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Manifold pathways of protein transport to the vacuole. (1) Direct uptake across the tonoplast. (2) Microautophagy. (3) Endocytosis via plasmalemmasomes. (4) Endocytosis via clathrin coated vesicles. (5) The secretory pathway. (6a) Macroautophagy (degradative). (6b) Macroautophagy (biosynthetic). (6c) Macroautophagy (storage). AL=autophago/lysosome; C=cytosol; CCV=clathrin coated vesicle; ER=endoplasmic reticulum; Gapp=Golgi apparatus; PLS=Plasmalemmasome; PM=Plasma membrane; V=vacuole.
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For many plant researchers protein transport to the vacuole is primarily a question of the mechanisms underlying the recognition
of vacuolar proteins and their segregation in the Golgi apparatus from other products of the secretory pathway. Autophagy
is an alternative process by which proteins can enter the vacuole. Examples of apparent selective a...
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... to know whether or not such proteins cytoplasm and/or organelles, and macroautophagy, which involves the de novo formation of an autophagosome are also ubiquinated. Obviously it would be useful to see whether starvation/E-64 induced autolysosomes in plants which then sequesters organelles, e.g. mitochondria and peroxisomes, and cytoplasm (Fig. 1). The majority are also enriched in ubiquitinated proteins, but the ques- tion remains as to why the central vacuole does not of the evidence available suggests that autophagosomes originate from ER membranes and then mature into respond to such stress conditions by performing micro- autophagy. Conversely: are the acid hydrolases of the ...
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... Multilamellar bodies and double membrane-bound autophagosomes have been associated with PCD processes in several species [12,13,15,20,35,36]. In the present study, the multivesicular body in the cytoplasm seemed to fuse with the plasma membrane, releasing vesicles into the buckling cell wall, which was also observed in PCD during floral nectary senescence in I. purpurea [16], aerenchyma formation in Typha angustifolia leaves [37], and rhytidome and interxylary cork formation of Astragalus membranaceus [38] and other plant systems [39]. ...
Plant glandular trichomes have received much attention due to their commercial and biological value. Recent studies have focused on the development of various glands in plants, suggesting that programmed cell death (PCD) may play an important role during the development of plant secretory structures. However, the development processes and cytological characteristics in different types of plant secretory structures differed significantly. This study aims to provide new data on the developmental PCD of the capitate glandular hairs in Dictamnus dasycarpus. Light, scanning, immunofluorescence labeling, and transmission electron microscopy were used to determine the different developmental processes of the capitate glandular hairs from a cytological perspective. Morphologically, the capitate glandular hair originates from one initial epidermal cell and differentiates into a multicellular trichome characterized by two basal cells, two lines of stalk cells, and a multicellular head. It is also histochemically detected by essential oils. TUNEL-positive reactions identified nuclei with diffused fluorescence or an irregular figure by DAPI, and Evans blue staining showed that the head and stalk cells lost their viability. Ultrastructural evidence revealed the developmental process by two possible modes of PCD. Non-autolytic PCD was characterized by buckling cell walls and degenerated nuclei, mitochondria, plastids, multivesicular body (MVB), and end-expanded endoplasmic reticulum in the condensed cytoplasm, which were mainly observed in the head cells. The MVB was detected in the degraded vacuole, a degraded nucleus with condensed chromatin and diffused membrane, and eventual loss of the vacuole membrane integrity exhibited typical evidence of vacuole-mediated autolytic PCD in the stalk cells. Furthermore, protoplasm degeneration coupled with dark oil droplets and numerous micro-dark osmiophilic substances was observed during late stages. The secretion mode of essential oils is also described in this paper.
... In the central cells of the pigment glands, epithelial cells, and sheath cells, the cytoplasm was surrounded by irregular membranous structures. From the perspective of morphological structure, this membranous structure was similar to autolysates in the PCD process of animal and plant cells [42][43][44]. Studies have shown that this membranous autolysate contains lytic enzymes, which can degrade the contents of cells including various organelles [45]. ...
Gossypium hirsutum is an important source of natural textile fibers. Gossypol, which is a sesquiterpenoid compound mainly existing in the cotton pigment glands, can facilitate resistance to the stress from diseases and pests. The level of gossypol in the cotton is positively correlated to the quantity of pigment glands. However, the underlying regulatory mechanisms of gossypol synthesis and gland morphogenesis are still poorly understood, especially from a transcriptional perspective. The transcripts of young leaves and ovules at 30 DPA of the glanded plants and glandless plants were studied by RNA-Seq and 865 million clean reads were obtained. A total of 34,426 differentially expressed genes (DEGs) were identified through comparative transcriptome analysis. Genes related to gossypol synthesis or gland morphogenesis displayed significant differential expression between the two cultivars. Functional annotation revealed that the candidate genes related to catalytic activity, the biosynthesis of secondary metabolites, and biomolecular decomposition processes. Our work herein unveiled several potential candidate genes related to gossypol synthesis or gland morphogenesis and may provide useful clues for a breeding program of cotton cultivars with low cottonseed gossypol contents.
... Autophagy is the main process for organelle degradation in most eukaryotes and hence plays a major role in cell homeostasis Michaeli et al., 2016). In addition, autophagy-related mechanisms appear also to be involved in a number of trafficking events, such as the direct ER-vacuole trafficking (Robinson et al., 1998;Herman and Larkins, 1999;Michaeli et al., 2014). Indeed, PBs have been reported to become surrounded by an autophagic membrane in the cytosol after their release from the ER (Herman and Larkins, 1999). ...
Due to the numerous roles plant vacuoles play in cell homeostasis, detoxification, and protein storage, the trafficking pathways to this organelle have been extensively studied. Recent evidence, however, suggests that our vision of transport to the vacuole is not as simple as previously imagined. Alternative routes have been identified and are being characterized. Intricate interconnections between routes seem to occur in various cases, complicating the interpretation of data. In this review, we aim to summarize the published evidence and link the emerging data with previous findings. We discuss the current state of information on alternative and classical trafficking routes to the plant vacuole.
... Interestingly, previous studies have investigated intermediate secretory structures, termed trichome cavities, which are characterized by a combination of lysigenous secretory cavities, capitate glandular hairs, and non-glandular hairs [6]. A series of degeneration characters were detected during the formation of trichome cavities in D. dasycarpus, suggesting a typical PCD phenomenon coupled with patterns of autophagy and autolysis [6,12,15,20]. For the homologous structures, the formation of secretory cavities in D. dasycarpus may also be PCD. ...
... The occurrence of multivesicular bodies in the secretory cells of the secretory cavities in D. dasycarpus has been considered typical evidence of autophagy in plant PCD [20,43,44], and a similar phenomenon has also been reported in the lysigenous formation of trichome cavities in D. dasycarpus [6] and in the schizolysigenous formation of secretory cavities in C. sinensis [10]. The formation of secretory cavities and trichome cavities in C. sinensis [11] and D. dasycarpus [6] is now considered a PCD process. ...
The formation of secretory cavities in Rutaceae has been the subject of great interest. In this study, cytological events that are involved in the lysigenous formation of the secretory cavities in the leaves of Dictamnus dasycarpus are characterized by an interesting pattern of programmed cell death (PCD). During the developmental process, clusters of cells from a single protoepidermal cell embark on different trajectories and undergo different cell death fates: the cell walls of the secretory cells have characteristics of thinning or complete breakdown, while the sheath cells present a predominantly thick-walled feature. A DAPI assay shows deformed nuclei that are further confirmed to be TUNEL-positive. Gel electrophoresis indicates that DNA cleavage is random and does not result in ladder-like DNA fragmentation. Ultrastructurally, several remarkable features of PCD have been determined, such as misshapen nuclei with condensed chromatin and a significantly diffused membrane, degenerated mitochondria and plastids with disturbed membrane systems, multivesicular bodies, plastolysomes, vacuole disruption and lysis of the center secretory cell. Cytological evidence and Nile red stains exhibit abundant essential oils accumulated in degenerated outer secretory cells after the dissolution of the center secretory cell. In addition, explanations of taxonomic importance and the relationship between PCD and oil droplet accumulation in the secretory cavities are also discussed.
... Macroautophagy, the major type of autophagy and hereafter referred to as 'autophagy', starts with the formation of spherical double membrane structures, termed autophagosomes, which enclose damaged proteins and organelles together with cytoplasm (Levine and Klionsky, 2004;Thompson and Vierstra, 2005;Bassham et al., 2006;Nakatogawa et al., 2009). Autophagosomes converge with endocytic vesicles, likely at prevacuolar compartments/multivesicular bodies (PVC/MVB), while moving toward lytic compartments, either lysosomes or vacuoles (Robinson et al., 1998). The outer membrane of autophagosomes fuses with membranes of lysosomes/ vacuoles, thereby delivering single-membrane structures, the autophagic bodies, into lysosomal or vacuolar lumens for degradation (Levine and Klionsky, 2004;Nakatogawa et al., 2009). ...
... PI3P is known to be involved in autophagic regulation by recruitment of ATG proteins to membranes and delivery of vacuolar hydrolases for autophagic degradation (Levine and Klionsky, 2004), and was proposed to regulate the convergence of autophagosomes and PVC/MVB in animals (Robinson et al., 1998). The presence of conserved PIbinding domains in plant ATGs (Thompson and Vierstra, 2005) suggested that PI3P may similarly regulate their membrane association. ...
... Transport of PI3P into the vacuole as a component of the autophagosome was also induced by starvation conditions in yeast (Obara et al., 2008). Based on studies in yeast, it was proposed that autophagy, lytic and endocytic pathways converge at the level of prevacuolar compartments (PVC) or multivesicular bodies (MVB) (Robinson et al., 1998). It was shown previously that PI3P was transported via trans-Golgi network (TGN) to PVC and finally to the vacuole in plant cells (Kim et al., 2001). ...
Autophagy is a pathway in eukaryotes by which nutrient remobilization occurs through bulk protein and organelle turnover. Autophagy not only aides cells in coping with harsh environments but also plays a key role in many physiological processes that include pollen germination and tube growth. Most autophagic components are conserved among eukaryotes, but phylum-specific molecular components also exist. We show here that Arabidopsis thaliana PTEN, a protein and lipid dual phosphatase homologous to animal PTENs (phosphatase and tensin homologs deleted on chromosome 10), regulates autophagy in pollen tubes by disrupting the dynamics of phosphatidylinositol 3-phosphate (PI3P). The pollen-specific PTEN bound PI3P in vitro and was localized at PI3P-positive vesicles. Overexpression of PTEN caused accumulation of autophagic bodies and resulted in gametophytic male sterility. Such an overexpression effect was dependent upon its lipid phosphatase activity and was inhibited by exogenous PI3P or by expression of a class III phosphatidylinositol 3-kinase (PI3K) that produced PI3P. Overexpression of PTEN disrupted the dynamics of autophagosomes and a subpopulation of endosomes, as shown by altered localization patterns of respective fluorescent markers. Treatment with wortmannin, an inhibitor of class III PI3K, mimicked the effects by PTEN overexpression, which implied a critical role for PI3P dynamics in these processes. Despite sharing evolutionarily conserved catalytic domains, plant PTENs contain regulatory sequences that are distinct from those of animal PTENs, which might underlie their differing membrane association and thereby function. Our results show that PTEN regulates autophagy through phylum-specific molecular mechanisms.
... Senescence-induced autophagy has best been studied in senescent leaves and cotyledons, where carbon and nitrogen are efficiently remobilized ( Wada et al. 2009). Both microautophagy and macroautophagy have been reported in plants (Matile 1975; Van der Wilden et al. 1980; Herman et al. 1981; Aubert et al. 1996; Moriyasu and Ohsumi 1996; Robinson et al. 1998; Swanson et al. 1998; Toyooka et al. 2001). The studies demonstrated that autophagic protein recycling is not only needed in response to nutritional demand, abiotic stress, and senescence, but is also maintained at a basal level under normal growth conditions (Slavikova et al. 2005; Inoue et al. 2006; Xiong et al. 2007a). ...
Autophagy is an evolutionarily conserved intracellular process for the vacuolar degradation of cytoplasmic constituents. The central structures of this pathway are newly formed double-membrane vesicles (autophagosomes) that deliver excess or damaged cell components into the vacuole or lysosome for proteolytic degradation and monomer recycling. Cellular remodeling by autophagy allows organisms to survive extensive phases of nutrient starvation and exposure to abiotic and biotic stress. Autophagy was initially studied by electron microscopy in diverse organisms, followed by molecular and genetic analyses first in yeast and subsequently in mammals and plants. Experimental data demonstrate that the basic principles, mechanisms, and components characterized in yeast are conserved in mammals and plants to a large extent. However, distinct autophagy pathways appear to differ between kingdoms. Even though direct information remains scarce particularly for plants, the picture is emerging that the signal transduction cascades triggering autophagy and the mechanisms of organelle turnover evolved further in higher eukaryotes for optimization of nutrient recycling. Here, we summarize new research data on nitrogen starvation-induced signal transduction and organelle autophagy and integrate this knowledge into plant physiology.
... Electron-opaque vacuolar deposits in lichens are often attributed to the increased availability of N compounds (Holopainen & Ka$ renlampi, 1984 ;Balaguer et al., 1997), but they have also been found in lichens treated with acid rain and metals (Tarhanen, 1998). Vacuolar deposits might indicate the vacuolar sequestration of storage proteins (Robinson et al., 1998) and toxic substances (Gadd, 1993). Because pollutants can interfere with the uptake of essential elements, leading to nutrient stress, these vacuolar deposits could also be associated with starvationinduced autophagy in the cells (Robinson et al., 1998). ...
... Vacuolar deposits might indicate the vacuolar sequestration of storage proteins (Robinson et al., 1998) and toxic substances (Gadd, 1993). Because pollutants can interfere with the uptake of essential elements, leading to nutrient stress, these vacuolar deposits could also be associated with starvationinduced autophagy in the cells (Robinson et al., 1998). Autophagosomes have been recorded, for example, for yeast and suspension-cultured plant cells growing under nutrient-deficient conditions (Robinson et al., 1998). ...
... Because pollutants can interfere with the uptake of essential elements, leading to nutrient stress, these vacuolar deposits could also be associated with starvationinduced autophagy in the cells (Robinson et al., 1998). Autophagosomes have been recorded, for example, for yeast and suspension-cultured plant cells growing under nutrient-deficient conditions (Robinson et al., 1998). ...
The photobiont ultrastructure of the epiphytic lichens Bryoria fuscescens and Bryoria fremontii was studied along the pollution gradient from two Cu-Ni smelters in Nikel and Monchegorsk in northern Finland and north-western Russia. The relationship between ultrastructural characteristics of B. fuscescens and environmental factors (i.e. climate, atmospheric SO2 and bark element concentrations) was studied by using a principal component analysis (PCA) aiming to assess the air quality in a northern environment. Based on PCA, increased plasmolysis and mitochondrial changes in the Trebouxia photobiont were significantly correlated with elevated pollutant concentrations. Degenerated cells, showing altered chloroplasts and electron-translucent pyrenoglobuli, occurred in lichens growing 35–50 km from the Monchegorsk smelter. Cell wall and cytoplasmic lipid volumes, and size of pyrenoglobuli, positively correlated with the distance from the Monchegorsk smelter. Vacuoles and electron-opaque vacuolar deposits were significantly increased at the Finnish site in the vicinity of a pulp mill. Swelling of mitochondrial cristae and thylakoids showed little correlation with environmental factors, but indicated of initial stage of injuries and were observed at several slightly polluted sites in northern Finland and north-western Russia. The results suggest that the severe photobiont injuries of lichens are strongly associated with poor air quality.
... The yeast vacuole is often used as a model for plant vacuoles, but so far no similar mechanism has been observed in plant cells. Aside from the targeted transfer so far described, cytoplasmic material, including proteins, is taken up into the vacuole by autophagic processes (Robinson et al., 1998b; Herman and Schmidt, 2004; see also section below entitled 'Programmed cell death'). According to Marty's hypothesis about vacuole generation from the TGN (Marty, 1997Marty, , 1999), cytoplasmic material is trapped autophagically by the emerging vacuole and is afterwards degraded by lytic enzymes. ...
Plant cells cannot live without their vacuoles. The tissues and organs of a plant contain a wide variety of differentiated and specialized vacuoles -- even a single plant cell can possess two or more types of vacuoles. Vacuolar proteins are encoded by nuclear genes and synthesized in the cytoplasm. Their transport into the vacuolar compartment is under cytoplasmic control. Transcription seems to be a major control level for differential protein supply to the vacuoles. It is at this level that vacuole differentiation and functions are mainly integrated into cellular processes. Recycling amino acids generated by protein degradation is a major function of the vacuole. This is most evident when storage proteins are mobilized in storage tissues of generative or vegetative organs in order to nourish the embryo of germinating seeds or sprouting buds. When specific proteins are transferred to the vacuole for immediate degradation this compartment contributes to the adaptation of protein complexes in response to changes in developmental or environmental conditions. Vacuolar proteases are involved in protein degradation during reversible senescence and programmed cell death, which is also called irreversible senescence. Vacuoles contribute to defence against pathogens and herbivores by limited and unlimited proteolysis. Our present knowledge on functions and processes of vacuolar protein dynamics in plants is reviewed. Research perspectives are deduced.
... The outer membrane of the autophagosome then fuses to the vacuolar membrane, thus delivering the inner membrane structure, the autophagic body, into the vacuolar lumen for degradation. So far, in plants, both microautophagy and macroautophagy have been reported (Matile, 1975; Van Der Wilden et al., 1980; Herman et al., 1981; Aubert et al., 1996; Moriyasu and Ohsumi, 1996; Robinson et al., 1998; Swanson et al., 1998; Rojo et al., 2001; Toyooka et al., 2001). Although most studies of autophagy have been based on morphological observations, genetic screens in the yeast Saccaromyces cerevisiae have expanded the molecular dissection of autophagy. ...
Autophagy is an intracellular process for vacuolar degradation of cytoplasmic components. Thus far, plant autophagy has been studied primarily using morphological analyses. A recent genome-wide search revealed significant conservation among autophagy genes (ATGs) in yeast and plants. It has not been proved, however, that Arabidopsis thaliana ATG genes are required for plant autophagy. To evaluate this requirement, we examined the ubiquitination-like Atg8 lipidation system, whose component genes are all found in the Arabidopsis genome. In Arabidopsis, all nine ATG8 genes and two ATG4 genes were expressed ubiquitously and were induced further by nitrogen starvation. To establish a system monitoring autophagy in whole plants, we generated transgenic Arabidopsis expressing each green fluorescent protein-ATG8 fusion (GFP-ATG8). In wild-type plants, GFP-ATG8s were observed as ring shapes in the cytoplasm and were delivered to vacuolar lumens under nitrogen-starved conditions. By contrast, in a T-DNA insertion double mutant of the ATG4s (atg4a4b-1), autophagosomes were not observed, and the GFP-ATG8s were not delivered to the vacuole under nitrogen-starved conditions. In addition, we detected autophagic bodies in the vacuoles of wild-type roots but not in those of atg4a4b-1 in the presence of concanamycin A, a V-ATPase inhibitor. Biochemical analyses also provided evidence that autophagy in higher plants requires ATG proteins. The phenotypic analysis of atg4a4b-1 indicated that plant autophagy contributes to the development of a root system under conditions of nutrient limitation.
... It is unlikely that this labelling was artefactual since in similar control sections the mitochondrial enzyme IDH (Lancien et al. 2000) was not detected in this type of cellular component. The formation of similar multivesicular bodies has already been described in Cstarved (Aubert et al. 1996) or senescing plant tissues (Robinson et al. 1998), including petals (Matile and Winkenbach 1971) and anthers (Sangwan 1986), and shown to correspond to autophagic activity of the vacuole. These structures, which contain a high concentration of GDH, were detected mainly in the flower receptacle. ...
The subcellular localisation of glutamine synthetase (GS) and glutamate dehydrogenase (GDH) in grapevine (Vitis vinifera L.) leaves and flowers was investigated using immunogold-labelling experiments. In mature leaf tissue or fully developed flowers, GS was visualised both in the cytosol and in the chloroplasts, a high proportion of the protein being present in the phloem companion cells. GDH was preferentially located in the mitochondria of the phloem companion cells in both leaves and flowers. This observation suggests that, in conjunction with GS, GDH plays a major role in controlling the translocation of organic carbon and nitrogen metabolites in both vegetative and reproductive organs. Significant amounts of GDH protein were also visualised in multivesicular bodies within the flower receptacle. Although the function of such organelles is still unknown, its is possible that the presence of GDH in such cellular structures is important for the recycling of carbon and nitrogen molecules in senescing tissues in which the enzyme is generally induced.
