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Expression and Characterization of Two Domains of Pinellia Ternata Agglutinin (PTA), a Plant Agglutinin from Pinellia Ternata with Antifungal Activity

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Expression and Characterization of Two Domains of Pinellia Ternata Agglutinin (PTA), a Plant Agglutinin from Pinellia Ternata with Antifungal Activity World J Microbiol Biotechnol (2010) 26:545–554 DOI 10.1007/s11274-009-0204-2 ORIGINAL PAPER Expression and characterization of two domains of Pinellia ternata agglutinin (PTA), a plant agglutinin from Pinellia ternata with antifungal activity Li-Jun Ling • Yan-Zhuo Yang • Yu-Rong Bi Received: 16 July 2009 / Accepted: 28 September 2009 / Published online: 9 October 2009 Ó Springer Science+Business Media B.V. 2009 Abstract Pinellia ternata agglutinin (PTA) from P. ter- defined simple sugar and/or complex carbohydrates nata f. angustata is a two-domain GNA-related lectin. The (Fouquaert et al. 2009). Monocot mannose-binding lec- current study indicates that the PTA gene encodes a pre- tins is one of major plant lectin families that have been cursor consisting of two tandemly arrayed domains, reported. The monocot mannose-binding lectins have N-terminal domain (PTA-DOM1) and C-terminal domain been widely found in higher plants in last decade with (PTA-DOM2). Both domains and the precursor without most of them playing significant roles in defense against signal peptide (PTA-P) present different number of activity foreign microorganisms or plant predators due to their mannose-binding sites which play key roles for the lectin ability to recognize high-mannose-type glycans. Because function. Analyses of the three fusion proteins, PTA- the monocot mannose-binding lectins do not only occur DOM1, PTA-DOM2 and PTA-P, expressed in Escherichia in the monocot plant families but also in other species coli revealed that one mannose-binding site the aggluti- such as liverwort Marchantia polymorpha, gymnosperm nation activity while the additional sites do not possess Taxus media and fish Fuga rubripes, the monocot such activity. However, the number of carbohydrate-bind- mannose-binding lectins have been generally designated ing sites suggests some significant properties on the anti- as ‘‘GNA (Galanthus nivalis agglutinin)-related lectin’’ fungal effectiveness. In addition, each of the PTA domains (Van Damme et al. 2007). has the same function when compared with the natural GNA was the first monocot mannose-binding lectin PTA (N-PTA). The information on PTA gene obtained in isolated and characterized (Van Damme et al. 1987). this study will served as baseline information in developing Native GNA is a homotetramer compose of four non- this protein as a form of transgenic plant protection. covalently associated 12 kDa monomers. The GNA tetra- mer contains 12 apparently functional mannose-binding Keywords Plant lectin Á Domain Á Mannose-binding site Á sites. Other monocot mannose-binding lectins possess a Antifungal protein Á Expression Á P. ternata similar three-dimensional structure (Chandra et al. 1999; Wood et al. 1999). Recent investigations of the two- domains of GNA-related lectins revealed that some of Introduction these lectins have dual specificity and interact with both high-mannose and complex N-glycans, and that some have Lectins or agglutinins are a heterogeneous group of complex specificity. For instance, lectin from Xanthosema carbohydrate-binding proteins classified together on the sagittifolium (XSA) has two different types of carbohy- basis of their ability to bind in a reversible way to well- drate-binding sites recognizing oligomannoses and com- plex N-linked carbohydrates, respectively (Mo et al. 1999). On the contrary, lectin from Arum maculatum (AMA) has L.-J. Ling Á Y.-Z. Yang Á Y.-R. Bi (&) an apparently complex specificity due to its two distinct Key Laboratory of Arid and Grassland Agroecology (Ministry binding sites (Van Damme et al. 1995). of Education), School of Life Sciences, Lanzhou University, 730000 Lanzhou, People’s Republic of China Some plant lectins have potent antifungal activities, e-mail: [email protected] such as, Amaranthus viridis lectin (AVL) which exert 123 546 World J Microbiol Biotechnol (2010) 26:545–554 antifungal activity against phytopathogenic fungi Botrytis was a generous gift from Gansu Academy of Agriculture cinerea and Fusarium oxysporum (Kaur et al. 2006). Sciences. Similarly, two chitin-binding lectins from seeds of Arto- carpus genus inhibited the growth of Fusarium monili- Isolation of the cDNA clone encoding PTA forme and Saccharomyces cerevisiae (Trindade et al. 2006) from P. ternata f. angustata while the protein obtained from Gastrodia elata confer antifungal activity against Botrytis cinerea, Gibberella For 30 Rapid amplification of cDNA ends (RACE), 1.0 ll zeae, Ganoderma lucidum, Rhizoctonia solani and Valsa total RNA was reversely transcribed with the 30 RACE ambiens (Wang et al. 2001). Adaptor. The specific primer P1 for the 30-RACE system Previous studies demonstrated that the function of lec- was designed and synthesized (TaKaRa, Japan) according tins depends on their specific carbohydrate binding activi- to the conserved amino acid sequence of the monocot ties (Trigue´ros et al. 2001). For example the specific mannose-binding site (MQGDCNL). 30 RACE Outer Pri- carbohydrate-binding capacities of lectins involve the mer and P1 were used for PCR in the 30 RACE. PCR extensive use of water bridges, post-translation modifica- reaction for 30 RACE and 50 RACE was the same and tion and oligomerisation. Exogenous saccharides including performed under the following condition: cDNA was glycoproteins on surface of fungi, plant viruses, the midgut denatured at 94°C for 3 min following by 35 cycles of epithelial membrane of insects and plant predators are the amplification (94°C for 30 s, 55°C for 30 s, 72°C for most possible receptors of lectins (De Hoff et al. 2009). 1 min) and 72°C for a 10-min extension. Based on the Crop losses due to fungal diseases pose a serious threat sequence of the 30-RACE product, specific primers P2 and to global food security. In addition, certain groups of fungi P3 were designed to amplify the 50 end of PTA. The Outer can produce highly toxic and carcinogenic mycotoxins in PCR was performed with primer P2 and 50 RACE Outer infected crops, posing a direct health hazard to humans and Primer. The Inner PCR was carried out with primer P3 and animals. Some fungi, such as Alternaria alternata, Bipo- 50 RACE Inner Primer. By comparing the 30-RACE and 50- laris sorokiniana and Curvularia lunata, cause wilt disease RACE sequences, the full-length cDNA of PTA was in important crop plants, such as wheat and potato, obtained using gene-specific primers P4 and P5. All the resulting in poor yield and quality. The main control primers used above are listed in Table 1 and the PCR methods for fungal pathogens in agricultural crops involve products were purified and cloned into pMDTM 18-T (Ta- chemicals which, although effective, have serious ecolog- KaRa) vector and sequenced. 30 RACE Adaptor, 30 RACE ical and social consequences due to the toxic residues that Outer Primer, 50 RACE Outer Primer and 50 RACE Inner remain after their use. The ability to control fungal Primer used in this assay provided by Kit (30 Full RACE pathogens through transgenic expression of a lectin such as Core Set, 50 Full RACE Core Set kits, TaKaRa). PTA would be a useful and preferable alternative to toxic chemicals. Bioinformatics analysis of PTA gene and structure We report in this paper the cloning, expression, purifi- analysis of PTA cation and characterization of an agglutinin from P. ter- nata, designated as PTA, a traditional Chinese medicinal The open reading frame (ORF) of the PTA gene was plant species belong to Araceae to explore its potential as searched using the ORF finder program (http://www.ncbi. plant defense system against fungal pathogens of agricul- nlm.nih.gov/gorf/gorf.html). The theoretical molecular tural crops. mass and isoelectric points of the proteins were calculated using the ProtParam tool (http://us.expasy.org/tools/prot param.html). Using GNA as the model protein, molecular Materials and methods modeling was carried out using the Swiss-Model program according to (Schwede et al. 2003). Amino acid sequences Plant material and fungal strains of lectins from different plant species were aligned using the ClustalX program. Pinellia ternata f. angustata was collected from the prov- ince of Gansu, China while A. alternata, B. sorokiniana, Plasmid constructs for recombinant proteins and C. lunata were obtained from the Institute of Plant Protection, Chinese Academy of Agricultural Sciences. To obtain clones merely with the mature peptide coding The strains A. alternata (No. 3.5373), B. sorokiniana (No. region of PTA-DOM1, PTA-DOM2 and PTA-P, primers 3.2881), and C. lunata (No. 3.1866) have been deposited at (Table 1) with corresponsive restriction enzyme sites were the China General Microbiological Culture Collection designed based on the mature peptide domains sequences of Centre (CGMCC). Natural PTA isolated from P. ternata the target clone obtained above (PTA-DOM1, P6 and P7; 123 World J Microbiol Biotechnol (2010) 26:545–554 547 Table 1 Primers used in this Primer Sequence study P1 50-ATGCAGGGCGACTGCAACCT-30 P2 50-ACCCTGCTTGGAGCTGGACTG-30 P3 50-CAGCCGTACTTGCCGCCGT-30 P4 50-ACACAAAGCCGCGAACACGTATTC-30 P5 50-GGGAGCCATATTTATTTATTCAAGGG-30 P6 50-GCTAGC GCAGTGGGCACCAACTATCTGCTGTCC-30 (NheI) P7 50-AAGCTTGGGGACCCAAGGGTTGATCTTGAAGAC-30 (HindIII) P8 50-GCTAGCATCAACCCTTGGGTCCCCGGCCTCAAC-30 (NheI) P9 50-AAGCTTCGTCTCCTGAGCAGCAACGGAGCGC-30 (HindIII) Engineered restriction sites are ActinF 50-CCTCCAATCCAGACACTGTA-30 underlined. All primers were ActinR 50-AACTGGGATGATATGGAGAA-30 synthesized by TaKaRa PTA-DOM2, P8 and P9; PTA-P, P6 and P9). The follow dialysis against 20 mM PBS for 12 h. Desalted sample was assays of construction were performed as previous descri- adjusted to *2 mg/ml and stored at -20°C for the coming bed (Li et al. 2007). PCR reaction was as follows: 94°C for use. Primary antibodies against purified antigens were 30 s, 60°C for 45 s, 72°C for 30 s (30 cycles), and finally, produced by a commercial vendor (IGDB, CAS, China) 72°C for a 10-min extension.
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