JXB Advance Access originally published online on May 13, 2003
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Journal of Experimental Botany, Vol. 54, No. 388, pp. 1645-1654,
July 1, 2003
© 2003 Oxford University Press
Storage and mobilization as antagonistic functional constraints on seed storage globulin evolution
Received 25 November 2002; Accepted 5 March 2003
1 Laboratory of Protein Chemistry, State University of Moldova, Mateevici str. 60 MD-2009 Kishinev, Republic of Moldova
2 Institut für Pflanzengenetik und Kulturpflanzenforschung (IPK), Corrensstr. 3, D-06466 Gatersleben, Germany
* To whom correspondence should be addressed. Fax: +49 39482 5523. E-mail: muentz{at}IPK-Gatersleben.de
Abbreviations: MVP, vicilin-like protein from the fern Matteuccia struthiopteris (L.) TOD; VPE, vacuolar processing enzyme.
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Abstract |
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Top
Abstract
The dilemma in storage...When seeds germinate nearly all the proteins are degraded in senescing storage tissue cells. All these proteins act as amino acid reserves which are mobilized to nourish the seedling. Nevertheless, the major amount of the seeds’ protein reserve consists of a few enzymatically inactive, abundant, genuine storage proteins. In their metabolism the conflicting processes of biosynthesis, protein turnover and breakdown, are temporally separated. No degradation of correctly formed storage proteins was observed at the time of synthesis and accumulation during seed maturation. Breakdown takes place after a (long) period of rest when seeds germinate and seedlings start growing. At that time genuine storage proteins are no longer synthesized. Genuine storage proteins have evolved structural features permitting controlled temporal patterns of protection and proteolysis. The acquisition of inserted sequence stretches as sites accessible to limited proteolysis played a key role in the evolution of this control system and happened in coevolution of genuine storage proteins with specific proteinases. This can be deduced from the results of current research on the mechanisms of limited and unlimited proteolysis of storage globulins and on storage globulin evolution. The evolved system of controlled structure–function interplay between storage globulins and proteinases is part of a syndrome that, in addition, comprises differential compartmentation and gene expression of storage proteins and proteinases for controlling the total spatial and temporal patterns of globulin storage and mobilization in maturing and germinating seeds.
Key words: Deposition, evolution, mobilization, proteinases, seed storage globulins.
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The dilemma in storage protein metabolism |
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Many seed proteins are mobilized during germination and seedling growth. However, only a few seed proteins that account for the major protein content of a seed are genuine storage proteins. They are enzymatically inactive and act as high-molecular weight amino acid reserves destined to nourish the growing seedling. Genuine storage proteins are formed during seed maturation and deposited predominantly in specialized storage tissues, like the cotyledon mesophyll or endosperm. At that time, half-life times of 2–3 weeks have been measured (Madison et al., 1981). Correctly formed and assembled mature storage proteins are stably accumulated. Their degradation happens only after a long period of rest when seeds germinate and seedlings start to grow. Synthesis and degradation, the antagonistic processes of protein turnover, occur during different developmental stages. This temporal separation creates a dilemma in storage protein metabolism: at the time of formation and deposition these proteins have to be protected against premature breakdown, whereas with the initiation of germination they should become accessible for complete degradation.
Two major mechanisms protect storage proteins against uncontrolled proteolysis during seed maturation: (a) protein transport into membrane-bounded compartments like protein storage vacuoles or protein bodies to protect them from cytoplasmic proteinases and (b) structural features prohibiting cleavage by proteinases that are simultaneously present in the same compartment.
During germination and seedling growth, the complete degradation of storage proteins takes place inside the storage organelle. This process is usually triggered by newly formed proteinases, which are targeted into the organelle.
The dilemma becomes even more complicated because some storage proteins like legumins, 2S albumins or some lectins and some vicilins are synthesized as precursors that undergo molecular maturation by limited proteolysis before deposition. Similar proteinases catalyse the proteolytic processing of these proteins and contribute to their complete breakdown during germination and seedling growth.
Subsequently, in this review legumin (11S storage globulin) and vicilin (7S storage globulin) are taken as outstanding examples of the dilemma of storage protein metabolism and to show how this dilemma was resolved during storage globulin evolution.
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Legumin and vicilin structures have been inherited from an ancestral germin |
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Legumins and vicilins are storage globulins found in all investigated seeds of both spermatophyte classes (for a review see Shewry and Casey, 1999). Both types of globulins have subunits consisting of two structurally equivalent domains and both have evolved from a common single-domain germin-like ancestor (Bäumlein et al., 1995; Shutov and Bäumlein, 1999). Extant germins are proteins involved in the response of plants to stress (reviewed by Dunwell et al., 2000).
Both legumin and vicilin share basic features of tertiary and quaternary structure with germin (Ko et al., 1993, 2000; Lawrence et al., 1994; Woo et al., 2000; Adachi et al., 2001; Maruyama et al., 2001). Like the germin monomers, storage globulin domains consist of a ß-barrel followed by 
-helices (Fig. 1). The ß-barrel comprises two antiparallel ß-sheets formed by strands ABIDG and CHEFJ, respectively. The two-domain storage globulin subunit evolved due to the duplication of a germin-like ancestral domain. Consequently, it is structurally equivalent to a dimer of germin monomers. The structures of germin homodimers and storage globulin subunits are both formed by hydrophobic association of BIDG ß-sheets. The germin holoprotein is a trimer consisting of three homodimers. Similarly, the mature vicilin, as well as the precursor of legumin (prolegumin), form a trimer composed of three two-domain subunits. In the trimers, germin homodimers as well as storage globulin subunits are held together by hydrophobic interactions between the -helices. The trimers of germin, vicilin and prolegumin are disc-shaped and have similar quaternary structures (reviewed by Dunwell et al., 2001).
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Several features of prolegumin and mature legumin are structural novelties (Adachi et al., 2001) acquired due to the diversification of legumin and vicilin evolutionary pathways. Thus, hexameric mature legumin consists of two vicilin-like trimers that associate after each of the prolegumin subunits has been cleaved into an
-chain (N-domain) and a ß-chain (C-domain) by limited proteolysis (processing) of an Asn-flanked peptide bond. Additionally, disulphide bridges, which are lacking in vicilins but are formed between the domains of prolegumin, stabilize the conformation of legumin subunits. Obviously, the germin-like module inherited from prokaryotes (Dunwell and Gane, 1998; Shutov et al., 1999; Dunwell et al., 2001) has been recruited as a suitable structural basis for genuine storage globulins. The following paragraphs try to answer, at least in part, the questions of why and how this has occurred.
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Vicilin and legumin have independently acquired their genuine storage function |
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The duplication of an ancestral germin-like progenitor, probably involved in cell responses to desiccation, hydration and osmotic stress (Lane et al., 1991), can be regarded as a first step in the molecular evolution of the present structure of vicilin and legumin families of genuine storage proteins (reviewed by Shutov and Bäumlein, 1999). In addition, two-domain proteins with vicilin-like and legumin-like sequence features exist. The topology of an evolutionary tree (Fig. 2a) reveals that both kinds of these storage globulin-like proteins might reflect sequence features of immediate storage globulin progenitors.
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Sequence features of a common vicilin/legumin progenitor immediately prior to the duplication event are reflected by the C-domain of the vicilin-like protein (MVP) from the fern Matteuccia struthiopteris (L.) TOD (Fig. 2a). It cannot be excluded that the MVP, specifically expressed in spores (Shutov et al., 1998), functions as a primitive storage protein that combines structural features both of vicilin and legumin. However, several spermatophyte two-domain proteins, which are most similar to the MVP (up to 55% identities can be detected within the C-domain sequences), are unlikely to function as storage proteins. Thus, seeds of Cucurbita sp. contain the membrane-associated non-storage proteins MP27 and MP32 (Inoue et al., 1995), which are synthesized as a common MVP-like precursor (BAA06186 [GenBank] ). The precursor either lost an ancient storage function or represents an evolutionary step prior to the formation of storage-related structural attributes. Remarkably, the vicilin-like M27/32 precursor possesses a legumin-like Asn-flanked processing site (Fig. 2b). Moreover, MVP and M27/32 as well as related proteins share both vicilin and legumin sequence features (Fig. 2a). Nevertheless, they can be classified clearly as vicilin-like proteins according to the exon/intron patterns of the encoding genes (Fig. 2c), which are identical to those of genuine vicilin genes (Shutov and Bäumlein, 1999).
Whereas vicilin-like proteins share sequence features of both storage globulins, a group of spermatophyte two-domain proteins, exemplified by the Arabidopsis thaliana (L.) Heyh. protein AAD24367 [GenBank] , can be classified as legumin-like proteins. This is both based on their sequence features (Fig. 2a) and exon/intron patterns, which are characteristic of genuine legumin genes (Fig. 2c). Nevertheless, these legumin-like proteins lack both the processing site and the inter-domain disulphide bridge (Fig. 3) and resemble vicilins in these features. The legumin-like proteins exhibit extremely conserved primary structures. Within their C-terminal domains up to 82% residues are identical, even between dicot and monocot proteins. The strong sequence conservation of the legumin-like proteins argues in favour of their antiquity. It is suggested that legumin-like proteins reflect sequence features of an ancestor of genuine legumins prior to the acquisition of both the disulphide bridge between domains and the processing site inside the inter-domain linker. Furthermore, these proteins obviously cannot fulfil a storage function, because they all lack a signal peptide and, therefore, unlike genuine storage globulins, cannot be targeted to the storage organelle.
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In conclusion, the vicilin-like and legumin-like two-domain proteins reflect putative evolutionary steps after the bifurcation of the storage globulin lineage into the vicilin and legumin branches, but prior to the transition of both of them into genuine seed storage globulins. This implies that genuine vicilins and legumins have independently acquired their storage-related attributes specific to spermatophyte seed globulins. Sequence features of storage globulins that will be described in the following section support this conclusion.
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Storage globulins have acquired specific target sites for limited proteolysis |
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Two kinds of hydrophilic polypeptide regions (Figs 1, 3), which participate in the formation of the faces of vicilin and prolegumin disc-shaped trimers, turned out to be susceptible to limited proteolysis (Shutov et al., 1996): (a) extended loops between ß-strands E and F inside legumin N-domains and vicilin C-domains (inserts I1), and the extended ß-barrel/
-helix junction inside legumin N-domains (insert I2); (b) extended regions outside the germin-like structural module represented by the N-terminal extension of ‘large’ 70 kDa vicilins and the extended inter-domain linkers of both storage globulins. In the mature legumin hexamer the former inter-domain linker of prolegumin corresponds to the C-terminus of the -chain, which is highly susceptible to proteolytic attack. Being separated from the ß-chain because of the Asn-specific /ß-chain processing cleavage (see section, Legumin and vicilin structures have been inherited from an ancestral germin) the linker sequence is moved from the face of the trimer to its side (Adachi et al., 2001). In this way steric hindrances for the assembly of two prolegumin trimers into one mature legumin hexamer are eliminated and hexamer formation occurs. The alteration of prolegumin structure due to a single peptide bond cleavage exemplifies the structural and, therefore, functional, importance of a limited proteolysis. Limited proteolysis of prolegumin that occurs in developing seeds as well as limited proteolysis that occurs for both legumin and vicilin during seedling growth (Shutov and Vaintraub, 1987) is determined by the presence of the two kinds of susceptible sites in storage globulin subunits described above. The mature storage globulins both retain quaternary structure, irrespective of the cleavage of their susceptible sites. However, their tertiary structures become altered and the alteration imparts to storage globulins a susceptibility to complete proteolytic mobilization (see section, Limited proteolysis controls mobilization of storage globulins during seedling growth).
Unlike storage globulins, germin is extremely resistant to proteolytic attack (Lane, 1994). The following major structural features provide the basis of this resistance: (a) although the germin homodimer is structurally equivalent to storage globulin subunits, it lacks any insertions I1/I2 as well as an inter-domain linker (Fig. 1); (b) the N-terminal extension of germin is folded into the centre of the holoprotein and comprises a disulphide bridge as well as several structurally ordered elements (Woo et al., 2000). The structural specificity of germin forms the basis of its inaccessibility to limited proteolysis as well as to complete degradation.
Vicilin-like and legumin-like proteins, which have been suggested to reflect putative ancestral structures of genuine vicilin and legumin, respectively (Fig. 2a), both lack inserts I1 and I2 as targets for proteolytic attack (Fig. 3) and thus resemble germins. Moreover, the inter-domain linkers of all legumin-like proteins are too short to be a target of proteolytic attack, and their role seems to be restricted to domain junction.
However, to a certain extent, the MVP sequence resembles storage globulins (Fig. 3). Its N-terminal domain is supplemented by an N-terminal extension and its inter-domain linker is not truncated. Both these extensions remain uncleaved in the mature MVP holoprotein (IA Kakhovskaya et al., unpublished data) and, therefore, might represent specific target sites for limited proteolysis during spore germination. The existence of these sites invites the speculation that MVP might be a primitive storage protein (see section, Vicilin and legumin have independently acquired their genuine storage function). In this context it should be mentioned that some circumstantial evidence argues in favour of an ancient origin for the vicilin N-terminal extension, which has either been specifically acquired by ancient vicilins (Dure, 1990) or even earlier (Shutov et al., 1996).
The above data suggest that the acquisition of specific sites susceptible to limited proteolysis is essential for the storage function of a protein. Thus, the location of the I1 insertions in different domains of vicilin and legumin subunits (Fig. 1a) further supports the idea that these protein families independently acquired their storage function in seeds.
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How storage globulins are protected against premature breakdown in maturing seeds |
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Site-specific limited proteolysis of prolegumin (Fig. 3) is catalysed by an Asn-specific vacuolar processing enzyme (VPE) belonging to the cysteine endopeptidase family C13, called legumains (for a review see Müntz et al., 2002). After processing, mature legumins are resistant against premature VPE-mediated degradation although, in the protein bodies, the enzyme remains present until the first days of seedling growth. Vicilins, which are co-localized with legumins and VPEs but because of the lack of the Asn-flanked cleavage site do not undergo an Asn-dependent processing, are protected as well.
As can be concluded from the previous section, the mode of protection of structurally ordered elements of both storage globulins against any proteolytic attack has been inherited from their common germin-like ancestor. The potentially susceptible sites of vicilin and legumin described above have evolved in such a way as to become resistant to VPE attack and to afford protection of both to breakdown until mobilization starts during germination. These potentially susceptible regions are highly variable in size and sequence and usually do not adopt a regular secondary structure (Adachi et al., 2001). Therefore, they should tolerate hydrophilic substitutions. Hence, functional, rather than structural, constraints have determined the primary structure of the susceptible sites, reflecting the coevolution of storage globulins and processing proteinases.
An extensive analysis of storage globulin sequences reveals that Asn residues are rarely present within the inserts I1 and I2, or in the inter-domain linkers and the extended N-termini of 70 kDa vicilins (Fig. 3). As a rule, the few Asn residues found in some storage globulins are usually located in close proximity to the structurally ordered elements and thereby become protected against VPE attack. Two known exceptions support this rule: the legumin G4 from Glycine max (L.) Merr. (Momma et al., 1985) and a vicilin from Pisum sativum L. (Gatehouse et al., 1983). In both proteins an unprotected Asn residue is located in a central part of the insert I1, creating an unusual processing site. Despite cleavage at that site during seed maturation, both proteins remain stable until germination, indicating that this unique cleavage is not sufficient to trigger unlimited proteolysis.
In several other storage globulins Asn residues are protected in vivo against cleavage, although they are located distantly from structurally ordered elements. For example, the Vicia sativa L. legumin (CAA83674 [GenBank] ) contains an Asn–Pro bond inside the inter-domain linker (Fig. 3), which is not processed by VPE in vivo, but is cleaved by Asn-specific proteinase in vitro (Do et al., 1985; A Zakharov et al., unpublished data). A related situation is found in the processing site of some gymnosperm legumins (Häger and Fischer, 1999). Here, the insertion of a single Pro between the Asn/Gly residues of the regular processing site was found to prevent cleavage. This indicates that a specific local structure inside the potentially susceptible region might render an Asn-flanked bond inaccessible.
The mode of protection of phaseolin, the vicilin from Phaseolus vulgaris L. against VPE attack remains a mystery. Although the insert I1 and the inter-domain linker are both inaccessible in phaseolin during seed maturation, it was shown that Asn-specific limited proteolysis does occur during seedling growth (Senyuk et al., 1998). All three detected Asn-flanked cleavage points are unusual for ordinary vicilins.
At least in vitro, Asn-specific VPEs as well as other legumains can also cleave Asp-flanked peptide bonds although with 100-fold lower efficiency (Rotari et al., 2001). It remains to be explained whether this protects the abundant Asp-flanked peptide bonds in susceptible regions of many storage globulins.
Finally, papain-like proteinases of low cleavage specificity coexist with VPEs and storage globulins in the protein bodies of maturing seeds (Müntz et al., 2001). The inaccessibility of storage globulins to these papain-like enzymes might be due to the spatial separation from globulins in different vacuolar subcompartments as shown for tomato seeds (Jiang et al., 2001) or by the transformation of globulins into an inaccessible crystal state as suggested previously (Weber and Neumann, 1980).
In fact, the mature storage globulins found intact in dry seeds are protected against VPE attack in vivo. Although some aspects of this protection still remain unclear, its general mode consists of the combination of inherited inaccessibility of the tertiary structure of germin-like domains and the absence of unprotected Asn residues within newly acquired susceptible sites.
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Limited proteolysis controls mobilization of storage globulins during seedling growth |
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As mentioned above (see section, Storage globulins have acquired specific target sites for limited proteolysis), the cleavage of susceptible sites provokes the destabilization of the tertiary structure of storage globulins and thereby imparts susceptibility to unlimited proteolysis. Two observations support this hypothesis (Shutov and Vaintraub, 1987). First, limited proteolysis of storage globulins that precedes their complete breakdown was shown to occur at the beginning of storage globulin mobilization in many (possibly, all) spermatophyte seeds. Second, this in vivo limited proteolysis is accompanied by a dramatic increase in the susceptibility of legumin and vicilin to in vitro proteolytic attack. A sharp increase of legumin susceptibility was also observed as a result of in vitro limited proteolysis (Shutov and Vaintraub, 1987). In this context it should be mentioned that even a minor intervention into the primary structure of Vicia faba L. legumin via site-specific mutagenesis led to an dramatic increase of its susceptibility to proteolytic attack and complete degradation in developing seeds (Saalbach et al., 1995; Jung et al., 1998). Similarly, limited proteolysis can be regarded as an intervention into the structure of mature storage globulin that occurs in vivo.
Limited proteolysis that triggers unlimited degradation of storage globulins can be catalysed by small amounts of low specificity endopeptidases, either stored as active species in the protein bodies of dry seeds or activated during early germination. However, the limited triggering cleavages are mainly mediated by increasing amounts of proteinases synthesized de novo and transported into the protein bodies during seedling growth (Müntz et al., 2001). Papain-like proteinases play a major role among such low specificity proteinases.
Legumains closely similar to VPEs (Müntz et al., 2002), which are synthesized abundantly de novo during germination and seedling growth, contribute greatly to the subsequent unlimited degradation of storage globulins. In vitro, legumain from cotyledons of Vicia sativa seedlings (Shutov et al., 1982; Becker et al., 1995) was shown to catalyse almost exhaustive cleavage of all Asn-flanked peptide bonds in legumin which had previously been subjected to a very limited proteolysis by an endogenous papain-like enzyme (Do et al., 1985). In vivo, legumains degrade storage globulins in combination with papain-like enzymes and carboxypeptidases also present in protein bodies (Shutov and Vaintraub, 1987; Müntz et al., 2001). In some cases the degradation patterns of individual storage globulins can be more complicated. For instance, unlimited degradation of phaseolin (see section, How storage globulins are protected against premature breakdown in maturing seeds) can be achieved only under simultaneous attack by Asn-specific and papain-like proteinases (A Zakharov et al., unpublished data).
The contribution of legumains and papain-like enzymes to storage globulin mobilization depends on the relative level of their activities in seeds of different plants (Shutov and Vaintraub, 1987). A Vicia sativa papain-like enzyme (Becker et al., 1997) alone can catalyse both limited and unlimited proteolyses of legumin (Do et al., 1985). This ‘mixed-type proteolysis’ of legumin consists of two partially overlapping phases: fast limited and slow unlimited proteolysis (Shutov et al., 1991). The destabilization of the germin-like tertiary structure during the first phase is a prerequisite for the further unlimited degradation (the second phase) of the legumin holoprotein.
The pattern of in vitro proteolysis of phaseolin supports this conclusion most convincingly. Although phaseolin follows the canonical structural model of ordinary vicilins (Lawrence et al., 1994; Lawrence, 1999; Maruyama et al., 2001), it possesses an EF loop (insert I1), which is short enough to be inaccessible to limited proteolysis (Fig. 3). Thus, limited proteolysis of phaseolin is restricted to the cleavage of the inter-domain linker (Rotari et al., 1997). This generates a germin-like holoprotein structure that, like germin, appears to be inaccessible to in vitro unlimited proteolysis by trypsin, chymotrypsin and pepsin (Vaintraub et al., 1976, 1979; Romero and Ryan, 1978) and endogenous papain-like proteinase (Rotari et al., 1997).
Thus, independent of the enzyme involved in the unlimited degradation, the triggering initial cleavage of susceptible sites is regarded as the common functional prerequisite.
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The insertion of susceptible sites into the germin-like ancestor has been a major step in the evolution of structure–function relationships of seed storage globulins |
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Two ontogenetically separated requirements, accumulation during seed maturation and mobilization during seed germination and seedling growth, have been the functional constraints that directed the evolution of seed storage globulins to the pathway of adjustment of their structure to proteinases recruited to be involved in both the processes. The following evolutionary milestones mark this hypothetical pathway. First, the recruitment of the germin-like module of a single-domain progenitor generated a stable structural foundation. Second, the duplication of this single-domain progenitor, together with a short N-terminal extension, generated a two-domain structure consisting of N- and C-terminal modules connected by an inter-domain linker. Third, the enlargement of both the N-terminal extension and the inter-domain linker created polypeptide regions outside N-/C-terminal modules that were susceptible targets for limited proteolysis, and a prerequisite for the development of the putative storage function of proteins in non-seed plants. Fourth, the bifurcation of this general pathway led to the two separate branches for vicilins and legumins. In each, specific extended sequence insertions inside the modular structures have been acquired separately for vicilins and legumins. This generated targets for proteolytic attack and the structural basis for controlled storage globulin mobilization in spermatophytes.
The formation of sites specifically susceptible to limited proteolysis and the retention of the basic modular structures inaccessible to direct proteolytic attack provide important prerequisites for the precise control of storage protein metabolism: (a) accessibility for the processing by Asn-specific proteolytic attack, (b) inaccessibility to any further Asn-specific proteolytic attack during seed maturation, (c) susceptibility to limited proteolysis by unspecific proteases and imparting of accessibility to the holoprotein as a whole for unlimited proteolysis during germination and seedling growth, and (d) as a consequence, unrestrained complete proteolysis due to repeated Asn-specific and/or further unspecific attack.
In summary, the transient protection of susceptible sites during storage globulin deposition followed by their limited proteolysis at the beginning of mobilization represents a key mechanism that evolved to overcome the dilemma in storage globulin metabolism. Together with temporal protection by membrane bounding due to differential compartmentation and with differential temporal patterns of globulin and protease gene expression, the evolved protein structure basis for controlled proteolysis forms part of a syndrome of cellular tools acting in the total control of storage globulin metabolism. Modern molecular biology provides instruments to engineer structure elements for storage globulin processing and mobilization into extant germin and vice versa to transform extant storage globulins into germin-like proteins. The products of such engineering can be tested in vivo by seed-specific expression in transgenic plants as well as in vitro by incubating recombinantly produced proteins with appropriate protease(s). This will bring experimental verification for the described interdependent structure–function evolution of storage globulins for overcoming the storage protein dilemma.
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Acknowledgements |
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The authors are indebted to Professor S Utsumi and Dr M Adachi from the Research Institute of Food Science, Kyoto University, Japan, and to Professor JM Dunwell from the School of Plant Sciences, The University of Reading, UK, for kindly providing the ribbon diagrams of storage globulin and germin structures, respectively, prepared according to the requirements for fig. 1 of this review. In addition, the competent and skilful preparation of the final versions of all figures by Mrs U Tiemann and K Lipfert from the designers’ office of IPK, Gatersleben, is gratefully acknowledged. The authors’ research on proteinases and proteolysis of storage proteins as well as on storage protein evolution that partially forms the basis of the review was continuously supported by grants and project funding of Deutsche Forschungsgemeinschaft (DFG), and last but not least by grant GZ: 436 MOL 17/3/02 covering the expenses of the 2-month stay of AD Shutov at IPK, Gatersleben, for preparing this review.
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