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Separation of the nucleus and cytoplasm, maintained by two membrane bilayers that form the nuclear envelope, allows for spatial control over transcription factors and signaling molecules. This compartmentalization further ensures the presence of specialized environments for different stages of gene expression, such as transcription and protein production. Selective exchange between these two compartments is clearly important as well. Whereas many types of active transport between the nucleus and cytoplasm rely on transport receptors in the importin-β superfamily, export of mRNA utilizes distinct soluble machinery (6, 92). Moreover, in general mRNA export does not depend on a specific motif in the cargo, as has been demonstrated in many other cases of receptor-cargo interactions (22). Recent progress in identifying soluble factors important to mRNA trafficking is beginning to reveal the molecular basis for functional coupling between steps in mRNA biogenesis and how such coupling, rather than a consensus motif, brings specificity to mRNA export.
Studies with Saccharomyces cerevisiae revealed that the key modulators of cellular mRNA export are unrelated to canonical importin-β-related receptors. Specifically, yeast deficient in a gene called MEX67 accumulate poly(A)+ RNA in the nucleus (73). A second protein, Mtr2p, binds Mex67p, and this interaction is required for the export of poly(A)+ RNA in yeast (71, 77). In an independent avenue of investigation, involving metazoan cells and the simian type D retrovirus Mason Pfizer monkey virus, the cellular protein TAP was found to facilitate export of RNA containing the viral constitutive transport element (CTE) (8, 32). TAP, confirmed to be the human orthologue of Mex67p, has been redesignated NXF1 (nuclear export factor 1).
NXF1 interacts with p15/NXT1, the presumed functional homologue of Mtr2p (33, 44). Although Mtr2p and p15 share no sequence similarity, the Mex67p-Mtr2p complex displays similar structural architecture to the NXF1-p15 heterodimer (21). Indeed, the mRNA export defect in yeast cells deficient in both Mex67p and Mtr2p can be rescued by expression of human NXF1 and its cofactor p15 (44). Expression knock-down studies using RNA interference have demonstrated that NXF1 and p15 are required for poly(A)+ RNA export (35, 84, 93), further strengthening the case for an evolutionarily conserved system of mRNA export that is distinct from the importin-β superfamily. Likewise, studies with Xenopus oocytes support the conclusion that the small GTPase Ran, a key modulator of importin-β-type receptors, is not key to mRNA export (10). However, the distinction between mRNA export and the importin-β family/Ran network is not absolute, as an importin-β family member has recently been implicated in mRNA export as well (74).
In contrast to CTE-mediated transport, NXF1 does not bind directly to cellular mRNA. Therefore, deciphering how NXF1 is recruited to mRNA is crucial to understanding mRNA export and has been the focus of much current work. Experiments with Xenopus oocytes demonstrated that the process of splicing can contribute to the efficiency of mRNA export; the spliced product from adenovirus major late (Adml) mRNA was shown to export more efficiently than an identical mRNA engineered to lack an intron (58). In addition, the spliced Adml mRNA and its engineered counterpart form distinct RNP complexes in splicing extracts, suggesting that recruitment of a unique set of proteins to the spliced mRNA may promote export competency. Indeed, specific proteins, including the factor Aly (renamed REF for RNA export factor), the acute myeloid leukemia-associated protein DEK, and the RNA binding protein Y14, were individually found to preferentially interact with processed mRNA (46, 60, 97). The identification and characterization of an entire protein complex, the exon junction complex (EJC), associated with spliced mRNA soon followed (53). Components originally identified in the EJC (53) include REF, SRm160, RNPS1, DEK, Y14, and later its protein partner Magoh (45).
The notion that EJC deposition leads to recruitment of NXF1 is an attractive model to explain the stimulatory effect of splicing on export. Direct interactions between REF and NXF1 have been observed in both human and yeast systems (69, 81). REF also shuttles between nucleus and cytoplasm and enhances mRNA export when injected into Xenopus oocyte nuclei as a recombinant protein (69, 97). Studies with yeast demonstrated a high degree of functional conservation since Yra1p (the yeast orthologue of REF)-deficient cells accumulate poly(A)+ RNA; Yra1p also physically interacts with mRNA in vivo (79). The enhanced placement of REF onto mRNA in a splicing-dependent fashion, as well as its association with NXF1, made REF a prime candidate for recruiting NXF1 to mRNA.
A connection between splicing and mRNA export was further solidified with the characterization of a novel role for the putative RNA helicase UAP56 [56-kDa U2AF(65)-associated protein]. UAP56 was originally characterized for its contribution to spliceosome assembly (20). More recently, independent from its function in splicing, a role for Sub2p (yeast orthologue of UAP56) in mRNA export has also been identified (78). Sub2p directly interacts with Yra1p in vitro and in vivo, a characteristic conserved in metazoan counterparts (59, 78). Interestingly, Sub2p and Mex67p bind to the same domain of Yra1p, suggesting that Sub2p may recruit Yra1p to mRNA and may subsequently be displaced by Mex67p (78). Moreover, recruitment of REF to spliced mRNA is dependent upon its interaction with UAP56 (59) and UAP56 is essential for mRNA export in Drosophila (25). From these data, a very simple yet elegant mode of coupling splicing with mRNA export became evident. Namely, REF is recruited to spliced mRNA through direct interactions with UAP56, and consequently, REF (and the EJC in general ) recruits the export factor NXF1 to promote exit from the nucleus by mediating docking and presumably movement through the pore.
Despite the observation that splicing promotes export of mRNA, such processing is not the only or even the major route for export factor recruitment. For example, antibodies directed against REF block the export of both spliced and intronless mRNA in Xenopus oocytes (69). Yeast cells deficient in Sub2p show arrest of bulk poly(A)+ mRNA (42, 78) despite the lack of an intron in most genes. Moreover, the interaction between Yra1p and mRNA occurs in the absence of splicing in yeast (55) and the same is thought to be true for UAP56 in Chironomus tentans (48). RNA interference studies with Drosophila also showed that depletion of UAP56 causes the export inhibition of both spliced and nonspliced RNAs (25). In fact, additional studies with Drosophila demonstrated essential roles in bulk mRNA export for NXF1, p15, and UAP56, while the EJC components Y14, RNPS1, SRm160, and REF appear to be dispensable (24).
Recent functional analysis of mammalian cells also suggested that splicing does not always have a major effect on mRNA export per se. When compared to intron-containing counterparts, intronless constructs did not show a specific decrease in cytoplasmic RNA levels but rather were found to result in a general decrease in both nuclear and cytoplasmic RNA (57). This result was corroborated in Xenopus oocytes, where the relative RNA distribution of a luciferase reporter construct did not significantly change if an intron was present to recruit EJC components (64). In fact, in these studies, members of the EJC complex appear to be involved in increasing the translational yield or in enhancing mRNA abundance rather than influencing export.
Together, these observations suggest that the coupling between splicing and export factor recruitment that has been documented may represent only one way that export factors load onto mRNA and indeed may make a significant contribution at this step only when the RNA is particularly short. This conclusion is further illustrated by the work of Mattaj and colleagues, who engineered a hybrid U1 snRNA harboring an intron flanked by minimal exonic sequences and demonstrated that splicing endows this hybrid molecule with hallmark features of mRNA export (65). They further observed that hybrid U1 snRNA molecules containing sufficiently long, unstructured stretches of exonic sequences are also exported using mRNA export machinery instead of U1 snRNA-associated export factors (65). The function of this inserted sequence is independent of orientation and has thus defined a stretch of approximately 300 nucleotides of any unstructured RNA to be an mRNA identity element (reviewed in reference 86). A previously observed correlation between export and mRNA length requirements also supports this connection (69). This insight, however, begs the question of exactly which are the critical proteins that recognize and bind unstructured stretches of mRNA. REF is a good candidate, but the observation that REF is dispensable for mRNA export (24, 56) suggests that other proteins work in conjunction or in parallel at this step.
CREATING EXPORT COMPETENT mRNPS: DIFFERENT MEANS TO THE END?
Presumably, export factors can load onto mRNA in both a relatively nonspecific way as well as via splicing-coupled mechanisms. If an mRNA is sufficiently long, generic loading of factors appears to be no more limiting than splicing-dependent mechanisms. The above-mentioned results provide insight into how a diverse array of mRNAs can be recognized by export machinery and point toward the influence of mRNA cargo size and global appearance on export requirements. However, while a baseline for mRNA export requirements may be met by an mRNA identity element or by splicing, additional mechanisms could promote efficiency in connecting to either NXF1 or other transport factors. For instance, RNA elements that recruit export factors have been characterized (39) and, as discussed in more detail below, export factors are also recruited during very early events in mRNA biogenesis (Fig. 1).
Interconnections between steps in mRNA biogenesis. A schematic illustration of mRNA biogenesis is depicted, with the proposed times of recruitment and functions for specific proteins indicated in the boxes. (1) Transcription. Much evidence points to cotranscriptional loading of factors involved in RNA processing, export, and quality control to the nascent transcript. The mobile pore proteins, Nup153 and Nup98, are candidates (indicated in red text) for loading onto mRNA early in its biogenesis, although this is yet to be demonstrated. RNAPII, RNA polymerase II. (2) Splicing. The splicing factor UAP56 interacts with REF, which is one of a group of proteins referred to as the EJC that is deposited on mRNA in conjunction with splicing. Loading of certain transport factors, such as REF, can also occur independent of splicing as a part of TREX or if the RNA is sufficiently long. (3) Remodeling and export. NXF1-p15 is recruited to the mRNA via protein-protein interactions, readying export-competent mRNA for mobilization out of the nucleus. At this step, other proteins, such as Gle1, RAE1, Trn-2 (transportin-2), and TREX components, are also thought to function. Certain hnRNPs and EJC components are shed from the mRNP prior to export, and proper mRNP formation appears to be monitored at this stage by the exosome. Specific pore proteins, or Nups, are implicated in moving mRNA cargo through the pore (Fig. 2). Although loaded onto the transcript early in biogenesis, Dbp5 may play a late role in remodeling and/or moving the mRNP complex. (4) Cytoplasmic function. Factors remaining on the mRNA, such as Y14 and Magoh, influence translation and localization of mature mRNPs.
Baseline requirements for mRNA export have been illustrated by a recent genome-wide analysis of mRNA export. Drosophila cells were depleted of export factors via RNA interference, and RNA levels were then assessed by microarray (36). In the absence of NXF1, p15, or UAP56, a large population of mRNA showed decreased cytoplasmic levels and, at early time points, levels in the cytoplasm had decreased more than in total RNA, suggestive of a block in mRNA export. Moreover, mRNA expression profiles of cells independently depleted of NXF1, p15, or UAP56 are markedly similar, indicating an underlying global pathway in mRNA biogenesis in which these three factors function (24, 36). However, although the roles of these proteins intersect, there may still be diversity in how each protein is recruited to different transcripts.
In fact, a recent study of a different system demonstrated that specific mRNAs are associated with distinct mRNA export factors (37). Hieronymus and Silver utilized a coimmunoprecipitation strategy to pull out either Yra1p or Mex67p from yeast extracts and analyzed mRNAs associated with these proteins by microarray. Surprisingly, these general export factors associated with distinct populations of mRNAs (37). Although other interpretations are also possible, these results are consistent with the idea that there may be different ways to get a shared set of export factors loaded onto mRNA and, depending on how factors get loaded onto a transcript, the association may be of different duration and/or stability.
The addition of a 5′ cap, splicing, polyadenylation, and cleavage all occur in close connection to transcription. Concurrent with the processing events, mRNAs are also packaged with a number of proteins specific to this class of RNA (Fig. 1). A significant subset of such proteins was originally classified as hnRNPs for their ability to associate with heterogeneous nuclear RNA (reviewed in reference 15). Interestingly, hnRNP A1 was later implicated in mRNA export, as a fragment of hnRNP A1 injected into Xenopus oocytes inhibited the export of dihydrofolate reductase mRNA (41). However, the extent to which hnRNP proteins function in export has not yet been elucidated. Mutation of the yeast protein Npl3p, which bears characteristics of both hnRNP and SR (serine-arginine)-type proteins, causes an mRNA export defect (52). Npl3p has been found in a complex with RNA polymerase II and is recruited to genes in a transcription-dependent manner (54).
Other proteins, not necessarily classified originally in the hnRNP category but loaded onto mRNA, have been functionally connected to both export and transcription. Yra1p and Sub2p display both genetic and physical interactions with all members of the yeast THO complex, a protein complex identified originally for a role in transcription elongation (9). REF and UAP56 along with the vertebrate counterparts of THO and a new protein of unknown function, Tex1, make up the TREX (transcription and export) complex (80). In yeast, specific TREX components associate with genes during transcription and, individually, their deletion results in nuclear poly(A)+ accumulation. Together, this suggests that TREX proteins may be important in mediating cotranscriptional recruitment of factors important in export. For example, one protein in the TREX complex, Hpr1p, is required for efficient targeting of Yra1p and Sub2p to genes undergoing active transcription (95). Therefore, cotranscriptional recruitment and splicing-dependent recruitment represent two broad mechanisms by which mRNA export factors can associate with RNA cargo. For instance, REF may be efficiently loaded onto specific RNA cargos via cotranscriptional targeting of the TREX complex and/or through splicing-dependent deposition of the EJC.
Another example of the connection between transcription and export is found in the DEAD box helicase Dbp5 (16). Dbp5 is localized at steady state to the cytoplasmic fibrils of the nuclear pore complex (NPC) and has been hypothesized to be involved in a terminal step of mRNA release from the NPC, possibly acting in a remodeling step to unwind mRNPs entering the cytoplasm (see reference 16 and references therein). On the other hand, yeast Dbp5p shuttles (38), and in C. tentans, Dbp5 associates with mRNA as early as during its transcription, accompanying the mRNA through the NPC and into the cytoplasm (96). Recent work with S. cerevisiae has shown that Dbp5p both genetically interacts with genes involved in early transcription events and physically interacts with multiple subunits of transcription factor TFIIH (16). Thus, Dbp5 may load onto mRNA cargo very early in biogenesis, although this does not preclude (and in fact may enhance) a later role for Dbp5 in remodeling the mRNP. Overall, much evidence is arising to support a link between mRNA synthesis and the effective recruitment of export factors to the nascent transcript.
An emerging theme is that coupling of mRNA cargo recognition to other important aspects of its physiology, such as transcription or splicing, is a general strategy to generate specificity in mRNA export, perhaps compensating for the generic nature of identifying features of mRNA export cargo. Likewise, proofreading mechanisms appear to be in place to rid the cell of any mRNAs that have been produced but not properly coupled to the next step. Notably, studies have identified functional interactions between the mRNA export factor Yra1p and Rrp6p and Rrp45p, components of the nuclear exosome, which is a protein complex containing multiple RNA exonucleases (95). Failure to correctly form mRNPs results in the nuclear retention and degradation of aberrant mRNA species, serving as an additional level of control to regulate export and ultimately efficient gene expression (recently reviewed in references 43, 68, and 82). This complicated network interconnecting transcription, export, and RNA stability additionally underscores the importance of having functional read-outs for export to complement the bulk poly(A)+ accumulation assay.
NPCs span the nuclear envelope and serve as gateways of communication between the nucleus and cytoplasm. The pore is a huge structure with ∼30 individual nuclear pore proteins or nucleoporins (Nups) present several times, creating octagonal symmetry. The pore also has asymmetric features on its nuclear and cytoplasmic faces (for recent reviews, see references 6 and 83). Although much of the process of mRNA export is being deciphered, there is still little known about how mRNPs interface with pore machinery. Some recent studies have focused on the roles of proteins that are closely associated with the pore, such as Gle1 and RAE1/Gle2. Gle1 is essential for mRNA export in both yeast and human cells (13, 62, 63, 91), and hGle1 is a dynamic factor that shuttles between nucleus and cytoplasm (47). The shuttling domain of hGle1 acts as a dominant-negative export inhibitor of both bulk poly(A)+ RNA and specific mRNA transcripts (47). Docking of hGle1 at the NPC was recently shown to depend on an interaction with the pore protein Nup155 (67).
Murine RAE1 is essential; however, cells from mice bearing targeted disruption of RAE1 do not have a detectable defect on bulk mRNA export (1). In contrast, RAE1 deletion in yeast results in nuclear accumulation of poly(A)+ RNA (61). Although there appear to be redundant factors in vertebrates, hRAE1 interacts with NXF1 and the nucleoporin Nup98, as well as with mRNA itself (51), and has been speculated to be involved in delivering mRNA cargo-receptor complexes to Nup98 (7). Nup98, in turn, has been implicated through antibody inhibition studies in the export of mRNA as well as other classes of RNA (66). Nup98 shares similarity with yeast nuclear pore proteins Nup145, Nup116, and Nup100. Deletion of yNup145 causes the nuclear accumulation of poly(A)+ RNA (17).
Vertebrate pore proteins have not been exhaustively screened and individually tested for roles in mRNA export. However, along with Nup98, five other vertebrate pore proteins, Nup153, Nup160, Nup133, Tpr, and CAN/Nup214, have so far been implicated in the export of mRNA (Fig. 2). Mouse embryos deficient in CAN/Nup214 not only show arrest in the G2 phase of the cell cycle but also demonstrate nuclear accumulation of poly(A)+ RNA (88). Nup159/Rat7, the yeast orthologue of CAN/Nup214, is similarly implicated in mRNA export, with a temperature-sensitive mutation causing very rapid onset of accumulation of poly(A)+ RNA in the nucleus (26). CAN/Nup214 associates with the mRNA export factor Dbp5, an interaction conserved from yeast to vertebrates (38, 72). In addition, CAN/Nup214 is the only vertebrate nucleoporin with a steady-state localization exclusively on the cytoplasmic side of the pore that has been implicated in mRNA export thus far.
Distribution and dynamics of pore proteins and associated factors implicated in mRNA export. Nup153 and Nup98 are both dynamically associated with the nuclear pore in a manner dependent on ongoing transcription. However, in the case of Nup153, there is also evidence for a stable population, which is schematically illustrated here proximal to the inner nuclear membrane. The presence of distinct populations of Nup153 is consistent with epitope exposure of this protein: different regions are exposed at the distal and proximal ends of the pore basket. An extended conformation of Nup153 at the pore is an alternative explanation for epitope distribution. Regardless of exactly how Nup153 is arranged at the pore basket, there is evidence that the C-terminal region of this pore protein can extend into the cytoplasm, although Nup153 does not appear to be released from this face of the pore. In contrast, Nup98 exists in equilibrium with a cytoplasmic pool and is known to interact with components of both sides of the pore. RAE1/Gle2 is a partner protein of Nup98. Both Nup153 and Nup98 associate with the Nup107-160 complex, a stable component of the pore. Tpr is also a component of the nuclear pore basket and relies on interaction with Nup153 for correct localization. CAN/Nup214 is localized to fibrils extending from the cytoplasmic ring of the pore and is a docking site for the dynamic DEAD box helicase, Dbp5.
The nucleoporin Nup153 has a complicated localization pattern but is found primarily at the nuclear pore basket (reference 19 and references therein) (Fig. 2; see also below). Overexpression of Nup153 fragments in cultured cells causes nuclear poly(A)+ accumulation (5), and perturbation of Nup153 function in Xenopus oocytes blocks specific RNA species, including mRNA, from being exported (87). Independent overexpression of either Nup160 or Nup133 fragments in culture also causes the nuclear accumulation of poly(A)+ RNA (89). Nup160 is found in a complex (termed the Nup107-160 complex) with Nup133, Nup107, and Nup96, which parallels a network of nucleoporins in yeast (83, 89). The Nup107-160 complex associates with both Nup153 and Nup98. However, whereas the Nup107-160 complex is a stable component of the pore (90), Nup98 and Nup153 are both mobile pore proteins (11, 29). Studies using FRAP (fluorescence recovery after photobleaching) have demonstrated that Nup98 is highly dynamic and its mobility is dependent on ongoing transcription by RNA polymerases I and II (29, 31). Photobleaching studies indicated that Nup153 is also highly mobile (11, 30). As seen with Nup98, mobility of Nup153 is arrested in the presence of transcription inhibitors, although transcription-dependent dynamics are mediated by distinct domains within each protein (30). Transcription could be critical because the dynamic association of these nucleoporins with the pore is coupled to movement of RNA cargo through the pore. Given the links between transcription and export, it is also possible that these mobile pore proteins load onto RNAs destined for the pore at the time of transcription and require such association for ongoing mobility (Fig. 1). Although much remains to be elucidated, Nup98 and Nup153 are prime candidates for coupling the production of mRNA to its transport into the cytoplasm.
A novel RNA binding domain identified within Nup153 (14) preferentially interacts with unstructured RNA, independent of orientation (3). Such features match the criteria that define an mRNA identity element. The RNA binding domain within Nup153, therefore, may be involved in the interface between this pore protein and mRNA during the export process. Another possibility is that Nup153 aids in recognizing RNAs that have an anomalous stretch of unstructured RNA. In either case, understanding the functional contribution of RNA binding will go hand-in-hand with integrating other information about Nup153 since the RNA binding domain (amino acids 250 to 400) overlaps binding sites for the Nup107-160 complex (amino acids 1 to 339) (89) and Tpr (amino acids 228 to 439) (34). Surprisingly, in light of the rapid dynamics of Nup153, Tpr relies on this interaction with Nup153 for pore localization (34). If this interaction facilitates anchorage rather than delivery of Tpr, it would suggest that there is a population of Nup153 stably associated with the pore. The existence of such a nonmobile fraction of Nup153 is also supported by photobleaching studies (11, 30). Indeed, multiple populations of Nup153, present at different parts of the pore and in the nuclear interior itself, may be part of the explanation for how the N-terminal region of this protein can interact with so many partners. In terms of RNA export, the functional connection between Nup153 and Tpr is not well defined, although Tpr has also been implicated in the export of both protein and RNA in metazoan cells (4, 23, 75).
Studies with yeast have determined that Mlp1p and Mlp2p, proteins with similarity to mammalian Tpr, have a role in mRNA export. Overexpression of Mlp1p causes poly(A)+ RNA nuclear accumulation (50). In addition, the yeast hnRNP proteins Npl3p and Nab2p also interact with Mlp1p and may facilitate Mlp function. For example, Nab2p, previously shown to be required for poly(A)+ export in yeast (28), accumulates in the nucleus of cells overexpressing Mlp1p (27). In an intriguing recent development, Mlp interactions with the exosome component Rrp6p have also been determined (A.Corbett, personal communication), suggesting that Mlps could participate in a proofreading step that ensures export occurs only for properly formed mRNPs. The connection between the exosome and transport is further underscored by the observation that, in yeast, inhibition of RNA export leads to exosome (Rrp6p)-dependent accumulation of a heat shock transcript near its site of synthesis (85). The extent to which pore proteins and the exosome machinery are functionally connected in vertebrates has not yet been addressed. In this regard, however, it is intriguing that, upon heat shock, Drosophila Tpr has been seen to accumulate at a particular chromosomal puff region (93D), a heat shock locus encoding an RNA (hsr-[omega]) that is not exported (98). Future studies are needed to address the full significance of this localization as well as its relationship to the exosome.
In recent years, several models to explain the mechanism of movement through the pore have been proposed (18, 22, 70, 92). In each, the FG repeat regions found in several nucleoporins play a prominent role, both in contributing to an exclusion barrier as well as in serving as binding sites for cargo-receptor complexes. Consistent with this, NXF1 directly interacts with the FG repeat domains of several nucleoporins in vitro (2). A challenge in thinking about the mechanisms involved in mRNA translocation through the pore is that mRNPs represent a large and heterogeneous type of cargo and, further, appear to undergo remodeling in conjunction with transport. The large Balbiani ring mRNP of C. tentans has been shown by electron microscopy to first dock and then unwind as it traverses the pore (12, 49). Elegant immunoelectron microscopy studies have gone on to illustrate that certain proteins are shed from the mRNP, while others accompany the RNA through the pore (reviewed in references 12 and 15). Complicating things further, the nuclear pore basket itself has been observed to adopt different conformations when the Balbiani ring mRNA is traversing the pore. While this large RNA may utilize some specialized mechanisms to promote export, other features of its export are predicted to fit a general paradigm, raising the question of how dynamics of the nuclear pore basket fit into mRNA export. The dynamic nature of specific pore basket components themselves (Nup98 and Nup153), as well as the sensitivity of such mobility to the transcriptional status of the cell, suggests that basket remodeling may normally be ongoing in a manner linked to RNA trafficking. New information derived from reconstructing images of native NPCs suggests that the distal ring of the pore basket is not an open hole but rather a dense structure (76), further underscoring the necessity of remodeling events for this point of entry. Although not mutually exclusive with the idea of pore remodeling, an alternative point of entry into the pore, in between the fibers of the pore basket, has also been proposed (40). Much work is still needed to understand how mRNA enters and translocates through the pore. Future approaches that provide high-resolution real-time imaging as well as more precise functional assays are sure to yield a very interesting story about how the complicated network of mRNA biogenesis connects with translocation through the nuclear pore and the downstream fate of the mRNA.
During the review of the manuscript, two papers demonstrating further connections between pore proteins and distinct steps in mRNA biogenesis were published. Mlplp was found to play a role in retention of unspliced mRNA. Nup60p, a binding partner of Mlplp, was also implicated in this quality control process (V. Galy, O. Gadal, M. Fromont-Racine, A. Romano, A. Jacquier, and U. Nehrbass, Cell 116:63-73, 2004). Forler et al. found that RNAi knock-down of Nup358/RanBP2 in Drosophila cells led to nuclear poly(A)+ accumulation. They also independently targeted Nup214 and saw a similar effect on mRNA. However, reduction of Nup358 and not Nup214 led to mislocalization of NXF1, suggesting that Nup358 plays a key role in keeping NXF1 concentrated at the cytoplasmic face of the pore (D. Forler, G. Rabut, F. D. Ciccarelli, A. Herold, T. Kocher, R. Niggeweg, P. Bork, J. Ellenberg, and E. Izaurralde, Mol. Cell. Biol. 24:1155-1167, 2004).
We are grateful to Anita Corbett and Jennifer Ball for critical review of the manuscript. We especially thank Diana Lim for design and preparation of figures. We also thank Maureen Powers for helpful discussion and Anita Corbett for communication of unpublished work. We apologize to anyone whose work was not cited due to space limitations.
C.D. is supported by a Ruth L. Kirschstein NRSA individual fellowship from the NIH. This work was also supported by NIH grant GM61275 (to K.S.U.).
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Leave granted in S.L.P(C) No. 28304 of 2015.
These two appeals revisit the question of the correct construction of Section 24(2) of The Right to Fair Compensation and Transparency in Land Acquisition, Rehabilitation and Resettlement Act, 2013 (hereinafter referred to as "the 2013 Act"). We are constrained to observe that we are hearing these matters despite the fact that the law has been settled in Pune Municipal Corporation v. H.M. Solanki, 2014 (3) SCC 183, which is now stare decisis in that it has been followed in a large number of judgments.
3. The facts of the present case are as follows. A Notification under Section 4 of the Land Acquisition Act, 1894, was issued on 24th October, 1961, stating that the public purpose for acquisition was the planned development of Delhi. This Notification covered large tracts of land in and around Delhi. In this case, we are concerned with 33 bighas and 1 biswa of land in the Vasant Kunj area of New Delhi.
This Section 4 Notification was followed by a Notification under Section 6 dated 4th January, 1969, which in turn, was followed by notices issued under Section 9 on 26th April, 1983. An award relating to the aforesaid land was then made by the Land Acquisition Collector, New Delhi, only on 12th December, 1997. Possession of the said land, being an open piece of land, was taken by a Panchnama dated 27th January, 2000.
An affidavit that has been filed by the Commissioner, Land Management, Delhi Development Authority in this Court, pursuant to an order of this Court dated 17th April, 2015, discloses that the requisite compensation for taking over the said land was deposited by the DDA with the Land Acquisition Collector only in the year 2002. The said affidavit goes on to state that since the land had been sold to Respondent Nos. 3 to 5 in the present case, there was a dispute as to who would receive compensation and that, therefore, compensation could neither be paid nor tendered.
4. On the eve of the coming into force of the 2013 Act (on 1st January, 2014), an application styled as a Petition under Article 227 of the Constitution of India was made by the Land Acquisition Collector in the High Court of Delhi on 27th December, 2013, requesting the High Court of Delhi to accept cheques towards compensation amounts under the award dated 12th December, 1997, stating that non-deposit of compensation on or before 31st December, 2013 would adversely affect the acquisition proceedings inasmuch as the proceedings might lapse in view of the fact that the 2013 Act has been notified to take effect from 1st January, 2014. An order dated 30th December, 2013 was passed by the High Court on this application stating that the petition stands disposed of, recording that without prejudice to the rights and contentions of the land owners, the cheques tendered in each petition would be treated as a tender to the court of the learned Additional District Judge, Delhi as on today i.e. 30th December, 2013.
"5. Without going into the controversy with regard to physical possession, this much is clear that the award was made more than five years prior to the commencement of the 2013 Act and the compensation has also not been paid. The necessary ingredients for the application of Section 24(2) of the 2013 Act, as interpreted by the Supreme Court and this court in the following decisions, stand satisfied: Pune Municipal Coporation and Anr. v. H.M. Solanki, 2014 (2) SCC 183, Union of India & Ors. V. Shiv Raj & Ors., (2014) 6 SCC 564. Sree Balaji Nagar Residential Association v. State of Tamil Nadu & Ors.: Civil Appeal No. 8700/2013. Surender Singh v. Union of India & Others: W.P.(C) No. 2294/2014 decided on 12.09.2014 by this Court; and Gyanender Singh & Ors. V. Union of India & Ors., W.P.(C) No. 1393/2014, 10.09.2014.
6. As a result, the petitioners are entitled to a declaration that the said acquisition proceedings initiated under the 1894 Act in respect of the subject lands are deemed to have lapsed. It is so declared."
6. The present appeals have, therefore, been filed by both the Land Acquisition Collector and the DDA.
7. Shri Amarendra Sharan, Senior Advocate, appearing for the DDA and Ms. Rachna Srivastava, Advocate, appearing for the Land Acquisition Collector, have argued before us that Pune Municipal Corporation needs to be revisited on essentially two grounds. The first is that at least as far as Delhi is concerned, it is governed by a Standing Order of 26th June, 1909 as amended up to date, in which one method of making payment under Section 31 of the Land Acquisition Act is by deposit in the treasury. The distinguishing feature of this case is, therefore, that unlike in Pune Municipal Corporation, deposit in a treasury is a recognized mode of making payment for the purpose of Section 31 of the Land Acquisition Act, and that this being the case, it is clear that Pune Municipal Corporation would not, therefore, apply to the facts of the present case.
A second argument was also made by both the learned counsels to the effect that Pune Municipal Corporation did not notice that since possession had been taken in the facts of the present case, in the year 2000, vesting of the land in the State had already taken place and the original owner had been divested of his title. This being the case, the acquisition proceedings being over in the year 2000, no question of lapse of a proceeding that is already over can possibly take place in the year 2014 after the enactment of the 2013 Act. For the aforesaid proposition, the learned counsel relied upon Satendra Prasad Jain v. State of U.P., (1993) 4 SCC 369.
They further argued that, in the present case, a subsequent purchaser had come into the picture by a registered sale deed dated 23rd June, 1992. This being the case, it is clear that the State was in a dilemma as to who should be paid compensation, and it is for this reason that compensation was neither tendered nor paid after the award. For this purpose, they relied upon Meera Sahni v. Lt. Governor of Delhi & Ors., (2008) 9 SCC 177.
8. The submissions of both the learned counsels were rebutted by Shri A.K. Sanghi, Senior Advocate, appearing on behalf of the original owner and Shri V. Giri, appearing on behalf of the subsequent purchasers. Both the learned counsels emphasized the fact that compensation money had neither been tendered or paid in accordance with Section 31 of the Land Acquisition Act. They further went on to state that even possession had not been taken in accordance with law as no notice had been issued to the land owners before taking possession and, that therefore, this was a case which was covered by both contingencies mentioned in Section 24(2) of the 2013 Act.
They also argued that it is too late in the day to go back on the ratio of Pune Municipal Corporation, which squarely applies on the facts of the present case, as it has now been followed in a catena of judgments. 9. Having heard the arguments on both sides, it is necessary to first set out the relevant provisions of the Land Acquisition Act.
Provided that no award shall be made by the Collector under this sub- section without the previous approval of the appropriate Government or of such officer as the appropriate Government may authorize in this behalf: Provided further that it shall be competent for the appropriate Government to direct that the Collector may make such award without such approval in such class of cases as the appropriate Government may specify in this behalf.
(4) Notwithstanding anything contained in the Registration Act, 1908 (16 of 1908), no agreement made under sub-section (2) shall be liable to registration under that Act.
(1) Such award shall be filed in the Collector's office and shall, except as hereinafter provided, be final and conclusive evidence, as between the Collector and the persons interested, whether they have respectively appeared before the Collector or not, of the true area and value of the land, and the appointment of the compensation among the persons interested.
16. Power to take possession. - When the Collector has made an award under section 11, he may take possession of the land, which shall thereupon vest absolutely in the Government, free from all encumbrances.
(1) On making an award under section 11, the Collector shall tender payment of the compensation awarded by him to the persons interested entitled thereto according to the award and shall pay it to them unless prevented by some one or more of the contingencies mentioned in the next sub-section.
(3) Notwithstanding anything in this section the Collector may, with the sanction of the appropriate Government instead of awarding a money compensation in respect of any land, make any arrangement with a person having a limited interest in such land, either by the grant of other lands in exchange, the remission of land-revenue on other lands held under the same title, or in such other way as may be equitable having regard to the interests of the parties concerned.
34. Payment of interest - When the amount of such compensation is not paid or deposited on or before taking possession of the land, the Collector shall pay the amount awarded with interest thereon at the rate of nine per centum per annum from the time of so taking possession until it shall have been so paid or deposited: Provided that if such compensation or any part thereof is not paid or deposited within a period of one year from the date on which possession is taken, interest at the rate of fifteen per centum per annum shall be payable from the date or expiry of the said period of one year on the amount of compensation or part thereof which has not been paid or deposited before the date of such expiry."
10. The scheme of the Land Acquisition Act, in so far as the making of award and the payment of compensation to persons interested, is as follows. On the day fixed, the Collector after the inquiry that is contemplated under Section 11, has to make an award which must contain the necessary ingredients mentioned in Section 11. As soon as the award is made, under Section 12(2) of the Act, the Collector is to give immediate notice of the award to such of the persons interested as are not present personally.
This provision, when read with Section 31 of the Act, makes it clear that the statutory scheme is that the Collector is to tender payment of compensation awarded by him to the persons who are interested and entitled thereto, according to the award, on the date of making the award itself. It is therefore, clear that under the statutory scheme, the Collector must be armed with the amount of compensation payable to persons interested as soon as the award is made. Such persons have to be paid the sum mentioned in the award, it being well settled that the award is only an offer which may be accepted or rejected by the claimants.
If accepted, whether under protest or otherwise, it is the duty of the Collector to make payment as soon as possible after making the award. It is only in a situation where the persons interested refuse consent to receive monies payable, or there be no person competent to alienate the land, or if there be any dispute as to title to receive compensation or its apportionment, is the Collector to deposit the amount of compensation in the reference court. It is only after these steps have been taken that the Collector may take possession of the land, which shall thereupon vest absolutely in the Government free from all encumbrances.
The Act further makes it clear, on a reading of Section 34, that where such compensation is neither paid or deposited on or before taking possession of the land, interest is payable at the rate of 9 per cent per annum for one year and 15 per cent per annum thereafter. This is because a person becomes divested of both possession and title to his property without compensation having been paid or deposited, as the case may be.
This statutory scheme has been adverted to in some of the decisions of this Court. In New Reviera Coop. Housing Society v. Special Land Acquisition Officer, (1996) 1 SCC 731 at para 3, this Court held: "...Once the award has been made and compensation has been deposited or paid under Section 31 of the Act, the Land Acquisition Officer is entitled to take possession and the possession thereby taken stands vested in the State under Section 16 of the Act free from all encumbrances..."
"... What the legislature intended was to make the aggregate amount under Section 23 of the Act to reach the hands of the person as and when the award is passed, at any rate as soon as he is deprived of the possession of his land. Any delay in making payment of the said sum should enable the party to have interest on the said sum until he receives the payment. Splitting up the compensation into different components for the purpose of payment of interest under Section 34 was not in the contemplation of the legislature when that section was framed or enacted."
In Bangalore Development Authority v. R. Hanumaiah, (2005) 12 SCC 508 at para 47, this Court held: "...Section 31 contemplates that on making of an award under Section 11 the Collector shall tender amount of compensation awarded by him to the person interested and entitled thereto according to the award and shall pay to them unless prevented by any one or more of the contingencies mentioned in the subsequent clauses. None of those contingencies arose in the present case. Thus, once the amount was tendered and paid the acquisition process was complete. After making the award under Section 11 the Collector can take possession of the land under Section 16 which shall thereupon vest absolutely in the Government free from all encumbrances.
In the instant case, after making the payment in terms of the award, possession was taken. The acquisition process stood completed.
Provided that where an award has been made and compensation in respect of a majority of land holdings has not been deposited in the account of the beneficiaries, then, all beneficiaries specified in the notification for acquisition under section 4 of the said Land Acquisition Act, shall be entitled to compensation in accordance with the provisions of this Act."
12. Section 24(1) begins with a non-obstante clause and covers situations where either no award has been made under the Land Acquisition Act, in which case the more beneficial provisions of the 2013 Act relating to determination of compensation shall apply, or where an award has been made under Section 11, land acquisition proceedings shall continue under the provisions of the Land Acquisition Act as if the said Act had not been repealed.
(e) The fatality is pronounced by stating that the said proceedings shall be deemed to have lapsed, and the appropriate Government, if it so chooses, shall, in this game of snakes and ladders, start all over again.
14. The picture that therefore emerges on a reading of Section 24(2) is that the State has no business to expropriate from a citizen his property if an award has been made and the necessary steps to complete acquisition have not been taken for a period of five years or more. These steps include the taking of physical possession of land and payment of compensation.
What the legislature is in effect telling the executive is that they ought to have put their house in order and completed the acquisition proceedings within a reasonable time after pronouncement of award. Not having done so even after a leeway of five years is given, would cross the limits of legislative tolerance, after which the whole proceeding would be deemed to have lapsed. It is important to notice that the Section gets attracted if the acquisition proceeding is not completed within five years after pronouncement of the award.
This may happen either because physical possession of the land has not been taken or because compensation has not been paid, within the said period of five years. A faint submission to the effect that 'or' should be read as 'and' must be turned down for two reasons. The plain natural meaning of the sub-section does not lead to any absurdity for us to replace language advisedly used by the Legislature.
Secondly, the object of the Act, and Section 24 in particular, is that in case an award has been made for five years or more, possession ought to have been taken within this period, or else it is statutorily presumed that the balance between the citizen's right to retain his own property and the right of the State to expropriate it for a public purpose gets so disturbed as to make the acquisition proceedings lapse. Alternatively, if compensation has not been paid within this period, it is also statutorily presumed that the aforesaid balance gets disturbed so as to free such property from acquisition.
"On the other hand, on behalf of the Corporation and so also for the Collector, it is argued that the award was made by the Special Land Acquisition Officer on 31-1-2008 strictly in terms of the 1894 Act and on the very day the landowners were informed regarding the quantum of compensation for their respective lands. Notices were also issued to the landowners to reach the Office of the Special Land Acquisition Officer and receive the amount of compensation and since they neither received the compensation nor any request came from them to make reference to the District Court under Section 18, the compensation amounting to Rs 27 crores was deposited in the Government treasury.
16. After setting out Section 24(2), the Court went on to hold: "Section 24(2) also begins with non obstante clause. This provision has overriding effect over Section 24(1). Section 24(2) enacts that in relation to the land acquisition proceedings initiated under the 1894 Act, where an award has been made five years or more prior to the commencement of the 2013 Act and either of the two contingencies is satisfied viz.
(ii) the compensation has not been paid; such acquisition proceedings shall be deemed to have lapsed.
On the lapse of such acquisition proceedings, if the appropriate Government still chooses to acquire the land which was the subject-matter of acquisition under the 1894 Act then it has to initiate the proceedings afresh under the 2013 Act. The proviso appended to Section 24(2) deals with a situation where in respect of the acquisition initiated under the 1894 Act an award has been made and compensation in respect of a majority of landholdings has not been deposited in the account of the beneficiaries then all the beneficiaries specified in the Section 4 notification become entitled to compensation under the 2013 Act.
(iii) there is dispute as to the title to receive compensation or as to the apportionment of it. If due to any of the contingencies contemplated in Section 31(2), the Collector is prevented from making payment of compensation to the persons interested who are entitled to compensation, then the Collector is required to deposit the compensation in the court to which reference under Section 18 may be made.
Simply put, Section 31 of the 1894 Act makes provision for payment of compensation or deposit of the same in the court. This provision requires that the Collector should tender payment of compensation as awarded by him to the persons interested who are entitled to compensation. If due to happening of any contingency as contemplated in Section 31(2), the compensation has not been paid, the Collector should deposit the amount of compensation in the court to which reference can be made under Section 18.
The mandatory nature of the provision in Section 31(2) with regard to deposit of the compensation in the court is further fortified by the provisions contained in Sections 32, 33 and 34. As a matter of fact, Section 33 gives power to the court, on an application by a person interested or claiming an interest in such money, to pass an order to invest the amount so deposited in such Government or other approved securities and may direct the interest or other proceeds of any such investment to be accumulated and paid in such manner as it may consider proper so that the parties interested therein may have the benefit therefrom as they might have had from the land in respect whereof such money shall have been deposited or as near thereto as may be.
While enacting Section 24(2), Parliament definitely had in its view Section 31 of the 1894 Act. From that one thing is clear that it did not intend to equate the word "paid" to "offered" or "tendered". But at the same time, we do not think that by use of the word "paid", Parliament intended receipt of compensation by the landowners/persons interested. In our view, it is not appropriate to give a literal construction to the expression "paid" used in this sub-section [sub-section (2) of Section 24]. If a literal construction were to be given, then it would amount to ignoring the procedure, mode and manner of deposit provided in Section 31(2) of the 1894 Act in the event of happening of any of the contingencies contemplated therein which may prevent the Collector from making actual payment of compensation.
The 1894 Act being an expropriatory legislation has to be strictly followed. The procedure, mode and manner for payment of compensation are prescribed in Part V (Sections 31-34) of the 1894 Act. The Collector, with regard to the payment of compensation, can only act in the manner so provided. It is settled proposition of law (classic statement of Lord Roche in Nazir Ahmad [Nazir Ahmad v. King Emperor, (1935-36) 63 IA 372 : (1936) 44 LW 583 : AIR 1936 PC 253 (2)] ) that where a power is given to do a certain thing in a certain way, the thing must be done in that way or not at all. Other methods of performance are necessarily forbidden. Now, this is admitted position that award was made on 31-1-2008.
Notices were issued to the landowners to receive the compensation and since they did not receive the compensation, the amount (Rs 27 crores) was deposited in the Government treasury. Can it be said that deposit of the amount of compensation in the Government treasury is equivalent to the amount of compensation paid to the landowners/persons interested?
We do not think so. In a comparatively recent decision, this Court in Agnelo Santimano Fernandes [Ivo Agnelo Santimano Fernandes v. State of Goa, (2011) 11 SCC 506 : (2011) 4 SCC (Civ) 268] , relying upon the earlier decision in Prem Nath Kapur [Prem Nath Kapur v. National Fertilizers Corpn. of India Ltd., (1996) 2 SCC 71] , has held that the deposit of the amount of the compensation in the State's revenue account is of no avail and the liability of the State to pay interest subsists till the amount has not been deposited in court. From the above, it is clear that the award pertaining to the subject land has been made by the Special Land Acquisition Officer more than five years prior to the commencement of the 2013 Act.
"71. Payment of compensation when made - As soon as the award has been announced the acquiring officer will proceed to pay the compensation awarded to those persons who are present and who accept the award. Sufficient notice should be given to enable all payees to assemble at the place where they will receive their dues but no time should be wasted on useless endeavours to secure the attendance of absentees.
A note shall be made of the names of those persons who refused to accept the amount awarded or who accept it under protest. Much trouble will be avoided if the principle that payment of compensation should be made at the time of award, is strictly observed. Most of the persons interested will then be present and immediate payment will save them the necessity of making frequent journeys to the tehsil. It will usually be found of advantage to draw in advance a sum sufficient to cover the probable amount of the award and to make payments against this especially when the award is announced at a place distant from the headquarters.
73. Statement to be forwarded to the Accountant General - When an award is made under Section 11 of the Act the acquiring officer shall have a statement prepared in the following Form marked AA showing the amounts payable to each person under the award and shall, on the day the award is made, forward a copy of this statement signed by him to the accountant general or other audit officer, with whom he is in account and the Deputy Commissioner concerned simultaneously with a certificate that the land has been taken possession of and mutated in favour of Government fiving the number and date of the attested mutation.
On the basis of this certificate, the Deputy Commissioner may forward a proposal to the Financial Commissioner for sanctioning reduction of land revenue under Paragraph 79 infra. Before signing the copy the Officer should carefully satisfy himself that it correctly shows the amounts due under the award and should himself enter the total of column 6 of the statement in words both in the original and copy. Subsidiary statement in Form AA below, giving particulars regarding the acceptance by the persons concerned of the amounts entered in column 6 of the Award statement should also be furnished to the auditing officer as soon as possible.
If the subsidiary statement is not complete on the day that the award is made, the necessary entries in column 7 of the statement in Form A will be made in the auditing office on receipt of the statement in Form AA.
Note - In noting these particulars in the award statement, it may be sufficient to enter the letter a, b, c or d as the case may be in column 7 of the statement when the whole amount of the award is shown in one of the four sub-columns a, b, c or d in the statement.
75. Direct payments (V) By treasury deposit - In giving notice of the award under Section 12(2) and tendering payment under Section 31(1) to such of the persons interested as were not present personally or by their representatives when the award was made, the officer shall require them to appear personally or by representatives by a certain date to receive payment of the compensation awarded to them, intimating also that no interest will be allowed to them if they fail to appear, if they do not appear and do not apply for a reference to the civil court under Section 18, the officer shall after any further endeavours to secure their attendance that may seem desirable, cause the amounts due to be paid to the treasury as revenue deposited payable to the persons to whom they are respectively due and vouched for in the Form marked E below. The officer shall also give notice to the payees of such deposits, specifying the treasury in which the deposit has been made.
When then payees ultimately claim payment of sums placed in deposit, the amounts will be paid to them in the same manner as ordinary revenue deposit. The officer should, as far as possible, arrange to make the payments due in or near the village to which the payee belong in order that the number of un-disbursed sums to be placed in deposits on account of non- attendance may be reduced to a minimum. Whenever payment is claimed through a representative whether before or after deposit of the amount awarded, such representative must have legal authority for receiving the compensation on behalf of his principal.
Serial Number in award statement No.
Note - this form should be used when the amounts of compensation due are sent to treasury in the absence of proprietors who have failed to present themselves for payment.
18. Far from the aforesaid Standing Order coming to the assistance of the appellants, it is clear that the said Standing Order fleshes out Section 31 of the Land Acquisition Act by insisting that compensation must be paid as soon as the award is announced, vide paragraph 71. Sufficient notice must be given to enable all payees to assemble at a place where they will receive their dues immediately. It is emphasized by the said paragraph that much trouble will be avoided if the principle that payment of compensation should be made at the time of the award is strictly observed. Also, it is important that the authorities draw in advance a sum sufficient to cover the probable amount of the award and to make payments.
19. Paragraph 73 makes it clear that payment may be accepted either without protest or under protest, and Paragraph 74 makes it clear that there are five methods of making payment. The first four methods are all methods strictly in consonance with Section 31 of the Land Acquisition Act in that they are all direct payments that have to be made to persons ready to accept compensation. This is clear from a reading of sub-paragraphs (I) to (IV) of paragraph 74.
Even the second method, which is payment by order on the treasury, is a direct method of payment in cases where no officer is specially deputed for acquisition of land. In such cases instead of making a direct payment, a receipt is countersigned making it immediately payable at the treasury to the payee. Otherwise, in certain circumstances, payment is to be made by money order and/or by cheque. When we come to paragraph (V), it is clear that payment is made into the treasury only when persons who are served notice under Section 12(2) are not present personally at the time the award is delivered.
Even though they may not appear at that stage, the officer shall require them to appear personally or by representatives by a certain date to receive payment of compensation awarded. It is only if they fail to appear after such an intimation, and if the officer, after further endeavours to secure their attendance, cannot so secure their attendance, that amounts due are to be paid to the treasury as revenue deposited payable to persons to whom they are due.
It is clear, therefore, that sub-para (V), when read in its proper perspective, is not a separate mode of payment by itself as is contended by learned counsel for the appellants. It is a residuary mode of payment after all necessary efforts have been made by the authorities to secure the attendance of the persons entitled to compensation, and it is only after all such methods have failed that, as a last resort, the money is then to be deposited in the treasury. In any case, such deposit in the treasury is referable only to Section 31(1) and cannot ever be a substitute for deposit before the reference court as provided under Section 31(2) of the Land Acquisition Act, which applies in the circumstances mentioned in the aforesaid sub-section. We are, therefore, of the opinion that no distinction between the facts of this case and the facts in Pune Municipal Corporation can be drawn on this ground, and the ratio of Pune Municipal Corporation will apply on all fours to the facts of the present case.
20. On facts, it is clear that neither tender, that is offer to the original claimant nor payment has been made in the manner provided by Section 31 read with Standing Order No. 28 of 1909. In the present case, as has been admitted in the affidavit filed in this Court, the DDA was not ready with compensation payable on the day the award was pronounced, but only handed over such compensation to the Land Acquisition Collector five years after the award was pronounced, that is, in 2002. The Land Acquisition Collector, in its turn, did nothing whatsoever to offer the said sum or pay it to the original owners.
On the contrary, by moving an application on the eve of the coming into force of the 2013 Act, and by depositing the said amount of compensation paid to it in the year 2002 only on 30th December, 2013, it is clear that the aforesaid mandatory provision and procedure were not followed by the authorities. The present original land owners' lands were notified for acquisition on 24th October, 1961, of which possession was taken four decades later, in 2000; after which the land owners have yet to see the colour of the paltry amount of compensation offered which has neither been tendered nor paid to them.
"3. Taking-over possession of notified land: As soon as the award is announced, the Land Acquisition Collector shall compulsorily issue notice to the interested persons u/s 12 of the L. A. Act and the service of notice shall be kept in records and shall also submit a demand of the compensation amount to the Land & Building Department with a copy to the DDA /intending agency within 30 days of the announcement of the award. The Land & Building Department shall forward the demand to the DDA within 7 days. DDA/other agency will release the payment to L & B Deptt. within 30 days after receipt of the communication from the L & B Department/ LAC as the case may be. As soon as the money is received by the LAC, notice u/s 12(2) shall be issued.
The LAC will takeover the possession of the land and handover the same to the DDA/intending department. The Land Acquisition Collector shall not take possession of the acquired land unless & until the compensation amount is received by him from the intending department. It has been noticed that in a large number of cases, the LACs have not taken over the possession of the notified land as possession could not be taken by the DDA due to the fact that the land is heavily built up and in some cases, some unauthorized colonies have come up which are under consideration of Govt. of India for regularization. In all such cases, the LACs shall prepare a separate list village wise and shall be submitted to competent authority for taking a policy decision.
4. Payment of Compensation/ Enhanced Compensation: On receipt of the amount of compensation from DDA/Requisitioning Agency and on taking the possession of the land, the Land Acquisition Collector shall send a reference/ letter within 15 days to the interested persons for collecting the payment of compensation. The Land Acquisition Collector will make the payment of the compensation within 60 days to the land owner. In case of any dispute, the Land Acquisition Collector will refer the matter to the ADJ Court u/s 30 immediately after expiry of the 60 days. If interested person is not coming forward for taking compensation amount and payment cannot be made within 60 days then compensation amount should be deposited in the court u/s 31 within next 15 days."
22. A cursory reading of these paragraphs will show that it is only pursuant to judicial orders that the State wakes up from its slumber. It is important to note that a notice of award under Section 12(2) to persons interested can only be issued after money is received by the Land Acquisition Collector, and that the said Collector shall not take possession of land unless and until compensation amount is received by him. Further, actual payment to land owners must be made latest within a period of 60 days. It is high time that the State realizes that persons whose property is expropriated need to be paid immediately so as to rehabilitate themselves.
Also, it cannot be forgotten that the amount usually offered by way of an award of a Land Acquisition Collector under the 1894 Act is way below the real market value, which is only awarded and paid years later when the reference proceedings culminate in judgments of the High Courts and of this Court.
23. We now come to the argument of Shri Sharan that, in any case, on the facts of this case, the pitch is queered by the presence of subsequent purchasers. As has been pointed out in Meera Sahni's case [(2008) 9 SCC 177], that the moment Section 4 of the Delhi Lands (Restrictions on Transfer) Act, 1972, applies, a sale subsequent to a Section 6 notification becomes illegal, being hit by Section 4 of the said Act.
This being the case, it is of no avail to the State, to submit (which submission has been made in the Supreme Court for the first time), that there is a dispute between the original owner and the subsequent purchaser, as a result of which compensation could neither be tendered nor paid. Apart from the said plea being an afterthought, it is also of no avail to either the DDA or the Land Acquisition Collector who, in any case, were not in any dilemma as to who should be paid. In fact, it is clear that the deposit made in Court pursuant to the order of the High Court of Delhi dated 30th December, 2013 has only been made in order to pay the original owner of the land. Accordingly, this plea has also to be turned down.
Provided that in a case where the said declaration has been published before the commencement of the Land Acquisition (Amendment) Act, 1984 (68 of 1984), the award shall be made within a period of two years from such commencement. Explanation - In computing the period of two years referred to in this section, the period during which any action or proceeding to be taken in pursuance of the said declaration is stayed by an order of a Court shall be excluded."
25. The judgment of Satendra Prasad Jain (supra) is also pressed into service by Shri Sharan, and in particular paragraph 15 thereof, which reads as under: "Ordinarily, the Government can take possession of the land proposed to be acquired only after an award of compensation in respect thereof has been made under Section 11. Upon the taking of possession the land vests in the Government, that is to say, the owner of the land loses to the Government the title to it. This is what Section 16 states.
The provisions of Section 11A are intended to benefit the landowner and ensure that the award is made within a period of two years from the date of the Section 6 declaration. In the ordinary case, therefore, when Government fails to make an award within two years of the declaration under Section 6, the land has still not vested in the Government and its title remains with the owner, the acquisition proceedings are still pending and, by virtue of the provisions of Section 11A, lapse.
26. Satendra Prasad Jain's case has been held in a subsequent judgment, namely, Laxmi Devi v. State of Bihar, (2015) 10 SCC 241, to have a limited ratio. The limited ratio has been said to be that it is not open to the beneficiary of an acquisition who has failed to make the necessary monies available, and who has been in occupation of the land since its possession was taken, to subsequently urge that such possession was taken illegally. It is clear that on the facts of that case, it was the land owners who filed a writ petition asking for a mandamus to complete the acquisition proceedings, and the State and the beneficiary of acquisition tried to resile from it by contending that the acquisition proceedings had lapsed under Section 11A of the Act. It was in these peculiar circumstances that the aforesaid judgment was delivered.
27. Even going by paragraph 15 of the Satendra Prasad Jain's case, we find that the difference in phraseology between Section 11A of the Land Acquisition Act and Section 24(2) of the 2013 Act really clinches the issue in favour of the land owners. The expression used in Section 24(2), namely, "deemed to have lapsed" is of great significance and differs from the use of the expression "lapsed" in Section 11A. As is well settled, a deeming fiction is enacted so that a putative state of affairs must be imagined, the mind not being allowed to boggle at the logical consequence of such putative state of affairs.
Even if we are to agree with Shri Sharan that, post vesting, acquisition proceedings cannot be said to lapse, yet we have to give effect to the deeming fiction contained in Section 24(2). In fact, Section 24(2) uses the expression "deemed to have lapsed" because the Legislature was cognizant of the fact that, in cases where compensation has not been paid, and physical possession handed over to the State, vesting has taken place, after which land acquisition proceedings could be said to have ended. For this reason also, we are of the view that Pune Municipal Corporation does not require to be revisited.
"(i) No hard-and-fast rule can be laid down as to what act would constitute taking of possession of the acquired land.
(ii) If the acquired land is vacant, the act of the State authority concerned to go to the spot and prepare a panchnama will ordinarily be treated as sufficient to constitute taking of possession.
(iii) If crop is standing on the acquired land or building/structure exists, mere going on the spot by the authority concerned will, by itself, be not sufficient for taking possession. Ordinarily, in such cases, the authority concerned will have to give notice to the occupier of the building/structure or the person who has cultivated the land and take possession in the presence of independent witnesses and get their signatures on the panchnama. Of course, refusal of the owner of the land or building/structure may not lead to an inference that the possession of the acquired land has not been taken.
(iv) If the acquisition is of a large tract of land, it may not be possible for the acquiring/designated authority to take physical possession of each and every parcel of the land and it will be sufficient that symbolic possession is taken by preparing appropriate document in the presence of independent witnesses and getting their signatures on such document.
29. As the present case will fall within sub-paragraph (ii), physical possession of the land can be said to have been taken on the facts of the present case.
30. Having regard to the law declared in the Pune Municipal Corporation case, as followed by the other judgments of this Court, we are of the opinion that the High Court is correct and that the impugned judgment calls for no interference. The appeals are, accordingly, dismissed.
Karnail Kaur v. State of Punjab (2015) 3 SCC 206 at paras 17, 18, 23; Rajiv Choudhrie HUF v. Union of India and Ors. 2015 (3) SCALE 203 at para 1; Competent Automobiles Co. Ltd. v. Union of India and Ors. AIR 2015 SC 3186 at para 4; Govt. of NCT of Delhi and Ors v. Jagjit Singh and Ors. AIR 2015 SC 2683 at para 3; Karan Singh and Ors. v. State of Haryana and Ors. 2015 (7) SCALE 191 at para 5; Delhi Development Authority v. Sukhbir Singh & Ors. SLP (CC) No. 5569 of 2015 at page 5; Shashi Gupta and Ors. v. State of Haryana and Ors. 2016 (5) SCALE 636 at para 5.

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