et al, 2002).…”

Section: Discussionmentioning

confidence: 95%

Expression in Multigene Families. Analysis of Chloroplast and Mitochondrial Proteases

Sinvany-Villalobo

Davydov²,

Ben-Ari³

et al. 2004

Plant Physiology

119

107

View full text Add to dashboard Cite

The proteolytic machinery of chloroplasts and mitochondria in Arabidopsis consists primarily of three families of ATPdependent proteases, Clp, Lon, and FtsH, and one family of ATP-independent proteases, DegP. However, the functional significance of the multiplicity of their genes is not clear. To test whether expression of specific isomers could be differently affected by growth conditions, we analyzed transcript abundance following short-term exposure to different environmental stimuli, using 70-mer oligonucleotide arrays. This analysis revealed variability in the response to high light and different temperatures within members of each family. Thirty out of the 41 tested genes were up-regulated in response to high light, including both chloroplast and mitochondrial isozymes, whereas only six and five genes responded to either high or low temperature, respectively. The extent of response was variable, ranging from 2-to 20-fold increase in the steady-state levels.Absolute transcript levels of the tested genes, compiled from one-channel arrays, were also variable. In general, transcripts encoding mitochondrial isozymes were accumulated to a lower level than chloroplastic ones. Within the FtsH family, transcript abundance of most genes correlated with the severity of mutant phenotypes in the relevant genes. This correlation was also evident at the protein level. Analysis of FtsH isozymes revealed that FtsH2 was the most abundant species, followed by FtsH5 and 8, with FtsH1 being accumulated to only 10% of FtsH2 level. These results suggest that, unlike previous expectations, the relative importance of different chloroplast protease isozymes, evidenced by mutant phenotypes at least in the FtsH family, is determined by their abundance, and not necessarily by different specific functions or specialized expression under certain conditions.The proteolytic machinery of chloroplasts and mitochondria is essential for controlling the quality and turnover of these organelles' proteins and, thus, is important for their proper function. In Arabidopsis, the proteolytic machinery of chloroplasts consists primarily of three families of ATP-dependent proteases, Clp, Lon, and FtsH, and one family of ATPindependent proteases, DegP (for review, see Adam and Clarke, 2002;Sokolenko et al., 2002). Homologous enzymes are found also in mitochondria (Sarria et al., 1998;Adam et al., 2001;Halperin et al., 2001b;Kolodziejczak et al., 2002). All these families have well-characterized homologs in Escherichia coli (for review, see Clarke, 1999;Adam, 2000). Clp is a Ser protease that separates its two essential functions in two different polypeptides: a small subunit, ClpP, containing the proteolytic active site, and a larger regulatory ATPase subunit, either ClpA or ClpX (for review, see Gottesman, 1996). Lon protease is an ATPdependent Ser protease in which the catalytic and ATPase domains reside in a single polypeptide (for review, see Gottesman, 1996). FtsH is the only essential ATP-dependent protease in E. coli. It is a membranebound metall...

show abstract

Section: Discussionmentioning

confidence: 95%

Expression in Multigene Families. Analysis of Chloroplast and Mitochondrial Proteases

Sinvany-Villalobo

Davydov²,

Ben-Ari³

et al. 2004

Plant Physiology

119

107

View full text Add to dashboard Cite

show abstract

“…Because Hsp93 is also proposed to function as a regulatory subunit for the ClpP protease complex in the stroma (Halperin and Adam, 1996;Desimone et al, 1997;Sokolenko et al, 1998;Halperin et al, 2001), an in organello proteolytic assay (Sjö gren et al, 2006) was conducted to investigate the degradation of the chloroplast GS2. GS2 has been shown to be a potential substrate for ClpP, because its amount increased in a mutant that only has 10% of the wild-type level of intact ClpP core complex (Stanne et al, 2009).…”

Section: Mutations In Athsp93v Do Not Affect the Degradation Of A Potmentioning

confidence: 99%

“…Double knockout of both genes causes lethality, indicating that Hsp93 is essential (Kovacheva et al, 2007). In addition, Hsp93 has been proposed to act as a regulatory subunit of the ClpP protease in chloroplasts (Shanklin et al, 1995;Desimone et al, 1997;Sokolenko et al, 1998;Halperin et al, 2001). Interestingly, although Hsp93 was not detected in the ClpP core complex isolated from chloroplasts, the land plant chloroplast ClpP complex contains two additional peripheral subunits, ClpT1 and ClpT2 (previously named ClpS1 and ClpS2), that have high sequence similarity to the N-terminal portion of Hsp93 (Peltier et al, 2004).…”

mentioning

confidence: 99%

The Amino-Terminal Domain of Chloroplast Hsp93 Is Important for Its Membrane Association and Functions in Vivo

Chu

2012

Plant Physiology

View full text Add to dashboard Cite

Chloroplast 93-kD heat shock protein (Hsp93/ClpC), an Hsp100 family member, is suggested to have various functions in chloroplasts, including serving as the regulatory chaperone for the ClpP protease in the stroma and acting as a motor component of the protein translocon at the envelope. Indeed, although Hsp93 is a soluble stromal protein, a portion of it is associated with the inner envelope membrane. The mechanism and functional significance of this Hsp93 membrane association have not been determined. Here, we mapped the region important for Hsp93 membrane association by creating various deletion constructs and found that only the construct with the amino-terminal domain deleted, Hsp93-DN, had reduced membrane association. When transformed into Arabidopsis (Arabidopsis thaliana), most atHsp93V-DN proteins did not associate with membranes and atHsp93V-DN failed to complement the pale-green and protein import-defective phenotypes of an hsp93V knockout mutant. The residual atHsp93V-DN at the membranes had further reduced association with the central protein translocon component Tic110. However, the degradation of chloroplast glutamine synthetase, a potential substrate for the ClpP protease, was not affected in the hsp93V mutant or in the atHSP93V-DN transgenic plants. Hsp93-DN also had the same ATPase activity as that of full-length Hsp93. These data suggest that the association of Hsp93 with the inner envelope membrane through its amino-terminal domain is important for the functions of Hsp93 in vivo.Chloroplasts are structurally complex organelles that perform diverse functions (Leister, 2003;Block et al., 2007). They are composed of three membranes, the outer and inner envelope membranes and the thylakoid membranes, and these membranes enclose three aqueous compartments, the intermembrane space, stroma, and thylakoid lumen. Although chloroplasts have their own genome, most chloroplast proteins are encoded by the nuclear genome and are translated in the cytosol as a precursor protein with an N-terminal extension called the transit peptide. Transit peptides direct the import of proteins into chloroplasts through the translocon complex located in the chloroplast envelope. Translocon components of the outer membrane are called Toc (for translocon at the outer envelope membrane of chloroplasts) proteins and those in the inner envelope membrane are called Tic (for translocon at the inner envelope membrane of chloroplasts) proteins. Three Toc components, Toc159, Toc34, and Toc75, form the Toc core complex. Toc159 and Toc34 function as receptors that recognize the precursors targeting to chloroplasts. Toc75 forms a protein-conducting channel across the outer membrane. Three proteins, Tic20, Tic21, and Tic110, have been suggested to function as the channel for precursor translocation across the inner membrane. Tic110 has also been shown to function as the stromal-side receptor for transit peptides and as a scaffold for assembling other stromal translocon components. Tic40 is a cochaperone that coordinates the actions of...

show abstract

“…(Hortensteiner, 2006). Proteases of the Clp, FtsH and DegP families are also expressed in chloroplasts and representative genes for these proteases are up-regulated in senescing leaves (Sokolenko et al, 1998;Nakabayashi et al, 1999;Itzhaki et al, 1998;Haussühl et al, 2001). Despite this observation, chloroplastic proteases are unlikely to account for the degradation of most photosynthetic proteins (eg, Rubisco) during senescence.…”

Section: Progress Of Senescence In Plantsmentioning

confidence: 99%