Arabidopsis senescence-associated protein DMP1 is involved in membrane remodeling of the ER and tonoplast
© Kasaras et al; licensee BioMed Central Ltd. 2011
Received: 6 December 2011
Accepted: 24 April 2012
Published: 24 April 2012
Arabidopsis DMP1 was discovered in a genome-wide screen for senescence-associated membrane proteins. DMP1 is a member of a novel plant-specific membrane protein family of unknown function. In rosette leaves DMP1 expression increases from very low background level several 100fold during senescence progression.
Expression of AtDMP1 fused to eGFP in Nicotiana benthamiana triggers a complex process of succeeding membrane remodeling events affecting the structure of the endoplasmic reticulum (ER) and the vacuole. Induction of spherical structures (“bulbs”), changes in the architecture of the ER from tubular to cisternal elements, expansion of smooth ER, formation of crystalloid ER, and emergence of vacuolar membrane sheets and foamy membrane structures inside the vacuole are proceeding in this order. In some cells it can be observed that the process culminates in cell death after breakdown of the entire ER network and the vacuole. The integrity of the plasma membrane, nucleus and Golgi vesicles are retained until this stage. In Arabidopsis thaliana plants expressing AtDMP1-eGFP by the 35S promoter massive ER and vacuole vesiculation is observed during the latest steps of leaf senescence, whereas earlier in development ER and vacuole morphology are not perturbed. Expression by the native DMP1 promoter visualizes formation of aggregates termed “boluses” in the ER membranes and vesiculation of the entire ER network, which precedes disintegration of the central vacuole during the latest stage of senescence in siliques, rosette and cauline leaves and in darkened rosette leaves. In roots tips, DMP1 is strongly expressed in the cortex undergoing vacuole biogenesis.
Our data suggest that DMP1 is directly or indirectly involved in membrane fission during breakdown of the ER and the tonoplast during leaf senescence and in membrane fusion during vacuole biogenesis in roots. We propose that these properties of DMP1, exacerbated by transient overexpression, may cause or contribute to the dramatic membrane remodeling events which lead to cell death in infiltrated tobacco leaves.
DMP1 (DUF679 Membrane Protein 1) is a short membrane protein of 207 amino acids with four transmembrane spans and belongs to a small, strictly plant-specific protein family comprising ten members in Arabidopsis thaliana. DMP1 is transcriptionally up-regulated during developmental senescence (NS) in siliques, rosette and cauline leaves, during dark induced senescence in attached (DIS) and detached leaves (DET) and is expressed in the phloem bundles of roots and the cortex of root tips . In all three senescence programs, DMP1 expression increases from the onset until the very late stages of senescence. This suggests conserved functions during developmental and induced senescence as well as an involvement during the entire senescence program. DMP1 is also expressed in the dehiscence and abscission zones of siliques , which indicates a role in programmed cell death (PCD).
In metazoans, based on cell morphology apoptosis, autophagy and necrosis are distinguished as the three main PCD forms. In plants “autolytic” and “non-autolytic” PCD are differentiated . Non-autolytic PCD is marked by the absence of rapid cytoplasm clearance , as is observed e.g. in hypersensitive response and endosperm degeneration. Autolytic PCD is characterized by rupture of the tonoplast and subsequent rapid cytoplasm clearance and occurs e.g. in tracheary element differentiation and senescence, although the relationship between senescence and PCD is still controversial [4–6]. In the present study, we use the term PCD for the terminal stage of leaf senescence. The earliest detectable alterations during leaf senescence are changes in the ultrastructure of chloroplasts. In the course of senescence all organelles are eventually degraded. In Iris and carnation petal senescence, ER and attached ribosomes, Golgi bodies and mitochondria have been reported to be degraded during senescence before vacuolar collapse . Ultrastructural, biochemical and gene expression data indicate that large-scale autophagy is involved in these degradation processes . However, the fate of organelles has been almost exclusively investigated by electron microscopy using fixed cells. Investigations of ultrastructural changes of organelles undergoing senescence using fluorescence tags in living cells are scarce.
Here we present an extensive characterization of the complex cellular processes induced by the senescence-associated DMP1 protein fused to eGFP in Nicotiana benthamiana and Arabidopsis thaliana by confocal fluorescence and electron microscopy. In tobacco, DMP1-eGFP overexpression triggers membrane remodeling, expansion, fusion and fission events at the tonoplast and the ER. We classified the successive remodeling events into five stages and showed that they ultimately can lead to cell death by extensive fragmentation of the ER and the vacuole. We note the formation of an additional network that we propose to be proliferating smooth ER. To our knowledge, this is the first observation of a clear separation of rough and smooth ER of the cortical ER in tobacco using fluorescent tags. Thus, overexpression of DMP1-eGFP might induce a differentiation of the cortical ER. In Arabidopsis we investigated DMP1-eGFP fluorescence patterns in tissues undergoing NS or DIS as well as the response to whole plant darkening, a treatment that induces a range of physiological effects which are not related to NS and DIS . We found that in all tissues and senescence types DMP1-eGFP illuminates vesiculation events of the ER and the tonoplast and the formation of aggregates (“boluses”) within the ER. The formation of boluses, which suggest altered protein flow and the vesiculation of the entire ER network, has not been reported during senescence yet. We suggest that rupture of the tonoplast, a hallmark of autolytic PCD in the terminal senescence stage, may be accompanied or preceded by fragmentation of the vacuole. The effects of DMP1-eGFP expression in tobacco and Arabidopsis suggest that DMP1 regulates membrane folding and is involved in tonoplast and ER membrane fusion and fission reactions.
Expression of DMP1-eGFP in Nicotiana benthamiana epidermis cells induces membrane remodeling
To characterize the membrane structures labeled by DMP1-eGFP we subsequently performed colocalization experiments with various membrane markers.
Stage 1: The tonoplast located DMP1-eGFP induces the formation of bulbs
Stage 2: Reorganization of the ER - transition from tubular elements to cisternae
Stage 2 is characterized by the appearance of bulky cisternae in the cytoplasm that strongly resemble cortical ER observed under certain conditions (see Discussion), while the bulbs and tonoplast labeling from stage 1 are still retained (Figure 1b). The ER localization of DMP1-eGFP was verified by co-expression with RFP-p24 (Figure 3i,j,k). We also occasionally observed RFP-p24 signals in bulbs (Figure 3j,k, arrows). This might either indicate mislocalization of the ER marker due to overexpression or some dysfunction of the ER during stage 2.
Stage 3: De novo formation of a cortical ER-derived network inside the cytoplasm and vacuolar sheets inside the vacuole
As mentioned above, vacuolar sheets crossing the lumen of the vacuole and first “foamy” membranes appear in stage 3 and accumulate gradually (Figure 2c). The density of vacuolar sheets correlates with a progressive loss of the DMP1-eGFP labeled network. Moreover, the tubules were occasionally found tightly associated with these vacuolar sheets (Additional file 1: Figure S2). These observations suggest a connection between these two structures. Golgi vesicles appeared to be unaffected during stage 3 (Figure 4i) suggesting proper ER-Golgi transport despite extensive remodeling of the ER.
Stage 4: Formation of “foamy” membrane structures inside the vacuole
During stage 4 intriguing sponge-like flat structures arise (Figure 2e, inset, Additional file 1: Figure S5). TPK1-mRFP is excluded from these areas (Additional file 1: Figure S5) which is reminiscent of the observations in individual bulbs (Figure 3d) and within foamy structures (Additional file 1: Figure S4). We hypothesize that these sponge-like structures represent residual TPK1-mRFP-free membrane domains derived from bulbs and vacuolar sheets. Additionally we observed the formation of crystalloid ER (Figure 5 j1,j2).
Stage 5: Vesiculation of the vacuole and the ER leading to cell death
Six days post infiltration some cells with severe vesiculation of endomembranes also display overall intracellular disintegration, indicating the onset of cell death (Figure 2f). As in stage 4, DMP1-eGFP only labels the tonoplast and foamy membrane formations but not the ER (Figure 5l,m,n). The ER is not reticulated but highly vesiculated (Figure 5m,n,o, arrow). The vacuolar and foamy membranes also appear to vesiculate more heavily than in stage 4 and form smaller vesicles (Figure 5o, arrow and p). Despite the obvious breakdown of the ER, the integrity of the nuclear membrane (Figure 5m, arrowhead and o) and Golgi vesicles (Figure 5q) is still retained. The Golgi marker, which is partially secreted to the apoplast ( 4i), indirectly indicates in Figure 5p that the plasma membrane, not labeled by DMP1-eGFP, is still intact (Figure 5p,q,r, arrows). The massive vesiculation of endomembranes was confirmed by electron microscopy (Figure 5s).
Expression of DMP1-eGFP in transgenic Arabidopsis thaliana reveals dual ER/tonoplast localization
Expression of DMP1-eGFP from the DMP1 promoter in Arabidopsis highlights formation of boluses within the ER and fragmentation of ER and tonoplast during senescence
In roots, vacuolar localization of DMP1-eGFP is obvious in the cortex of root tips (Figure 7k-o). In accordance with the current view of vacuole biogenesis, the emerging cells near the root tip contain several vacuoles differing in size (Figure 7d) whereas the older cells in the elongation zone have fewer vacuoles or a single central vacuole (Figure 7o). In these cells the plasma membrane is also labeled (Figure 7n, arrows), which is supposedly due to a truncated isoform of DMP1 (to be published elsewhere). In the phloem bundles, the subcellular localization could not be determined because of the small size of cells (Figure 7p). The ER network was also visible in roots, highlighting once more the ability of DMP1-eGFP to target multiple subcellular membrane systems (Figure 7q).
DMP1-eGFP shows dual intracellular targeting and induces membrane remodeling
Transient expression of DMP1-eGFP in tobacco epidermis cells revealed dynamic targeting of the protein to the tonoplast and the ER. This may indicate that DMP1 possesses competitive tonoplast targeting and ER retention signals, as has been found in proteins that are dually targeted to different compartments such as mitochondria and chloroplasts . The most striking effect of DMP1-eGFP is the complex remodeling and formation of novel membrane structures at the tonoplast and the ER. Shortly after transfection (stage 1), DMP1-eGFP induces the formation of bulbs resembling those first described in young Arabidopsis cotyledons . As they disappear upon progression of cell expansion, formation of these bulbs is believed to be independent of the cytoskeleton . It was initially suggested that they might serve as membrane reservoirs during rapid cell and vacuole expansion . More recently Saito et al. reported that bulbs emerge in germinating seeds by fusion of small vacuoles . Bulbs were found in numerous tissues, at various developmental stages, under stress conditions and in different plant species, suggesting additional functions [15–22]. Specific functions of the bulbs differing from the tonoplast are also indicated in our study by the segregation of DMP1-eGFP and TPK1-mRFP at bulb membranes. A similar case was made by Saito and colleagues who showed that though γ-TIP-GFP and GFP-AtRab7c were both located at the tonoplast, only γ-TIP-GFP was present at the bulbs .
In stage 2 DMP1-eGFP mostly localizes in the ER, which undergoes severe reorganization during that stage. As the cortical ER has in stage 1 a tubular morphology and contains almost no DMP1-eGFP, it is likely that during stage 2 the protein induces reorganization of the ER to large cisternae. Similarly, induction of ER cisternae formation has been observed by expressing GFP fused to the transmembrane domain of calnexin [23, 24]. Transition from tubular to cisternal architecture of the ER has been reported in response to various abiotic and biotic stresses and presumingly reflects modification in ER functions. The tubule-to-cisternae transition may be correlated to the integrity of the actin cytoskeleton, which precisely overlies the ER network , as its disassembly as well as myosin inhibition both lead to loss of the tubular structure and the formation of large cisternae .
The DMP1-eGFP-labeled tubules, which appear at the beginning of stage 3, form a network that matches the cortical ER (Figure 4 a-c). Towards the end of stage 3 the DMP1-eGFP-labeled network dissociates from the cortical ER network (Figure 4d-f). In contrast to a differentiation of the ER into distinct subregions with different protein content, e.g. reticulons which accumulate at edges of ER sheets [27, 28], we observe a segregation of the DMP1-eGFP-labeled structures from the ER, resulting in two physically disconnected membrane networks (Figure 4d-f and g-j). The DMP1-eGFP-labeled network appears more relaxed and less reticulated than the ER network associated with the YFP-HDEL and RFP-p24 markers. We observe additionally the formation of crystalloid ER which consists exclusively of smooth ER (Figure 5 j1 and j2) as has already been described in other studies [29–35]. Thus, we propose that the DMP1-eGFP-labeled network consists of smooth ER whereas the network labeled by YFP-HDEL and RFP-p24 represents rough ER. As crystalloid ER has not been described in tobacco epidermis cells before, an expansion of the smooth ER (stage 3) triggered by accumulation of DMP1-eGFP in the cortical ER (stage 2) seems plausible. To our knowledge this is the first documentation of the proliferation of tobacco epidermis cell cortical ER into smooth ER. Although the biological relevance of this observation has yet to be determined, the fluorescent DMP1 fusion protein is a novel in vivo indicator for the plasticity and differentiation capacity of the ER.
The transition from stage 3 to 4 is accompanied by the disappearance of the smooth ER network and the accumulation of vacuolar membrane sheets. The resulting foamy phenotype of the vacuole during stage 4 represents a massive increase of the tonoplast surface area, implying the supply of new lipids which are known to be synthetized in the smooth ER. We therefore speculate whether the proliferation of smooth ER reflects an increased synthesis of lipids which eventually accumulate in the tonoplast leading to the foamy phenotype. However, as the DMP1-eGFP-labeled network appears to break down to smaller tubules and vesicles (Figure 4g and k), it is also conceivable that these structures are directly taken up by the vacuole by fusing with the tonoplast leading ultimately to the foamy phenotype. Vacuolar membrane sheets have so far been proposed to be bulbs which lost their spherical shape and adopted a sheet-like configuration [11, 20]. This model is supported by our observation that the local separation of DMP1-eGFP and TPK1-mRFP signals in stage 1-bulbs (Figure 3a-d) re-emerges somewhat later in the foamy stage 3-vacuolar sheets (Figure 4e-h2). The sponge-like structures observed during late stage 3 and stage 4 may represent residual membrane islands originating from bulbs and vacuolar sheets. Despite severe membrane remodeling, stage 4-cells appear to remain viable for several days, suggesting that the essential physiological functions of the cells are still intact. Stage 5 presumably represents the fate of cells which have passed a developmental point of no return and undergo cell death marked by fragmentation of the vacuole and the ER.
In Arabidopsis DMP1 highlights dynamic restructuring of the ER and vacuole late in developmental and induced senescence
The fate of the ER during senescence is largely unknown. It has been reported to disappear like other organelles during petal senescence  and even less is known about its destiny during developmental (NS) or induced leaf senescence (DIS). We discovered that the first morphological alteration during NS and DIS affecting the whole ER is the formation of aggregates termed ‘boluses’. DMP1-eGFP expression by its native, senescence-associated promoter illuminates the formation of boluses in all studied organs undergoing NS or DIS (rosette leaves, cauline leaves and siliques). Bolus formation and ER fragmentation are most prominent in darkened plants, as this treatment probably synchronizes cells and subsequent cell death. Comparable aggregations within the ER have been shown by overexpressing reticulons, a class of ER proteins with membrane curvature-inducing properties, in tobacco epidermis cells. The luminal protein YFP-HDEL displays a punctate repartition within the ER network when coexpressed with RTNLB13 and RNTLB1-4 . It was suggested that overexpression of reticulons induces constrictions of the ER tubules creating luminal pockets in which soluble proteins accumulate. A formation of boluses resembling those in our study was also observed within the lumen and at membranes of the ER subdomain that associates with the chloroplast upon expression of a luminal, YFP-HDEL, and a transmembrane protein, YFP-RHD3 . Our study yields for the first time evidence that bolus formation at the ER network occurs during plant development and concerns the whole ER network within a cell. Bolus formation presumably reflects a restrained protein mobility and motion within the ER as a consequence of fading ER integrity and function during late senescence. The timing of membrane reorganization suggests that the subsequent stage in ER network degradation is a brief vesiculation phase (Figure 7c). The fate of these vesicles is unclear. They are possibly taken up by the vacuole for further degradation.
We only rarely observed fragmentation of the vacuole. It is not clear whether this fragmentation indicates PCD during senescence or another unrelated type of cell death that occurs independently in individual cells. Senescence is classified as ‘autolytic’ or ‘vacuolar’ plant cell death, that is marked by an initial increase of the vacuolar volume by fusion of smaller vacuoles and the shrinkage of the cytoplasm, followed by rupture of the tonoplast and rapid degradation of the cytoplasm [3, 36]. Fragmentation of the vacuole has not yet been reported in autolytic cells death. However, in epidermis cells the central vacuole already occupies more than 90 % of the cell volume which precludes the fusion of smaller vacuoles. It is conceivable that in these cells a rupture of the tonoplast is accompanied by a brief fragmentation of the central vacuole that can hardly be visualized in the EM.
A function of DMP1 in membrane fusion and fission events during development?
The molecular function of DMP1 is still unknown. However, as from stage 2 all phases of membrane remodeling in tobacco cells expressing DMP1-eGFP are associated with membrane fusion or fission, it seems likely that DMP1 is actively involved in these processes. In stage 1, the formation of bulbs results from invagination of the tonoplast forming a double-membrane inside the vacuole [10, 20] and may thus not require membrane fusion or fission. During stage 2, ER reorganization from tubular to cisternal elements requires membrane fusion. Apparent segregation of smooth ER from the cortical ER network can only be explained by membrane fission and membrane expansion. The emergence of free tubules and small vesicles in the cytosol that obviously originate from the smooth ER-network requires membrane fission. Formation of vacuolar sheets and foamy membrane structures in stage 4 presumably needs membrane fission and fusion, and eventually vesiculation of the vacuole during stage 5 necessitates membrane fission.
Also in Arabidopsis the localization of DMP1-eGFP suggests a close connection to membrane fission/fusion events. In root tips undergoing central vacuole biogenesis, known to take place by fusion of smaller vacuoles and vesicles, DMP1-eGFP is no longer expressed in the cortex layer as soon as the central vacuole is established. This strongly argues for a participation of DMP1 in vacuole biogenesis in this cell layer. During senescence, the protein is associated rather with the reverse reaction, i.e. the fragmentation of the ER and the tonoplast by membrane fission. It is conspicuous that DMP1 shares a similar overall architecture with the reticulons, which have been shown to shape ER tubules by membrane bending [37, 38]. The members of both protein families possess four transmembrane domains. In reticulons these are arranged in two long hydrophobic “hairpins” leading to a wedge-like topology with very short loops 1 and 3 and a longer loop 2 facing the cytosol . The DMP proteins have also short loops 1 and 3 and a longer loop 2 . Whether DMP1 is directly, e.g. by enforcing membrane distortion, or indirectly, e.g. by interaction and cooperation with other proteins, responsible for the membrane remodeling phenomena reported in this study remains to be elucidated.
AtDMP1 is a novel senescence-associated membrane protein that is targeted to the ER and the tonoplast. The DMP1-eGFP fusion protein illuminates dynamic ER and tonoplast remodeling processes and endomembrane reorganization during leaf senescence: (1) Transient expression of DMP1-eGFP in tobacco leaf cells led to temporally ordered remodeling events of the ER (tubules-to-sheets transition, proliferation of smooth ER and formation of crystalloid ER) and the tonoplast (formation of bulbs, vacuolar sheets and “foamy” structures). (2) Stable expression in Arabidopsis by the native promoter demonstrated for the first time the occurrence of aggregates inside the ER membranes (“boluses”) and vesiculation of the ER during developmental and induced senescence. (3) In root tips of Arabidopsis plants DMP1 is associated with vacuole biogenesis. Comparable temporally ordered restructuring of the ER, the tonoplast or other membranes has not yet been reported for other fusion proteins. We conclude that DMP1 is actively involved in endomembrane remodeling, membrane fission and membrane fusion in senescing cells and in root development.
Generation of constructs
35S:DMP1-eGFP mRFP-MUB2 and TPK1-mRFP expression vectors were generated and modified as described in . RFP-p24 and YFP-HDEL were provided by David Robinson (University of Heidelberg, Germany) and Chris Hawes (Oxford Brookes University, UK), respectively. DMP1p:DMP1-eGFP was generated by amplifying a 2364 bp DMP1promoter:624 bp DMP1 ORF fragment on genomic Arabidopsis Col-0 DNA with the primers 5′-CGGTCTAGAGAGAACAAAATCCTCCGTATC-3′ and 5′-AACTGCAGCGGCAGAGACCGAGGCTTTC-3′, followed by digestion of the PCR product with XbaI/PstI and ligation into XbaI/PstI digested binary vector pGTkan3 .
Plant material, growth conditions and plant transformation
Arabidopsis thaliana Col-0 and Nicotiana benthamiana plants were grown and transformed as described . All Agrobacterium cultures were resuspended to OD600 = 0,05 prior to tobacco infiltration. To reduce silencing of the transgenes, all constructs were co-infiltrated with the silencing suppressor p19 .
Confocal microscopy was performed on a Leica TCS-SP5 AOBS (acousto-optical beam splitter) confocal laser scanning microscope (Leica Microsystems) equipped with water immersion objectives (20x with numerical aperture of 0.7 and 63x with numerical aperture of 1.20). Excitation/emission wavelengths were: eGFP: 488 nm (argon laser)/495 nm - 510 nm; YFP: 514 nm (argon laser)/525 nm - 555 nm; mRFP and mCherry: 561 nm (diode-pumped solid-state (DPSS) laser)/585 nm - 655 nm. Multi-color imaging of cells co-expressing eGFP, YFP and mRFP (or mCherry) was performed by sequential scanning to prevent crosstalk. Post-acquisition image processing was performed with the Leica LAS AF software (Leica Microsystems). Depending on the object structure either single pictures or maximum projections resulting from z-stacks are shown. The following pictures result from maximum projections: Figure 1b and c; Figure 2b-e; Figure 3i-k; Figure 4a-c, g-j, k and l; Figure 5a-d, l-o and m; Figure 7m; Additional file 1: Figure S6.
Transmission electron microscopy
For fixation, substitution and embedding of one mm2 leaf sections (see Additional file 1: Table T1 for protocol) a laboratory microwave (PELO BioWave® 34700–230, Ted Pella, Inc., Redding CA, USA) was used. For analysis in a Tecnai G2 Sphera transmission electron microscope (FEI Company, Eindhoven, Netherlands) at 120 kV, ~70 nm ultra thin sections were cut with a diamond knife and contrasted with uranyl acetate and lead citrate prior to examination.
We thank David Robinson (University of Heidelberg, Germany) and Chris Hawes (Oxford Brookes University, UK) for providing constructs RFP-p24 and YFP-HDEL, respectively. A.K. and this project were supported by priority programme 1108 of the Deutsche Forschungsgemeinschaft (DFG).
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