A Cysteine Endopeptidase Isolated from Castor Bean Endosperm Microbodies Processes the Glyoxysomal Malate Dehydrogenase Precursor Protein

Gietl, Christine; Wimmer, Bernhard; Adamec, Jiřı́; Kalousek, František

doi:10.1104/pp.113.3.863

Cited by 33 publications

(25 citation statements)

References 39 publications

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“…The products of amplified PEX10/pex10 were purified, reamplified, digested with MbiI, and analyzed on a 3% agarose gel. (28). Defects in ␤-oxidation or photorespiration were assayed by growth on MS plates with or without 1% sucrose and measurement of root length (mean value of 20 plants) at days 3, 4, and 6.…”

Section: Methodsmentioning

confidence: 99%

Requirement of the C ₃ HC ₄ zinc RING finger of the Arabidopsis PEX10 for photorespiration and leaf peroxisome contact with chloroplasts

Schümann

Prestele

O’Geen

et al. 2007

Proc. Natl. Acad. Sci. U.S.A.

101

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Plant peroxisomes perform multiple vital metabolic processes including lipid mobilization in oil-storing seeds, photorespiration, and hormone biosynthesis. Peroxisome biogenesis requires the function of peroxin (PEX) proteins, including PEX10, a C3HC4 Zn RING finger peroxisomal membrane protein. Loss of function of PEX10 causes embryo lethality at the heart stage. We investigated the function of PEX10 with conditional sublethal mutants. Four T-DNA insertion lines expressing pex10 with a dysfunctional RING finger were created in an Arabidopsis WT background (⌬Zn plants). They could be normalized by growth in an atmosphere of high CO2 partial pressure, indicating a defect in photorespiration. ␤-Oxidation in mutant glyoxysomes was not affected. However, an abnormal accumulation of the photorespiratory metabolite glyoxylate, a lowered content of carotenoids and chlorophyll a and b, and a decreased quantum yield of photosystem II were detected under normal atmosphere, suggesting impaired leaf peroxisomes. Light and transmission electron microscopy demonstrated leaf peroxisomes of the ⌬Zn plants to be more numerous, multilobed, clustered, and not appressed to the chloroplast envelope as in WT. We suggest that inactivation of the RING finger domain in PEX10 has eliminated protein interaction required for attachment of peroxisomes to chloroplasts and movement of metabolites between peroxisomes and chloroplasts.␤-oxidation ͉ biogenesis ͉ glyoxysome E ukaryotic peroxisomes perform multiple metabolic processes, including fatty acid ␤-oxidation and H 2 O 2 inactivation by catalase (1). In plants, leaf peroxisomes interact with chloroplasts and mitochondria in photorespiration, a metabolic pathway in which two molecules of glycolate are converted in a series of enzymatic reactions through glyoxylate, glycine, serine, and hydroxypyruvate into CO 2 and phosphoglycerate (2-4). The advantage of the photorespiratory cycle is twofold. When CO 2 in the plant canopy becomes limited in supply (which is frequent at midday), ribulose-bisphosphate carboxylase/oxygenase functions as an oxygenase and protects the photosynthetic machinery from photodamage. It does so by using energy for respiration, producing CO 2 , and regenerating the substrate to be used in CO 2 fixation. Mutants lacking enzymes of the photorespiratory cycle are incapable of surviving in ambient air but are able to grow normally in atmosphere enriched in CO 2 because ribulosebisphosphate oxygenase is suppressed (2). Plant peroxisomes are necessary for jasmonic acid biosynthesis (5) and are implicated in conversion of indole-3-butyric acid (IBA) into indole-3-acetic acid (IAA) (6-8). Specialized peroxisomes called glyoxysomes contain glyoxylate cycle enzymes for lipid mobilization in germinating oil seedlings and senescing leaves (1).The peroxins (PEX proteins) are a set of cytosolic and membrane proteins involved in peroxisome biogenesis. Mutations of PEX genes leading to impaired peroxisome biogenesis result in severe metabolic and developmental disturbances in yeasts,...

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Section: Methodsmentioning

confidence: 99%

Requirement of the C ₃ HC ₄ zinc RING finger of the Arabidopsis PEX10 for photorespiration and leaf peroxisome contact with chloroplasts

Schümann

Prestele

O’Geen

et al. 2007

Proc. Natl. Acad. Sci. U.S.A.

101

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“…Ricinosomes were isolated from 5-day-old germinating castor bean endosperm (11) because, at this stage of development, the yield is highest and protein bodies are almost completely degraded (5). Ricinosomes isolated on a discontinuous sucrose gradient (10% to 57% sucrose) copurify with glyoxysomes at the interface between the 50 and 57% sucrose steps (cf.…”

Section: Methodsmentioning

confidence: 99%

“…Ricinosomes were first described and ultrastructurally characterized in the endosperm of R. communis (8,9), whereas KV were described as cytoplasmic ''foci'' in Vigna radiata (10). The mature CysEP was originally purified from germinating castor bean endosperm (11). Sequencing of cDNA clones from the endosperm of germinating seedlings and from developing seeds established the presence of a presequence for cotranslational targeting into the lumen of the endoplasmic reticulum (ER), an N-terminal propeptide and a C-terminal KDEL motif.…”

mentioning

confidence: 99%

The ricinosomes of senescing plant tissue bud from the endoplasmic reticulum

Schmid

Simpson

Sarioglu

et al. 2001

Proc. Natl. Acad. Sci. U.S.A.

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The ricinosome (synonym, precursor protease vesicle) is a novel organelle, found so far exclusively in plant cells. Electron microscopic studies suggest that it buds off from the endoplasmic reticulum in senescing tissues. Biochemical support for this unusual origin now comes from the composition of the purified organelle, which contains large amounts of a 45-kDa cysteine endoprotease precursor with a C-terminal KDEL motif and the endoplasmic reticulum lumen residents BiP (binding protein) and protein disulfide isomerase. Western blot analysis, peptide sequencing, and mass spectrometry demonstrate retention of KDEL in the protease proform. Acidification of isolated ricinosomes causes castor bean cysteine endopeptidase activation, with cleavage of the N-terminal propeptide and the C-terminal KDEL motif. We propose that ricinosomes accumulate during senescence by programmed cell death and are activated by release of protons from acidic vacuoles.Ricinus communis ͉ papain-type KDEL peptidase P rogrammed cell death (PCD) in higher plants and animals fulfills multiple functions in the differentiation or turnover of tissues and is triggered by pathogens at and around the site of infection as a mechanism to prevent proliferation of the disease (1, 2). Examples for elimination by PCD of organs that serve temporary functions are tadpole tails during metamorphosis and the endosperm of the castor bean during germination. In plants, the PCD of whole organs such as leaves, flowers, and fruits is designated as senescence (3).Biochemical pathways accompanying PCD or apoptosis in mammals have been elucidated in detail (reviewed in ref. 4). Plant cells undergoing senescence by PCD express papain-type cysteine endoproteases with a C-terminal KDEL sequence (5). They attract attention because they are present in the senescing endosperm cells of castor bean (Ricinus communis) as relatively inactive 45-kDa proenzymes until the final stages of PCD, at which time they are processed into the 35-kDa mature form with a 50-100 times higher activity (6).The cysteine endopeptidase from senescing castor bean endosperm (CysEP) is homologous to papain-type KDEL cysteine endopeptidases from senescing flower petals of daylily, the maturing French bean pods, and the cotyledons of germinating mung bean and vetch (6). In castor bean, daylily, and mung bean, the KDEL-tailed propeptidase is stored in a special organelle, called ricinosome (5, 6) or KDEL-tailed cysteine proteinaseaccumulating vesicles (KV) (7). Ricinosomes were first described and ultrastructurally characterized in the endosperm of R. communis (8, 9), whereas KV were described as cytoplasmic ''foci'' in Vigna radiata (10). The mature CysEP was originally purified from germinating castor bean endosperm (11). Sequencing of cDNA clones from the endosperm of germinating seedlings and from developing seeds established the presence of a presequence for cotranslational targeting into the lumen of the endoplasmic reticulum (ER), an N-terminal propeptide and a C-terminal KDEL motif. Immunogold l...

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“…First documented by Mollenhauer and Totten (1970), the ricinosomes and the enzymes within these unique organelles have been implicated in PCD of the cells of the postgerminative castor (Ricinus communis) seed endosperm and senescent day lily (Hemerocallis spp.) petal (Gietl et al, 1997;Schmid et al, 1999) and in PCD of the nucellus during castor seed development (Greenwood et al, 2005). More recently, ricinosomes, but not the enzymes within, have been implicated in PCD of the endosperm of postgerminative tomato (Solanum lycopersicum) seed (DeBono and .…”

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confidence: 99%

Ricinosomes Predict Programmed Cell Death Leading to Anther Dehiscence in Tomato

2008

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Successful development and dehiscence of the anther and release of pollen are dependent upon the programmed cell death (PCD) of the tapetum and other sporophytic tissues. Ultrastructural examination of the developing and dehiscing anther of tomato (Solanum lycopersicum) revealed that cells of the interlocular septum, the connective tissue, the middle layer/ endothecium, and the epidermal cells surrounding the stomium all exhibit features consistent with progression through PCD. Ricinosomes, a subset of precursor protease vesicles that are unique to some incidents of plant PCD, were also present in all of these cell types. These novel organelles are known to harbor KDEL-tailed cysteine proteinases that act in the final stages of corpse processing following cell death. Indeed, a tomato KDEL-tailed cysteine proteinase, SlCysEP, was identified and its gene was cloned, sequenced, and characterized. SlCysEP transcript and protein were restricted to the anthers of the senescing tomato flower. Present in the interlocular septum and in the epidermal cells surrounding the stomium relatively early in development, SlCysEP accumulates later in the sporophytic tissues surrounding the locules as dehiscence ensues. At the ultrastuctural level, immunogold labeling localized SlCysEP to the ricinosomes within the cells of these tissues, but not in the tapetum. It is suggested that the accumulation of SlCysEP and the appearance of ricinosomes act as very early predictors of cell death in the tomato anther.

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A Cysteine Endopeptidase Isolated from Castor Bean Endosperm Microbodies Processes the Glyoxysomal Malate Dehydrogenase Precursor Protein

Cited by 33 publications

References 39 publications

Requirement of the C ₃ HC ₄ zinc RING finger of the Arabidopsis PEX10 for photorespiration and leaf peroxisome contact with chloroplasts

Requirement of the C ₃ HC ₄ zinc RING finger of the Arabidopsis PEX10 for photorespiration and leaf peroxisome contact with chloroplasts

The ricinosomes of senescing plant tissue bud from the endoplasmic reticulum

Ricinosomes Predict Programmed Cell Death Leading to Anther Dehiscence in Tomato

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A Cysteine Endopeptidase Isolated from Castor Bean Endosperm Microbodies Processes the Glyoxysomal Malate Dehydrogenase Precursor Protein

Cited by 33 publications

References 39 publications

Requirement of the C 3 HC 4 zinc RING finger of the Arabidopsis PEX10 for photorespiration and leaf peroxisome contact with chloroplasts

Requirement of the C 3 HC 4 zinc RING finger of the Arabidopsis PEX10 for photorespiration and leaf peroxisome contact with chloroplasts

The ricinosomes of senescing plant tissue bud from the endoplasmic reticulum

Ricinosomes Predict Programmed Cell Death Leading to Anther Dehiscence in Tomato

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Requirement of the C ₃ HC ₄ zinc RING finger of the Arabidopsis PEX10 for photorespiration and leaf peroxisome contact with chloroplasts

Requirement of the C ₃ HC ₄ zinc RING finger of the Arabidopsis PEX10 for photorespiration and leaf peroxisome contact with chloroplasts