Exportar registro bibliográfico


Identification and analysis of seven effector protein families with different adaptive and evolutionary histories in plant-associated members of the Xanthomonadaceae (2017)

  • Authors:
  • Unidades: EACH; IQ
  • DOI: 10.1038/s41598-017-16325-1
  • Language: Inglês
  • Imprenta:
  • Source:
  • Acesso à fonteDOI
    Informações sobre o DOI: 10.1038/s41598-017-16325-1 (Fonte: oaDOI API)
    • Este periódico é de acesso aberto
    • Este artigo é de acesso aberto
    • URL de acesso aberto
    • Cor do Acesso Aberto: gold
    • Licença: cc-by

    How to cite
    A citação é gerada automaticamente e pode não estar totalmente de acordo com as normas

    • ABNT

      ASSIS, Renata A. B; POLLONI, Lorraine Cristina; PATANE, Jose S. L; et al. Identification and analysis of seven effector protein families with different adaptive and evolutionary histories in plant-associated members of the Xanthomonadaceae. Scientific Reports, London, v. 7, p. 1-17 art. 16133, 2017. Disponível em: < http://dx.doi.org/ 10.1038/s41598-017-16325-1 > DOI: 10.1038/s41598-017-16325-1.
    • APA

      Assis, R. A. B., Polloni, L. C., Patane, J. S. L., Thakur, S., Felestrino, E. B., Caballero, J. D., et al. (2017). Identification and analysis of seven effector protein families with different adaptive and evolutionary histories in plant-associated members of the Xanthomonadaceae. Scientific Reports, 7, 1-17 art. 16133. doi:10.1038/s41598-017-16325-1
    • NLM

      Assis RAB, Polloni LC, Patane JSL, Thakur S, Felestrino EB, Caballero JD, Digiampietri LA, Goulart LR, Almeida NF, Nascimento R, Dandekar AM, Zaini PA, Setubal JC, Guttman DS, Moreira LM. Identification and analysis of seven effector protein families with different adaptive and evolutionary histories in plant-associated members of the Xanthomonadaceae [Internet]. Scientific Reports. 2017 ; 7 1-17 art. 16133.Available from: http://dx.doi.org/ 10.1038/s41598-017-16325-1
    • Vancouver

      Assis RAB, Polloni LC, Patane JSL, Thakur S, Felestrino EB, Caballero JD, Digiampietri LA, Goulart LR, Almeida NF, Nascimento R, Dandekar AM, Zaini PA, Setubal JC, Guttman DS, Moreira LM. Identification and analysis of seven effector protein families with different adaptive and evolutionary histories in plant-associated members of the Xanthomonadaceae [Internet]. Scientific Reports. 2017 ; 7 1-17 art. 16133.Available from: http://dx.doi.org/ 10.1038/s41598-017-16325-1

    Referências citadas na obra
    Gao, X. Y., Zhi, X. Y., Li, H. W., Klenk, H. P. & Li, W. J. Comparative genomics of the bacterial genus Streptococcus illuminates evolutionary implications of species groups. PloS one 9, e101229, https://doi.org/10.1371/journal.pone.0101229 (2014).
    Endo, A. et al. Comparative genome analysis and identification of competitive and cooperative interactions in a polymicrobial disease. The ISME journal 9, 629–642, https://doi.org/10.1038/ismej.2014.155 (2015).
    Ji, B. et al. Comparative genomic analysis provides insights into the evolution and niche adaptation of marine Magnetospira sp. QH-2 strain. Environmental microbiology 16, 525–544, https://doi.org/10.1111/1462-2920.12180 (2014).
    Carlier, A. L. & Eberl, L. The eroded genome of a Psychotria leaf symbiont: hypotheses about lifestyle and interactions with its plant host. Environmental microbiology 14, 2757–2769, https://doi.org/10.1111/j.1462-2920.2012.02763.x (2012).
    Saddler, G. S. & Bradbury, J. F. In Bergey’s Manual of Systematics of Archaea and Bacteria (2015).
    Sayers, E. W. et al. Database resources of the National Center for Biotechnology Information. Nucleic acids research 37, D5–15, https://doi.org/10.1093/nar/gkn741 (2009).
    Brunings, A. M. & Gabriel, D. W. Xanthomonas citri: breaking the surface. Molecular plant pathology 4, 141–157, https://doi.org/10.1046/j.1364-3703.2003.00163.x (2003).
    Pieretti, I. et al. The complete genome sequence of Xanthomonas albilineans provides new insights into the reductive genome evolution of the xylem-limited Xanthomonadaceae. BMC Genomics 10, 616, https://doi.org/10.1186/1471-2164-10-616 (2009).
    Ryan, R. P. et al. Pathogenomics of Xanthomonas: understanding bacterium-plant interactions. Nature reviews. Microbiology 9, 344–355, https://doi.org/10.1038/nrmicro2558 (2011).
    Redak, R. A. et al. The biology of xylem fluid-feeding insect vectors of Xylella fastidiosa and their relation to disease epidemiology. Annual review of entomology 49, 243–270, https://doi.org/10.1146/annurev.ento.49.061802.123403 (2004).
    Mansfield, J. et al. Top 10 plant pathogenic bacteria in molecular plant pathology. Molecular plant pathology 13, 614–629, https://doi.org/10.1111/j.1364-3703.2012.00804.x (2012).
    Simpson, A. J. et al. The genome sequence of the plant pathogen Xylella fastidiosa. The Xylella fastidiosa Consortium of the Organization for Nucleotide Sequencing and Analysis. Nature 406, 151–159, https://doi.org/10.1038/35018003 (2000).
    Delepelaire, P. T. Type I secretion in gram-negative bacteria. Biochimica et biophysica acta 1694, 149–161, https://doi.org/10.1016/j.bbamcr.2004.05.001 (2004).
    Vinuesa, P. & Ochoa-Sanchez, L. E. Complete Genome Sequencing of Stenotrophomonas acidaminiphila ZAC14D2_NAIMI4_2, a Multidrug-Resistant Strain Isolated from Sediments of a Polluted River in Mexico, Uncovers New Antibiotic Resistance Genes and a Novel Class-II Lasso Peptide Biosynthesis Gene Cluster. Genome announcements 3, https://doi.org/10.1128/genomeA.01433-15 (2015).
    Youenou, B. et al. Comparative Genomics of Environmental and Clinical Stenotrophomonas maltophilia Strains with Different Antibiotic Resistance Profiles. Genome biology and evolution 7, 2484–2505, https://doi.org/10.1093/gbe/evv161 (2015).
    Pak, T. R. et al. Whole-genome sequencing identifies emergence of a quinolone resistance mutation in a case of Stenotrophomonas maltophilia bacteremia. Antimicrobial agents and chemotherapy 59, 7117–7120, https://doi.org/10.1128/AAC.01723-15 (2015).
    Dean, B. J. Recent findings on the genetic toxicology of benzene, toluene, xylenes and phenols. Mutation research 154, 153–181 (1985).
    Choi, E. J. et al. Comparative genomic analysis and benzene, toluene, ethylbenzene, and o-, m-, and p-xylene (BTEX) degradation pathways of Pseudoxanthomonas spadix BD-a59. Appl Environ Microbiol 79, 663–671, https://doi.org/10.1128/AEM.02809-12 (2013).
    Hou, L., Jiang, J., Xu, Z., Zhou, Y. & Leung, F. C. Complete Genome Sequence of Pseudoxanthomonas suwonensis Strain J1, a Cellulose-Degrading Bacterium Isolated from Leaf- and Wood-Enriched Soil. Genome announcements 3, https://doi.org/10.1128/genomeA.00614-15 (2015).
    Moreira, L. M. et al. Novel insights into the genomic basis of citrus canker based on the genome sequences of two strains of Xanthomonas fuscans subsp. aurantifolii. BMC Genomics 11, 238, https://doi.org/10.1186/1471-2164-11-238 (2010).
    Moreira, L. M., De Souza, R. F., Digiampietri, L. A., Da Silva, A. C. & Setubal, J. C. Comparative analyses of Xanthomonas and Xylella complete genomes. Omics: a journal of integrative biology 9, 43–76, https://doi.org/10.1089/omi.2005.9.43 (2005).
    Van Sluys, M. A. et al. Comparative genomic analysis of plant-associated bacteria. Annual review of phytopathology 40, 169–189, https://doi.org/10.1146/annurev.phyto.40.030402.090559 (2002).
    Fang, Y. et al. Genome sequence of Xanthomonas sacchari R1, a biocontrol bacterium isolated from the rice seed. Journal of biotechnology 206, 77–78, https://doi.org/10.1016/j.jbiotec.2015.04.014 (2015).
    Arpigny, J. L. & Jaeger, K. E. Bacterial lipolytic enzymes: classification and properties. The Biochemical journal 343(Pt 1), 177–183 (1999).
    Rosenau, F. & Jaeger, K. Bacterial lipases from Pseudomonas: regulation of gene expression and mechanisms of secretion. Biochimie 82, 1023–1032 (2000).
    Pleiss, J., Fischer, M., Peiker, M., Thiele, C. & Schmid, R. D. Lipase engineering database: Understanding and exploiting sequence–structure–function relationships. Journal of Molecular Catalysis B: Enzymatic 10, 491–508, https://doi.org/10.1016/S1381-1177(00)00092-8 (2000).
    Nascimento, R. et al. TheType II Secreted Lipase/Esterase LesA is a Key Virulence Factor Required for Xylella fastidiosa Pathogenesis in Grapevines. Scientific reports 6, 18598, https://doi.org/10.1038/srep18598 (2016).
    Aparna, G., Chatterjee, A., Sonti, R. V. & Sankaranarayanan, R. A cell wall-degrading esterase of Xanthomonas oryzae requires a unique substrate recognition module for pathogenesis on rice. The Plant cell 21, 1860–1873, https://doi.org/10.1105/tpc.109.066886 (2009).
    Tamir-Ariel, D., Rosenberg, T., Navon, N. & Burdman, S. A secreted lipolytic enzyme from Xanthomonas campestris pv. vesicatoria is expressed in planta and contributes to its virulence. Molecular plant pathology 13, 556–567, https://doi.org/10.1111/j.1364-3703.2011.00771.x (2012).
    Jaeger, K. E., Dijkstra, B. W. & Reetz, M. T. Bacterial biocatalysts: molecular biology, three-dimensional structures, and biotechnological applications of lipases. Annual review of microbiology 53, 315–351, https://doi.org/10.1146/annurev.micro.53.1.315 (1999).
    Djamei, A. et al. Metabolic priming by a secreted fungal effector. Nature 478, 395–398, https://doi.org/10.1038/nature10454 (2011).
    Boulanger, A. et al. Identification and regulation of the N-acetylglucosamine utilization pathway of the plant pathogenic bacterium Xanthomonas campestris pv. campestris. J Bacteriol 192, 1487–1497, https://doi.org/10.1128/JB.01418-09 (2010).
    Dupoiron, S. et al. The N-Glycan cluster from Xanthomonas campestris pv. campestris: a toolbox for sequential plant N-glycan processing. J Biol Chem 290, 6022–6036, https://doi.org/10.1074/jbc.M114.624593 (2015).
    Canonne, J. et al. The Xanthomonas type III effector XopD targets the Arabidopsis transcription factor MYB30 to suppress plant defense. The Plant cell 23, 3498–3511, https://doi.org/10.1105/tpc.111.088815 (2011).
    Furutani, A. et al. Identification of novel type III secretion effectors in Xanthomonas oryzae pv. oryzae. Molecular plant-microbe interactions: MPMI 22, 96–106, https://doi.org/10.1094/MPMI-22-1-0096 (2009).
    Jiang, W. et al. Identification of six type III effector genes with the PIP box in Xanthomonas campestris pv. campestris and five of them contribute individually to full pathogenicity. Molecular plant-microbe interactions: MPMI 22, 1401–1411, https://doi.org/10.1094/MPMI-22-11-1401 (2009).
    Lombard, V., Golaconda Ramulu, H., Drula, E., Coutinho, P. M. & Henrissat, B. The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic acids research 42, D490–495, https://doi.org/10.1093/nar/gkt1178 (2014).
    Deattie, G. A. In Plant-Associated Bacteria (ed S. S. Gnanamanickam) Ch. 1, 1–56 (Springer, 2007).
    Buttner, D. Protein export according to schedule: architecture, assembly, and regulation of type III secretion systems from plant- and animal-pathogenic bacteria. Microbiol Mol Biol Rev 76, 262–310, https://doi.org/10.1128/MMBR.05017-11 (2012).
    Del Giudice, M. G. et al. VirJ Is a Brucella Virulence Factor Involved in the Secretion of Type IV Secreted Substrates. The Journal of biological chemistry 291, 12383–12393, https://doi.org/10.1074/jbc.M116.730994 (2016).
    Esquerré-Tugayé, M. T., Boudart, G. & Bernard Dumas, B. Cell wall degrading enzymes, inhibitory proteins, and oligosaccharides participate in the molecular dialogue between plants and pathogens. Plant Physiology and Biochemistry 38, 157–163, https://doi.org/10.1016/S0981-9428(00)00161-3 (2000).
    Rajeshwari, R., Jha, G. & Sonti, R. V. Role of an in planta-expressed xylanase of Xanthomonas oryzae pv. oryzae in promoting virulence on rice. Molecular plant-microbe interactions: MPMI 18, 830–837, https://doi.org/10.1094/MPMI-18-0830 (2005).
    Jha, G., Rajeshwari, R. & Sonti, R. V. Functional interplay between two Xanthomonas oryzae pv,. oryzae secretion systems in modulating virulence on rice. Molecular plant-microbe interactions: MPMI 20, 31–40, https://doi.org/10.1094/MPMI-20-0031 (2007).
    Roper, M. C., Greve, L. C., Warren, J. G., Labavitch, J. M. & Kirkpatrick, B. C. Xylella fastidiosa requires polygalacturonase for colonization and pathogenicity in Vitis vinifera grapevines. Molecular plant-microbe interactions: MPMI 20, 411–419, https://doi.org/10.1094/MPMI-20-4-0411 (2007).
    Laine, A. L. Role of coevolution in generating biological diversity: spatially divergent selection trajectories. Journal of experimental botany 60, 2957–2970, https://doi.org/10.1093/jxb/erp168 (2009).
    Kast, P. et al. A strategically positioned cation is crucial for efficient catalysis by chorismate mutase. J Biol Chem 275, 36832–36838, https://doi.org/10.1074/jbc.M006351200 (2000).
    Bekal, S., Niblack, T. L. & Lambert, K. N. A chorismate mutase from the soybean cyst nematode Heterodera glycines shows polymorphisms that correlate with virulence. Molecular plant-microbe interactions: MPMI 16, 439–446, https://doi.org/10.1094/MPMI.2003.16.5.439 (2003).
    Vlot, A. C., Dempsey, D. A. & Klessig, D. F. Salicylic Acid, a multifaceted hormone to combat disease. Annual review of phytopathology 47, 177–206, https://doi.org/10.1146/annurev.phyto.050908.135202 (2009).
    Maeda, H. & Dudareva, N. The shikimate pathway and aromatic amino Acid biosynthesis in plants. Annual review of plant biology 63, 73–105, https://doi.org/10.1146/annurev-arplant-042811-105439 (2012).
    Schmit, J. C. & Zalkin, H. Chorismate mutase-prephenate dehydratase. Phenylalanine-induced dimerization and its relationship to feedback inhibition. J Biol Chem 246, 6002–6010 (1971).
    Grant, G. A. The ACT domain: a small molecule binding domain and its role as a common regulatory element. J Biol Chem 281, 33825–33829, https://doi.org/10.1074/jbc.R600024200 (2006).
    Zhang, S. et al. Chorismate mutase-prephenate dehydratase from Escherichia coli. Study of catalytic and regulatory domains using genetically engineered proteins. J Biol Chem 273, 6248–6253 (1998).
    Degrassi, G., Devescovi, G., Bigirimana, J. & Venturi, V. Xanthomonas oryzae pv. oryzae XKK.12 contains an AroQgamma chorismate mutase that is involved in rice virulence. Phytopathology 100, 262–270, https://doi.org/10.1094/PHYTO-100-3-0262 (2010).
    Ferreira, R. M. et al. Unravelling potential virulence factor candidates in Xanthomonas citri. subsp. citri by secretome analysis. PeerJ, https://doi.org/10.7717/peerj.1734 (2016).
    Marino, K., Bones, J., Kattla, J. J. & Rudd, P. M. A systematic approach to protein glycosylation analysis: a path through the maze. Nature chemical biology 6, 713–723, https://doi.org/10.1038/nchembio.437 (2010).
    Maeda, M. & Kimura, Y. Structural features of free N-glycans occurring in plants and functional features of de-N-glycosylation enzymes, ENGase, and PNGase: the presence of unusual plant complex type N-glycans. Frontiers in plant science 5, 429, https://doi.org/10.3389/fpls.2014.00429 (2014).
    Priem, B., Gitti, R., Bush, C. A. & Gross, K. C. Structure of ten free N-glycans in ripening tomato fruit. Arabinose is a constituent of a plant N-glycan. Plant physiology 102, 445–458 (1993).
    Suzuki, T. & Funakoshi, Y. Free N-linked oligosaccharide chains: formation and degradation. Glycoconjugate journal 23, 291–302, https://doi.org/10.1007/s10719-006-6975-x (2006).
    Priem, B. et al. Isolation and characterization of free glycans of the oligomannoside type from the extracellular medium of a plant cell suspension. Glycoconjugate journal 7, 121–132, https://doi.org/10.1007/BF01050375 (1990).
    Haweker, H. et al. Pattern recognition receptors require N-glycosylation to mediate plant immunity. J Biol Chem 285, 4629–4636, https://doi.org/10.1074/jbc.M109.063073 (2010).
    Saijo, Y. ER quality control of immune receptors and regulators in plants. Cellular microbiology 12, 716–724, https://doi.org/10.1111/j.1462-5822.2010.01472.x (2010).
    Kang, B. S. et al. N-Glycosylation process in both ER and Golgi plays pivotal role in plant immunity. Journal of Plant Biology 58, 374–382, https://doi.org/10.1007/s12374-015-0197-3 (2015).
    Boulanger, A. et al. The plant pathogen Xanthomonas campestris pv. campestris exploits N-acetylglucosamine during infection. mBio 5, e01527–01514, https://doi.org/10.1128/mBio.01527-14 (2014).
    Wang, Y. et al. Secretome analysis of the rice bacterium Xanthomonas oryzae (Xoo) using in vitro and in planta systems. Proteomics 13, 1901–1912, https://doi.org/10.1002/pmic.201200454 (2013).
    Peabody, C. R. et al. Type II protein secretion and its relationship to bacterial type IV pili and archaeal flagella. Microbiology 149, 3051–3072, https://doi.org/10.1099/mic.0.26364-0 (2003).
    Szczesny, R. et al. Functional characterization of the Xcs and Xps type II secretion systems from the plant pathogenic bacterium Xanthomonas campestris pv vesicatoria. The New phytologist 187, 983–1002, https://doi.org/10.1111/j.1469-8137.2010.03312.x (2010).
    Astua-Monge, G. et al. Expression profiling of virulence and pathogenicity genes of Xanthomonas axonopodis pv. citri. J Bacteriol 187, 1201–1205, https://doi.org/10.1128/JB.187.3.1201-1205.2005 (2005).
    Gonzalez, J. F. et al. A proteomic study of Xanthomonas oryzae pv. oryzae in rice xylem sap. Journal of proteomics 75, 5911–5919, https://doi.org/10.1016/j.jprot.2012.07.019 (2012).
    Palmieri, A. C., do Amaral, A. M., Homem, R. A. & Machado, M. A. Differential expression of pathogenicity- and virulence-related genes of Xanthomonas axonopodis pv. citri under copper stress. Genetics and molecular biology 33, 348–353, https://doi.org/10.1590/S1415-47572010005000030 (2010).
    Yamazaki, A., Hirata, H. & Tsuyumuv, S. HrpG regulates type II secretory proteins in Xanthomonas axonopodis pv. citri. Journal of General Plant Pathology 74, 138–150, https://doi.org/10.1007/s10327-008-0075-7 (2008).
    Jalan, N. et al. Comparative genomic analysis of Xanthomonas axonopodis pv. citrumelo F1, which causes citrus bacterial spot disease, and related strains provides insights into virulence and host specificity. J Bacteriol 193, 6342–6357, https://doi.org/10.1128/JB.05777-11 (2011).
    Guo, Y., Figueiredo, F., Jones, J. & Wang, N. HrpG and HrpX play global roles in coordinating different virulence traits of Xanthomonas axonopodis pv. citri. Molecular plant-microbe interactions: MPMI 24, 649–661, https://doi.org/10.1094/MPMI-09-10-0209 (2011).
    Anderson, J. P. et al. Plants versus pathogens: an evolutionary arms race. Functional plant biology: FPB 37, 499–512, https://doi.org/10.1071/FP09304 (2010).
    Farias, N. C. & Almeida, N. F. Orthologsorter: Inferring Genotyping and Functionality from Ortholog Protein Families Master thesis, Federal University of Mato Grosso do Sul, (2013).
    Li, L., Stoeckert, C. J. Jr & Roos, D. S. OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome research 13, 2178–2189, https://doi.org/10.1101/gr.1224503 (2003).
    Edgar, R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic acids research 32, 1792–1797, https://doi.org/10.1093/nar/gkh340 (2004).
    Castresana, J. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular biology and evolution 17, 540–552 (2000).
    Stamatakis, A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688–2690, https://doi.org/10.1093/bioinformatics/btl446 (2006).
    Boratyn, G. M. et al. BLAST: a more efficient report with usability improvements. Nucleic acids research 41, W29–33, https://doi.org/10.1093/nar/gkt282 (2013).
    Katoh, K. & Standley, D. M. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular biology and evolution 30, 772–780, https://doi.org/10.1093/molbev/mst010 (2013).
    Capella-Gutierrez, S., Silla-Martinez, J. M. & Gabaldon, T. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25, 1972–1973, https://doi.org/10.1093/bioinformatics/btp348 (2009).
    Nguyen, L. T., Schmidt, H. A., von Haeseler, A. & Minh, B. Q. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Molecular biology and evolution 32, 268–274, https://doi.org/10.1093/molbev/msu300 (2015).
    Vaneechoutte, M., Verschraegen, G., Claeys, G. & Flamen, P. Rapid identification of Branhamella catarrhalis with 4-methylumbelliferyl butyrate. Journal of clinical microbiology 26, 1227–1228 (1988).
    Kanehisa, M. & Goto, S. KEGG: kyoto encyclopedia of genes and genomes. Nucleic acids research 28, 27–30 (2000).
    Mitchell, A. et al. The InterPro protein families database: the classification resource after 15 years. Nucleic acids research 43, D213–221, https://doi.org/10.1093/nar/gku1243 (2015).
    Schultz, J., Milpetz, F., Bork, P. & Ponting, C. P. SMART, a simple modular architecture research tool: identification of signaling domains. Proceedings of the National Academy of Sciences of the United States of America 95, 5857–5864 (1998).
    Sonnhammer, E. L., Eddy, S. R., Birney, E., Bateman, A. & Durbin, R. Pfam: multiple sequence alignments and HMM-profiles of protein domains. Nucleic acids research 26, 320–322 (1998).
    Dhillon, B. K. et al. IslandViewer 3: more flexible, interactive genomic island discovery, visualization and analysis. Nucleic acids research 43, W104–108, https://doi.org/10.1093/nar/gkv401 (2015).
    Bendtsen, J. D., Nielsen, H., Widdick, D., Palmer, T. & Brunak, S. Prediction of twin-arginine signal peptides. BMC bioinformatics 6, 167, https://doi.org/10.1186/1471-2105-6-167 (2005).
    Kall, L., Krogh, A. & Sonnhammer, E. L. A combined transmembrane topology and signal peptide prediction method. Journal of molecular biology 338, 1027–1036, https://doi.org/10.1016/j.jmb.2004.03.016 (2004).
    Nielsen, H., Engelbrecht, J., Brunak, S. & von Heijne, G. Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein engineering 10, 1–6 (1997).
    Kuhn, M. et al. STITCH 4: integration of protein-chemical interactions with user data. Nucleic acids research 42, D401–407, https://doi.org/10.1093/nar/gkt1207 (2014).
    Berman, H. M. et al. The Protein Data Bank. Nucleic acids research 28, 235–242 (2000).

Digital Library of Intellectual Production of Universidade de São Paulo     2012 - 2021