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Structure of a Lectin from Canavalia Gladiata Seeds: New Structural

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Structure of a Lectin from Canavalia Gladiata Seeds: New Structural BMC Structural Biology BioMed Central Research article Open Access Structure of a lectin from Canavalia gladiata seeds: new structural insights for old molecules Plínio Delatorre*1,2, Bruno AM Rocha1,2, Emmanuel P Souza1, Taianá M Oliveira1, Gustavo A Bezerra1, Frederico BMB Moreno3, Beatriz T Freitas2, Tatiane Santi-Gadelha3, Alexandre H Sampaio1, Walter F Azevedo Jr4,5 and Benildo S Cavada*1 Address: 1Departamento de Bioquímica e Biologia Molecular, Universidade Federal do Ceará, Ceará, Brazil, 2Departamento de Biologia, Universidade Regional do Cariri, Ceará, Brazil, 3Departamento de Biologia, Universidade Federal da Paraíba, Paraíba, Brazil, 4Departamento de Física, IBILCE, Universidade Estadual Paulista, São Paulo, Brazil and 5Faculdade de Biociências, PUCRS, Av. Ipiranga 6681, Zip Code 90619-900, Porto Alegre, RS, Brazil Email: Plínio Delatorre* - [email protected]; Bruno AM Rocha - [email protected]; Emmanuel P Souza - [email protected]; Taianá M Oliveira - [email protected]; Gustavo A Bezerra - [email protected]; Frederico BMB Moreno - [email protected]; Beatriz T Freitas - [email protected]; Tatiane Santi- Gadelha - [email protected]; Alexandre H Sampaio - [email protected]; Walter F Azevedo - [email protected]; Benildo S Cavada* - [email protected] * Corresponding authors Published: 2 August 2007 Received: 6 October 2006 Accepted: 2 August 2007 BMC Structural Biology 2007, 7:52 doi:10.1186/1472-6807-7-52 This article is available from: http://www.biomedcentral.com/1472-6807/7/52 © 2007 Delatorre et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Abstract Background: Lectins are mainly described as simple carbohydrate-binding proteins. Previous studies have tried to identify other binding sites, which possible recognize plant hormones, secondary metabolites, and isolated amino acid residues. We report the crystal structure of a lectin isolated from Canavalia gladiata seeds (CGL), describing a new binding pocket, which may be related to pathogen resistance activity in ConA-like lectins; a site where a non-protein amino-acid, α- aminobutyric acid (Abu), is bound. Results: The overall structure of native CGL and complexed with α-methyl-mannoside and Abu have been refined at 2.3 Å and 2.31 Å resolution, respectively. Analysis of the electron density maps of the CGL structure shows clearly the presence of Abu, which was confirmed by mass spectrometry. Conclusion: The presence of Abu in a plant lectin structure strongly indicates the ability of lectins on carrying secondary metabolites. Comparison of the amino acids composing the site with other legume lectins revealed that this site is conserved, providing an evidence of the biological relevance of this site. This new action of lectins strengthens their role in defense mechanisms in plants. Background these proteins had been commonly reported in terms of Most of the biochemical lectin studies have been based on lectin-carbohydrate recognition. For several years, the def- monochromatic view since almost all the properties of inition of lectins has been improving focused on the car- Page 1 of 9 (page number not for citation purposes) BMC Structural Biology 2007, 7:52 http://www.biomedcentral.com/1472-6807/7/52 bohydrate-binding properties. The most recent accepted glycoconjugates on the surface or in the digestive tract of definition establishes lectins as proteins with at least one these organisms [10]. Although this interference has been non-catalytic domain able to recognize and bind reversi- reported as a specific event of carbohydrate recognition, it bly to specific mono and oligosaccharides. They are sub- has not been elucidated yet. Stress-regulated pathways for divided into four types: merolectins, hololectins, rapid and high gene expression are one of the essential chimerolectins and superlectins. This classification was elements in stress acclimation. Salicylic acid, jasmonic conceived in terms of the carbohydrate-binding domain acid, systemin, ethylene, and aminobutyric acid have and another unrelated domain [1]. Several studies have been implicated in the potentiation of gene expression tried to find other binding sites that could possibly recog- [11,12], and other signal molecules have been shown to nize plant hormones, secondary metabolites and isolated play a similar role [9]. amino acid residues [2-4]. The content of free protein amino acids in seeds varies Over 250 non-protein amino acids have been identified among species and increases dramatically after germina- in plants [5]. A number of these compounds are interme- tion. More non-protein amino acids were found in lentil diates in the synthesis and catabolism of protein amino seedlings compared to the seeds [12]. Most plant lectins acids [6]. However, many of these non-protein amino are probably involved in plant defense [13]. The mecha- acids may play a role as defensive agents. They show their nism of action still remains unclear even though induced toxicity in many ways; some of them block the synthesis response mechanisms are proposed for many pathogen- and the absorption of protein amino acids or can wrongly mediated injuries in plants. The direct interference with incorporated into proteins in organisms that feed on these viruses and microorganisms is rather exceptional, and the plants. Plants that synthesize non-protein amino acids are deleterious effects of plant lectins on both predatory not susceptible to the toxicity of these compounds. Seeds invertebrates and animals are well documented [13]. from Canavalia ensiformis, which synthesize high quanti- ties of non-protein amino acids, display a biological sys- We report here the crystal structure of a native and com- tem capable of discriminating between these amino acids plexed lectin isolated from Canavalia gladiata seeds, and the others [7]. describing a new binding pocket in ConA-like lectins, which may be related to pathogen resistance, a site where Non-protein amino acids are especially abundant in Legu- a non-protein amino acid, such as α-amino butyric acid, minosae, Liliaceae and in several higher fungi and marine can bind. algae. Plant organs rich in these metabolites are seeds (Leguminosae) or rhizomes (Liliaceae). Concentrations Results and discussion in seeds can exceed 10% of dry weight and up to 50% of Overall structure of CGL the nitrogen could be attributed to them. Since non-pro- The crystal structure of native CGL and in complex with α- tein amino acids are often remobilized during germina- methyl-mannoside (CGL-αMM) provides a new source of tion, they certainly function as N-storage compounds in information for the understanding of lectins and reveals a addition to their role as defense chemicals [8]. If non-pro- new binding site for a non protein amino acid at the mon- tein amino acids are taken up by herbivores, microorgan- omers contact interface of each canonical dimer of legu- isms or other plants, they may interfere with their minous lectins. The overall structure of native CGL and metabolism. CGL-αMM has been refined at the 2.3 Å and 2.31 Å reso- lutions, respectively (Figure 1). The lectin CGL model was Aminobutyric acid (Abu) is a non-protein amino acid that refined in the absence of ligand to produce the Fo-Fc map. can protect certain plants against pathogens; for instance, This map is unbiased insofar as the atomic coordinates when introduced into Arabidopis plants, it has the ability used for phase calculations have never been refined to induce resistance to certain pathogens. Abu protects together with the ligand. The ligand was finally inserted to these plants against pathogens through the activation of produce the final coordinates after some further refine- natural defense mechanisms of the plant, such as callose ment. The models present good stereochemistry, and the deposition, hypersensitive response (HR), and the forma- Ramachandran plot is consistent with a geometrically tion of trailing necroses. Induced resistance is often asso- well-defined structure (Table 1). ciated with a process called priming, which is an increased capacity to mobilize cellular defense responses [9]. Among the leguminous lectins isolated from the tribe Diocleinae, only those purified from the seeds of C. ensi- Most plant lectins not only play a role in the plant itself formis, C. brasiliensis, C. maritima, Dioclea grandiflora, D. (e.g., as a store of nitrogen or as a specific recognition fac- guianensis and Cratylia mollis have three-dimensional tor) but are also capable of interfering with the function- structures resolved by X-ray crystallography [14,15]. These ing of foreign organisms through an interaction with lectins showed respectively 98%, 98%, 99%, 84%, 82% Page 2 of 9 (page number not for citation purposes) BMC Structural Biology 2007, 7:52 http://www.biomedcentral.com/1472-6807/7/52 Table 1: Statistics of data collection, refinement and quality of the structure CGL CGL-αMM Data collection Total number of observations 238,197 483,177 Total number of unique observations 57,503 61,808 Rmerge (%) 8.8 (34.4) 7.3 (35.4) Resolution limit (Å) 42.64-2.3 51.99-2.31 Completeness (%) 97.87 (98.2) 99.1 (94.5) Multiplicity 3.9 4.5 (I)/σ 7.2 (2.2) 8.9 (2.0) Wavelength (Å) 1.431 1.431 Space group C2221 C2221 Cell parameters (Å) a = 100.90 a = 100.91 b = 115.35 b = 115.75 c = 241.08 c = 241.62 Refinement Resolution range (Å) 10-2.3 9.99-2.31 Rfactor (%) 18.38 16.87 Rfree (%) 23.28 22.31 CrystalFigure structure1 of CGL-αMM Number amino acid residues in biological 948 948 Crystal structure of CGL-αMM. The vision of the Abu assembly position can be seen in the canonical dimmer between the Number of water molecules 432 448 monomers at hydrophobic cavity.
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