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First published online February 23, 2007; 10.1104/pp.107.096263 Plant Physiology 143:1628-1639 (2007) © 2007 American Society of Plant Biologists OPEN ACCESS ARTICLE
Protein Mobilization in Germinating Mung Bean Seeds Involves Vacuolar Sorting Receptors and Multivesicular Bodies1,[W],[OA]Department of Biology and Molecular Biotechnology Program (J.W., Y.L., S.W.L., S.S.M.S., L.J.) and Institute of Plant Molecular Biology and Agricultural Biotechnology (J.W., S.S.M.S., L.J.), Chinese University of Hong Kong, Shatin, New Territories, Hong Kong, China; and Department of Cell Biology, Heidelberg Institute for Plant Sciences, University of Heidelberg, D–69120 Heidelberg, Germany (S.H., D.G.R.)
Plants accumulate and store proteins in protein storage vacuoles (PSVs) during seed development and maturation. Upon seed germination, these storage proteins are mobilized to provide nutrients for seedling growth. However, little is known about the molecular mechanisms of protein degradation during seed germination. Here we test the hypothesis that vacuolar sorting receptor (VSR) proteins play a role in mediating protein degradation in germinating seeds. We demonstrate that both VSR proteins and hydrolytic enzymes are synthesized de novo during mung bean (Vigna radiata) seed germination. Immunogold electron microscopy with VSR antibodies demonstrate that VSRs mainly locate to the peripheral membrane of multivesicular bodies (MVBs), presumably as recycling receptors in day 1 germinating seeds, but become internalized to the MVB lumen, presumably for degradation at day 3 germination. Chemical cross-linking and immunoprecipitation with VSR antibodies have identified the cysteine protease aleurain as a specific VSR-interacting protein in germinating seeds. Further confocal immunofluorescence and immunogold electron microscopy studies demonstrate that VSR and aleurain colocalize to MVBs as well as PSVs in germinating seeds. Thus, MVBs in germinating seeds exercise dual functions: as a storage compartment for proteases that are physically separated from PSVs in the mature seed and as an intermediate compartment for VSR-mediated delivery of proteases from the Golgi apparatus to the PSV for protein degradation during seed germination.
The seeds of high plants accumulate large amounts of storage proteins during seed development and seed maturation, which are mobilized to provide building blocks and energy for seed germination and early seedling growth upon seed germination (Bewley and Black, 1994  ). During seed development and maturation, newly synthesized storage proteins are usually transported and stored in a specialized compartment, termed protein storage vacuole (PSV), which is defined by the presence of  - and  -tonoplast intrinsic protein (TIP) in their tonoplasts (Jiang et al., 2000).
Upon seed germination, storage proteins, oil body, and starch are degraded and used for seedling growth (Bewley and Black, 1994
Transport of soluble proteins to lytic vacuoles in plant cells is a receptor-mediated process involving a protein family termed vacuolar sorting receptors (VSRs; Neuhaus and Rogers, 1998
Relatively little is known about the possible roles of VSR proteins during seed germination. VSRs have been found, via whole-genomic analysis and reverse transcription-PCR analysis, universally and are differentially expressed in various cell and tissue types during plant development and seed germination (Laval et al., 2003 In this study, we have tested the hypothesis that VSR proteins play a role in mediating protein degradation during seed germination. Toward this goal, we demonstrate that hydrolytic enzymes and, most likely, VSR proteins as well, are synthesized de novo during mung bean (Vigna radiata) seed germination. Whereas VSRs seem to be internalized into the lumen of MVBs for degradation, VSRs specifically interact with a newly synthesized Cys protease aleurain and colocalize together to MVBs in germinating mung bean seeds. Finally, aleurain reached PSVs in germinating seeds. Thus, VSRs transport newly synthesized proteases via PVCs/MVBs to PSVs for protein degradation during seed germination.
VSR Proteins Are Present in Germinating Seeds
Seven VSR isoforms with conserved amino acid sequences and structures have been identified in the Arabidopsis genome (Hadlington and Denecke, 2000
To study the possible roles of VSR proteins in germinating seeds, we then studied protein profiles during seed germination of mung bean seeds. Mung bean was chosen because the seed germinates uniformly almost 100% and rapidly with radicle appearance at day 1 after imbibition. Thus, seeds at different stages of imbibition were collected for protein extraction and western-blot analysis using various antibodies. As shown in Figure 2A , VSR proteins are present in all stages of germinating seeds with gradually decreased amounts from day 0 to day 4 after imbibition, where a new band with lower Mr was detected from day 2 germinating seeds. When the BP-80 CT antibodies, raised against a synthetic peptide corresponding to the CT of BP-80 (Tse et al., 2004 ), were used, the detected VSR proteins showed similar decreasing profiles in germinating seeds. Similarly, both - and -TIP, markers for PSVs, are present during the early stages of germination from day 0 to day 3 with decreased amounts, indicating the degradation of storage contents in germinating seeds. In contrast, the lytic vacuole marker  -TIP (Paris et al., 1996) and the two vacuolar Cys proteases, the Golgi-derived aleurain (Holwerda et al., 1990), and the ER-derived SH-EP (Toyooka et al., 2000; Okamoto, 2006), were not detected until 2 d after seed imbibition and increased thereafter from day 2 to day 4, indicating the transition of PSVs into a lytic vacuole for protein mobilization during seed germination. Because aleurain and SH-EP were newly synthesized during seed germination, they must play a role in mediating protein degradation in germinating seeds at a later stage.
To further ascertain whether new VSR proteins are synthesized de novo during seed germination, we performed a two-dimensional (2-D) gel/western-blot analysis with both VSR and BP-80 CT antibodies on proteins isolated from mature (day 0) and day 3 germinating seeds. As shown in Figure 2B, at least two VSR isoforms (indicated by an arrow) were detected by VSR antibodies in day 0 dry seeds, whereas two additional VSR isoforms (indicated by arrowheads) were found in day 3 germinating seeds, indicating that these VSRs are probably synthesized de novo during seed germination, even though the overall amounts of VSR proteins were decreased during seed germination as shown in Figure 2A. To further confirm that the two protein spots detected by VSR antibodies in day 3 germinating seeds were real VSR isoforms and not modifications of the day 0 VSRs, we performed similar western-blot analyses on both day 0 and day 3 protein samples using BP-80 CT antibodies. As shown in Figure 2B, BP-80 CT antibodies detected the same VSR proteins in both day 0 and day 3 samples (as indicated by an arrow) as those detected by VSR antibodies in day 0 samples, but did not recognize the two additional spots (arrowheads) in day 3 samples. Therefore, the two new spots detected by VSR antibodies in day 3 samples most likely represent newly synthesized VSR isoforms distinct from those detected by both VSR and BP-80 antibodies in day 0 samples. Thus, both preexisting and newly synthesized VSRs are detected in germinating seeds in which the old VSRs might be important in triggering the onset of seed germination, whereas the new VSRs function at later stages of seed germination. These results are consistent with a previous study in which mRNAs of newly synthesized VSR proteins in germinating cotyledons of Arabidopsis were compared to dry seeds (Laval et al., 2003 ). Thus, the presence of VSRs in germinating seeds might indicate their possible roles in transporting proteases via the Golgi-dependent pathway to a place where protein degradation occurs, a hypothesis being tested in this study.
As a first step to study the functional roles of VSRs during seed germination, we study the subcellular localization of VSR proteins via both confocal immunofluorescence and immunogold electron microscopy (EM) with VSRat-1 antibodies in germinating mung bean seeds. As shown in Figure 3
, confocal immunofluorescence with anti-VSRat-1 (Tse et al., 2004
To find out whether MVBs are present in developing, mature, and germinating seeds and study their morphology, we performed structural studies on MVBs using chemically fixed mung bean seed samples. As shown in Figure 4 , typical MVBs with typical internal vesicles were found in developing seeds (5 and 10 d after flowering), mature dry seeds, and germinating seeds (day 1 to day 3 after germination). These results indicated that MVBs are universally present during the life cycle of seeds from development, maturation, and germination. Because we could not prepare high-pressure frozen/freeze-substituted samples of dry seeds for immunogold EM study, labeling of VSRs in dry seeds was not possible.
To further confirm the presence of VSR proteins in MVBs, we isolated VSR-enriched fractions via continuous Suc density gradients (Tse et al., 2004 ) for use in immunogold negative staining with VSR antibodies. As shown in Figure 5
, the identified VSR-enriched fractions (17 and 19; Fig. 5A) contained MVB-like vesicles that were specifically labeled by VSRat-1 and BP-80 CT antibodies (Fig. 5B). Thus, isolated MVBs also contain VSR proteins and VSR proteins were concentrated on the MVB-like structures in germinating mung bean seeds.
Isolation and Identification of VSR-Interacting Proteins in Germinating Seeds To study the possible VSR cargos during seed germination, we next carried out biochemical cross-linking studies to identify VSR-interacting proteins in germinating seeds. We first prepared microsome fractions from day 3 germinating mung bean cotyledons, followed by chemically cross-linking and subsequent protein purification using an affinity column conjugated with VSRat-1 antibodies (Fig. 6A ). VSR-interacting proteins were then eluted from the column (termed S3 fraction) and subjected to matrix-assisted laser-desorption ionization (MALDI)-time-of-flight (TOF) analysis for protein identification (Fig. 6A). As controls, we used a column without VSR antibodies (C1) and microsome proteins without chemical cross-linking treatment eluted from columns conjugated with VSR antibodies (C2). As shown in Figure 6B, eluted proteins of cross-linked samples from anti-VSR columns in S3 contained the VSR band (asterisk) and eight other visible bands (numbered 1–8) in a Coomassie Blue-stained gel in which the VSR band, band 1, and band 4 were identified as a VSR homolog, a PV72 homolog (a pumpkin VSR), and aleurain, respectively, via MALDI-TOF analysis (see also Table III for detailed information on amino acids and matching). As expected, the bands corresponding to VSR and PV72 were also identified from non-cross-linked control samples (C2) due to binding of VSR antibodies. In addition, the identified aleurain was a specific VSR-interacting protein because no such band was detected in C2 (Fig. 6B). The identification of other protein bands via MALDI-TOF analysis was unsuccessful due to the poor quality of the generated fingerprints and lack of a database for mung bean (data not shown).
To further confirm that the eluted aleurain was due to specific interaction between VSR and aleurain, we performed western-blot analysis on various fractions of proteins using antibodies against known markers (Fig. 6C). As expected, VSR antibodies detected VSR proteins predominantly in S3 and C2 fractions (eluted from an anti-VSR column) with much less in S1 and S2 (Fig. 6C, image 1). Similar results were obtained when BP-80 CT antibodies were used (Supplemental Fig. S2). Similarly, the 42-kD proaleurain (indicated by a single asterisk) was mainly found in S3, probably in the presence of the VSR-interacting motif NPIR at its N terminus, whereas the 32-kD mature aleurain (indicated by a double asterisk) was found in S1 and S2, but absent in S3 because aleurain lacks NPIR (Fig. 6C, image 2). In contrast, the other Cys protease, SH-EP, and the two storage proteins, 2S albumin and phaseolin, as well as Rha1, a small GTP-binding protein of the Ras family (Sohn et al., 2003 ), were almost missing in S3, but present in both S1 and S2 (Fig. 6C, images 3–6). These results indicated that the interaction between VSR proteins and aleurain in germinating seeds is specific and consistent with the demonstrated interaction between BP-80 and the aleurain NPIR vacuolar sorting motif by which BP-80 was first shown to function as a sorting receptor for transporting hydrolases via the Golgi apparatus to the lytic vacuole (Kirsch et al., 1994; Paris et al., 1997; Ahmed et al., 2000; Cao et al., 2000).
To further demonstrate that the interaction between VSR and aleurain in germinating mung bean seeds is due to in vivo protein interaction, we next performed subcellular localization to compare VSR with aleurain. Paraffin sections prepared from day 3 germinating mung bean seeds were double labeled with two antibodies and observed under confocal microscopy for their localization and relationship to one another. As shown in Figure 7 , the punctate signals generated by VSR and aleurain antibodies were largely (more than 85%) overlapped (Fig. 7A; Table IV ), indicating colocalization of VSR and aleurain to the same organelles during seed germination. In contrast, PVC/MVB organelles detected by anti-VSR and anti-BP-80 were largely separated from the KV organelles labeled by SH-EP antibodies in the same cells of germinating seeds (Fig. 7, B and C). Similarly, when the two Cys proteases were compared directly in the same cell, they remained largely separated (Fig. 7D; Table IV). To further confirm the MVB localization of aleurain in germinating seeds, we performed an immunogold EM study with ultrathin sections prepared from high-pressure frozen/freeze-substituted cotyledon samples of day 3 germinating mung bean seeds. As shown in Figure 8 , anti-aleurain specifically labeled MVBs (Fig. 8A), whereas SH-EP antibodies labeled KV vesicles (Fig. 8C), but not MVB (Fig. 8B) in germinating seeds. These results demonstrated that VSR proteins colocalized with aleurain in PVCs/MVBs that are distinct from the KV organelles in germinating mung bean seeds.
SH-EP is a Cys protease that was newly synthesized during seed germination and transported to PSV via ER-derived KV vesicles for protein degradation in germinating mung bean seeds (Toyooka et al., 2000 ). In contrast, aleurain is transported by BP-80 via Golgi and PVC to the vacuole (Holwerda et al., 1990; Paris et al., 1997). These results are consistent with previous studies on SH-EP and aleurain for their distinct transport pathways leading to vacuoles.
To further ascertain whether aleurain and SH-EP reached PSV in germinating seeds, we next performed subcellular localization to compare the PSV marker
Roles of VSR Proteins in Germinating Seeds
VSR proteins may perform dual functions in plant cells. BP-80 was the first VSR protein to be identified based on its interaction with the vacuolar sorting determinant NPIR (Kirsch et al., 1994
Seven VSR homologs have been found in Arabidopsis that are present in different temporal and spatial expression profiles (Laval et al., 2003 In this study, we have shown that two Cys proteases, aleurain and SH-EP, and most likely a VSR as well, were synthesized de novo during seed germination. However, we cannot rule out the possibility that BP-80 CT antibodies might fail to discriminate various VSR isoforms due to VSR turnover and thus lost their epitopes for anti-BP-80 CT. Confocal immunofluorescence and immunogold EM studies further demonstrated that VSR and aleurain colocalized to MVBs in germinating mung bean seeds, indicating that VSR proteins transport aleurain to PSV via MVBs for protein degradation during seed germination. MVBs were found in developing, mature, and germinating mung bean seeds in structural EM studies, indicating the importance of MVB-mediated protein sorting in seed development and germination. However, in mature dry seeds, subcellular localization of VSRs was not successful due to technical difficulties in preparing high-pressure frozen sections for immunogold EM studies. Nevertheless, it is reasonable to assume that VSRs also located in MVBs in mature dry seeds because VSRs were specifically present in MVBs in day 1 and day 3 germinating seeds. So what are the functional implications of MVB localization of VSR proteins in mature dry seeds? Because VSRs seem to transport proteases to MVBs during seed development, the MVB compartmentation of VSR proteins in mature seeds suggests that the proteases might also locate to MVBs in mature seeds, thus providing a physical separation from PSV-localized storage proteins. Early in seed germination, these stored proteases would then be released into the PSV to degrade storage proteins. In this way, protein degradation in the PSV can be initiated before the new synthesis of VSRs and proteases can take effect. Therefore, our results support a model that proteases are newly synthesized and transported to PSVs via MVBs by VSR proteins for protein degradation in germinating seeds.
It is believed that VSR proteins sort cargo proteins at the trans-Golgi network and pack them into CCVs for delivery to a lytic PVC, from where the receptors are recycled back to the Golgi via the newly characterized retromer complex (Oliviusson et al., 2006
In this study, we demonstrated that, whereas VSRs are being newly synthesized, the total amounts of VSR proteins in germinating seeds, as detected by western-blot analysis with VSRat-1 antibodies, gradually decreased as germination proceeded from day 1 to day 3. However, the differential subcellular distribution of VSR proteins within the PVCs/MVBs as shown by immunogold EM has to be taken into account: Whereas the majority (more than 80%) of the VSR proteins were found on the peripheral membrane of MVBs in day 1 germinating seeds, VSR proteins were mainly found inside the lumen of MVBs in day 3 germinating seeds. This novel observation indicates that the membrane-localized VSRs at steady state may represent the population of recycling receptors, whereas those VSRs inside the lumen of MVBs are destined for degradation, presumably after fusion of the PVCs/MVBs with the vacuole (Jiang et al., 2002
Plant Materials Mung bean (Vigna radiata) seeds were germinated on wet filter paper at 26°C in the dark. The cotyledons of germinating mung bean were used for protein extraction, organelle isolation via fractionation, and sample preparation for transmission EM.
Characterization of the following antibodies used in this study has been described as follows: polyclonal VSRat-1 and BP-80 CT antibodies (Tse et al., 2004
Cotyledons of germinating mung bean at different stages were collected and ground to a fine powder in liquid nitrogen. Protein extraction buffer (Tris-HCl 50 mM, pH 7.4 containing 150 mM NaCl, 1 mM EDTA, 0.1 mM phenylmethylsulfonyl fluoride, 1% SDS, and 5 µg/mL leupeptin) was then added to the powder for extraction of proteins. Protein extracts were boiled for 10 min and centrifuged at 14,000 rpm for 5 min. Supernatants were collected for determination of protein concentrations (Bradford, 1976
For 2-D gel electrophoresis, protein samples were prepared as recommended by the manufacturer (Amersham Biosciences). Briefly, cotyledon powder was suspended in 10% TCA, 0.3% dithiothreitol in acetone, and stored at –20°C overnight. After centrifugation, the pellet was washed with acetone and air dried, followed by addition of the rehydration buffer (8 M urea, 4% CHAPS, 60 mM dithiothreitol, 2% Pharmalyte 3–10, 0.002% bromphenol blue) to solubilize the pellet before protein samples were directly loaded onto the Immobiline DryStrip (pH 3–10, 7 cm, nonlinear; Amersham Biosciences) and rehydrated overnight. One-dimensional isoelectric focusing (IEF) was performed with the Amersham Biosciences IPGphor II IEF system. Upon completion of IEF electrophoresis, the gel strip was equilibrated according to the manufacturer's instructions. Proteins in the gel strip were separated via SDS-PAGE using a Bio-Rad Protean II mini electrophoresis unit, followed by protein transfer to the membrane and immunoblot analysis with VSR antibodies as previously described (Tse et al., 2004
The cotyledons of day 3 germinating mung bean were collected and ground in grinding buffer (HEPES, pH 7.2 containing 0.4 M Suc), followed by centrifugation at 800g for 10 min. The resulting supernatant was further subjected to ultracentrifugation at 100,000g for 1 h before the pellet was resuspended in grinding buffer and used as a microsome fraction. For the cross-linking study, dithiobis(succinimidylpropionate) (20 mM, dissolved in dimethyl sulfoxide; Pierce) was added to the microsome fraction at 2 mM (final concentration) and incubated at room temperature for 30 min. To quench the reaction, Tris-HCl (pH 8.0) was added at 20 mM (final concentration), followed by incubation at room temperature for 30 min. Triton X-100 was then added at 1% (final concentration) to lyse the microsomes, followed by incubation at room temperature for 4 h before the insoluble materials were removed by centrifugation at 20,000g for 10 min. For isolation of VSR-interacting proteins, 4 volumes of 1x Tris-buffered saline containing 0.25% NP-40 were added to the supernatant of the above cross-linked samples and mixed with the resin conjugated with VSR antibodies, followed by rotation at room temperature overnight before the resin was transferred to a column and washed with phosphate-buffered saline. The bound proteins were eluted from the column with 0.2 M Gly-HCl (pH 2.0) and collected in equal volumes of 1 M Tris-HCl (pH 8.0) to each fraction. The eluted proteins, along with other controls, including un-cross-linked samples, total protein, and passing-through proteins, were separated by SDS-PAGE analysis, followed by Coomassie Blue staining and protein identification via MALDI-TOF or western-blot analysis with various antibodies.
Fixation and preparation of tissues from cotyledons of germinating mung bean for paraffin-embedded sections and their labeling and analysis by confocal immunofluorescence have been described previously (Jiang and Rogers, 1998
PVC isolation was performed according to Tse et al. (2004)
The general procedures for conventional thin sectioning of chemically fixed samples of mung bean were performed essentially as described previously (Ritzenthaler et al., 2002
Immunogold EM on ultrathin sections prepared from high-pressure frozen/freeze substitution of germinating mung bean cotyledons was performed essentially as previously described (Tse et al., 2004
The following materials are available in the online version of this article.
We are grateful to Dr. T. Okamoto and Dr. K. Toyooka (Tokyo Metropolitan University), Dr. K. Matsuoka (RIKEN) for sharing various SH-EP antibodies, and Prof. I. Hwang (Pohang University of Science and Technology) for the Rha1 antibody. Received January 22, 2007; accepted February 12, 2007; published February 23, 2007.
1 This work was supported by the Research Grants Council of Hong Kong (grant nos. CUHK4156/01M, CUHK4260/02M, CUHK4307/03M, and CUHK4580/05M), the National Science Foundation of China (grant no. 30529001), Chinese University of Hong Kong Scheme C, University Grants Committee-Area of Excellence (grant no. B–07/99 to L.J.), and the German Research Council (to D.G.R.).  The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Liwen Jiang (ljiang{at}cuhk.edu.hk).
[W] The online version of this article contains Web-only data.
[OA] Open Access articles can be viewed online without a subscription. www.plantphysiol.org/cgi/doi/10.1104/pp.107.096263 * Corresponding author; e-mail ljiang{at}cuhk.edu.hk; fax 852–2603–5646.
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