{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,1,15]],"date-time":"2026-01-15T05:10:07Z","timestamp":1768453807761,"version":"3.49.0"},"reference-count":31,"publisher":"MDPI AG","issue":"11","license":[{"start":{"date-parts":[[2011,10,25]],"date-time":"2011-10-25T00:00:00Z","timestamp":1319500800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/3.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>A germin-like gene (CchGLP) cloned from geminivirus-resistant pepper (Capsicum chinense Jacq. Line BG-3821) was characterized and the enzymatic activity of the expressed protein analyzed. The predicted protein consists of 203 amino acids, similar to other germin-like proteins. A highly conserved cupin domain and typical germin boxes, one of them containing three histidines and one glutamate, are also present in CchGLP. A signal peptide was predicted in the first 18 N-terminal amino acids, as well as one putative N-glycosylation site from residues 44\u201347. CchGLP was expressed in E. coli and the recombinant protein displayed manganese superoxide dismutase (Mn-SOD) activity. Molecular analysis showed that CchGLP is present in one copy in the C. chinense Jacq. genome and was induced in plants by ethylene (Et) and salicylic acid (SA) but not jasmonic acid (JA) applications in the absence of pathogens. Meanwhile, incompatible interactions with either Pepper golden mosaic virus (PepGMV) or Pepper huasteco yellow vein virus (PHYVV) caused local and systemic CchGLP induction in these geminivirus-resistant plants, but not in a susceptible accession. Compatible interactions with PHYVV, PepGMV and oomycete Phytophthora capsici did not induce CchGLP expression. Thus, these results indicate that CchGLP encodes a Mn-SOD, which is induced in the C. chinense geminivirus-resistant line BG-3821, likely using SA and Et signaling pathways during incompatible interactions with geminiviruses PepGMV and PHYVV.<\/jats:p>","DOI":"10.3390\/ijms12117301","type":"journal-article","created":{"date-parts":[[2011,10,25]],"date-time":"2011-10-25T12:46:40Z","timestamp":1319546800000},"page":"7301-7313","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":30,"title":["A Germin-Like Protein Gene (CchGLP) of Capsicum chinense Jacq. Is Induced during Incompatible Interactions and Displays Mn-Superoxide Dismutase Activity"],"prefix":"10.3390","volume":"12","author":[{"given":"Fabiola","family":"Le\u00f3n-Galv\u00e1n","sequence":"first","affiliation":[{"name":"Divisi\u00f3n de Ciencias de la Vida, Departamento de Ingenier\u00eda en Alimentos, Campus Irapuato-Salamanca, Universidad de Guanajuato, Ex-Hacienda el Copal km 9, Carretera Irapuato-Silao, CP 36500, Irapuato Guanajuato, Mexico"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Ahuizolt de Jes\u00fas","family":"Joaqu\u00edn-Ramos","sequence":"additional","affiliation":[{"name":"Divisi\u00f3n de Biolog\u00eda Molecular, Instituto Potosino de Investigaci\u00f3n Cient\u00edfica y Tecnol\u00f3gica, Camino a la Presa San Jos\u00e9 2055, Colima, Lomas 4 secci\u00f3n CP 78216, San Luis Potos\u00ed, S.L.P. Mexico"},{"name":"Laboratorio de Biolog\u00eda Molecular, Departamento de Ingenier\u00eda Bioqu\u00edmica, Instituto Tecnol\u00f3gico de Celaya, Avenida Tecnol\u00f3gico y A, Garc\u00eda-Cubas, S\/N, Col, FOVISSSTE, CP 38010, Celaya, Guanajuato, Mexico"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Irineo","family":"Torres-Pacheco","sequence":"additional","affiliation":[{"name":"C.A de Ingenier\u00eda de Biosistemas, Facultad de Ingenier\u00eda, Universidad Aut\u00f3noma de Quer\u00e9taro, Centro Universitario Cerro de las Campanas, S\/N, Col, Las Campanas, CP 76010, Santiago de Quer\u00e9taro, Quer\u00e9taro, Mexico"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Ana P. Barba","family":"De la Rosa","sequence":"additional","affiliation":[{"name":"Divisi\u00f3n de Biolog\u00eda Molecular, Instituto Potosino de Investigaci\u00f3n Cient\u00edfica y Tecnol\u00f3gica, Camino a la Presa San Jos\u00e9 2055, Colima, Lomas 4 secci\u00f3n CP 78216, San Luis Potos\u00ed, S.L.P. Mexico"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Lorenzo","family":"Guevara-Olvera","sequence":"additional","affiliation":[{"name":"Laboratorio de Biolog\u00eda Molecular, Departamento de Ingenier\u00eda Bioqu\u00edmica, Instituto Tecnol\u00f3gico de Celaya, Avenida Tecnol\u00f3gico y A, Garc\u00eda-Cubas, S\/N, Col, FOVISSSTE, CP 38010, Celaya, Guanajuato, Mexico"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Mario M.","family":"Gonz\u00e1lez-Chavira","sequence":"additional","affiliation":[{"name":"Unidad de Biotecnolog\u00eda, Instituto Nacional de Investigaciones Forestales, Agr\u00edcolas y Pecuarias, Carr, Celaya-San Miguel de Allende, km 6, CP 38010, Celaya, Guanajuato, Mexico"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Rosal\u00eda V.","family":"Ocampo-Velazquez","sequence":"additional","affiliation":[{"name":"C.A de Ingenier\u00eda de Biosistemas, Facultad de Ingenier\u00eda, Universidad Aut\u00f3noma de Quer\u00e9taro, Centro Universitario Cerro de las Campanas, S\/N, Col, Las Campanas, CP 76010, Santiago de Quer\u00e9taro, Quer\u00e9taro, Mexico"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Enrique","family":"Rico-Garc\u00eda","sequence":"additional","affiliation":[{"name":"C.A de Ingenier\u00eda de Biosistemas, Facultad de Ingenier\u00eda, Universidad Aut\u00f3noma de Quer\u00e9taro, Centro Universitario Cerro de las Campanas, S\/N, Col, Las Campanas, CP 76010, Santiago de Quer\u00e9taro, Quer\u00e9taro, Mexico"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Ram\u00f3n Gerardo","family":"Guevara-Gonz\u00e1lez","sequence":"additional","affiliation":[{"name":"C.A de Ingenier\u00eda de Biosistemas, Facultad de Ingenier\u00eda, Universidad Aut\u00f3noma de Quer\u00e9taro, Centro Universitario Cerro de las Campanas, S\/N, Col, Las Campanas, CP 76010, Santiago de Quer\u00e9taro, Quer\u00e9taro, Mexico"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2011,10,25]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"541","DOI":"10.1046\/j.1365-313X.1999.00624.x","article-title":"Transient expression of members of the germin-like gene family in epidermal cells of wheat confers disease resistance","volume":"20","author":"Schweizer","year":"1999","journal-title":"Plant J"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"797","DOI":"10.1007\/s00425-004-1290-x","article-title":"Molecular characterization of pepper germin-like protein as the novel PR-16 family of pathogenesis-related proteins isolated during the resistance response to viral and bacterial infection","volume":"219","author":"Park","year":"2004","journal-title":"Planta"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"1161","DOI":"10.1093\/jxb\/erl282","article-title":"A germin-like protein with superoxide dismutase activity in pea nodules with high protein sequence identity to a putative rhicadhesin receptor","volume":"58","author":"Gucciardo","year":"2007","journal-title":"J. Exp. Bot"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"153","DOI":"10.1128\/MMBR.64.1.153-179.2000","article-title":"Microbial relatives of the seed storage proteins of higher plants: Conservation of structure and diversification of function during evolution of the cupin superfamily","volume":"64","author":"Dunwell","year":"2000","journal-title":"Microbiol. Mol. Biol. Rev"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"36726","DOI":"10.1074\/jbc.M006461200","article-title":"Tobacco nectarin I-purification and characterization as a germin-like, manganese superoxide dismutase implicated in the defense of floral reproductive tissues","volume":"275","author":"Carter","year":"2000","journal-title":"J. Biol. Chem"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"181","DOI":"10.1104\/pp.106.083824","article-title":"The multigene family encoding germin-like proteins of barley. Regulation and function in basal host resistance","volume":"142","author":"Zimmerman","year":"2006","journal-title":"Plant Physiol"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"342","DOI":"10.1080\/07352680802333938","article-title":"Germin and Germin-like Proteins: Evolution, Structure, and Function","volume":"27","author":"Dunwell","year":"2008","journal-title":"Crit. Rev. Plant Sci"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"499","DOI":"10.1016\/j.plantsci.2009.08.012","article-title":"Germins: A diverse protein family important for crop improvement","volume":"177","author":"Davidson","year":"2009","journal-title":"Plant Sci"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"381","DOI":"10.1007\/s11103-004-3475-x","article-title":"Germin-like protein gene family of a moss, Physcomitrella patents, phylogenetically falls into two characteristic new clades","volume":"56","author":"Nakata","year":"2004","journal-title":"Plant Mol. Biol"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"44","DOI":"10.1016\/S0014-5793(01)02135-4","article-title":"Two isoforms of a nucleotide-sugar pyrophosphatase\/phosphodiesterase from barley leaves (Hordeum vulgare L.) are distinct oligomers of HvGLP1, a germin-like protein","volume":"490","author":"Munoz","year":"2001","journal-title":"FEBS Lett"},{"key":"ref_11","first-page":"95","article-title":"Analysis of transcriptional expression induced in Capsicum chinense BG-3821 under conditions of biotic and abiotic stress","volume":"42","year":"2008","journal-title":"Agrociencia"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"276","DOI":"10.1080\/07060660509507225","article-title":"Inducible gene expression by pepper huasteco virus in Capsicum chinense plants with resistance to geminivirus infections","volume":"27","year":"2005","journal-title":"Can. J. Plant Pathol"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"135","DOI":"10.1146\/annurev.phyto.44.070505.143425","article-title":"Significance of inducible defense-related proteins in infected plants","volume":"44","author":"Rep","year":"2006","journal-title":"Annu. Rev. Phytopathol"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"620","DOI":"10.1186\/1471-2164-11-620","article-title":"Identification and an\u00e1lisis of the germin-like gene family in soybean","volume":"11","author":"Lu","year":"2010","journal-title":"BMC Genomics"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"925","DOI":"10.1016\/j.bbrc.2007.03.097","article-title":"Characterization of wheat germin (oxalate oxidase) expressed by Pichia pastoris","volume":"356","author":"Pan","year":"2007","journal-title":"Biochem. Biophys. Res. Commun"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"53","DOI":"10.1016\/j.jbiotec.2003.10.026","article-title":"Heterologous expression of barley and wheat oxalate oxidase in an E. coli txB gor double mutant","volume":"109","author":"Cassland","year":"2004","journal-title":"J. Biotechnol"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"1036","DOI":"10.1038\/80954","article-title":"Germin is a manganese containing homohexamer with oxalate oxidase and superoxide dismutase activities","volume":"7","author":"Woo","year":"2000","journal-title":"Nat. Struct. Biol"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"286","DOI":"10.1104\/pp.108.128348","article-title":"A germin-like protein gene family functions as a complex quantitative trait locus conferring broad-spectrum disease resistance in rice","volume":"149","author":"Manosalva","year":"2009","journal-title":"Plant Physiol"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"672","DOI":"10.1111\/j.1744-7909.2006.00266.x","article-title":"Species and organ diversity in the effects of hydrogen peroxide on superoxide dismutase activity in vitro","volume":"48","author":"Cheng","year":"2006","journal-title":"J. Integr. Plant Biol"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"179","DOI":"10.1534\/genetics.106.058156","article-title":"Spatial and temporal divergence of expression in duplicated barley germin-like protein-encoding genes","volume":"174","author":"Federico","year":"2006","journal-title":"Genetics"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"1126","DOI":"10.1104\/pp.105.073700","article-title":"Silencing of a germin-like gene in Nicotiana attenuata improves performance of native herbivores","volume":"140","author":"Lou","year":"2006","journal-title":"Plant Physiol"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"1112","DOI":"10.1094\/MPMI-20-9-1112","article-title":"Induction of a grapevine germin-like protein (VvGLP3) gene is closely linked to the site of Erysiphe necator infection: A possible role in defense?","volume":"20","author":"Godfrey","year":"2007","journal-title":"Mol. Plant-Microbe Interact"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"325","DOI":"10.1016\/S1369-5266(02)00275-3","article-title":"Cross talk between signaling pathways in pathogen defense","volume":"5","author":"Kunkel","year":"2002","journal-title":"Curr. Opin. Plant Biol"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1149","DOI":"10.1104\/pp.104.053389","article-title":"Major signaling pathways modulate Arabidopsis glucosinolate accumulation and response to both phloem-feeding and chewing insects","volume":"138","author":"Mewis","year":"2005","journal-title":"Plant Physiol"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"4244","DOI":"10.1128\/IAI.66.9.4244-4253.1998","article-title":"Comparison of serum resistance by defined lipopolysaccharide mutants and an acapsular mutant of uropathogenic Escherichia coli O75:K5","volume":"66","author":"Burns","year":"1998","journal-title":"Infect. Immun"},{"key":"ref_26","unstructured":"Sambrook, J., Fritsch, E.F., and Maniatis, T (1989). Molecular Cloning: A Laboratory Manual, Cold Spring Harbor Laboratory Press."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1023\/B:BILE.0000009465.08712.a6","article-title":"Expression of ornithine decarboxylase of Coccidioides immitis in three Escherichia coli strains carrying the lamdba DE3 lysogen and an E. coli EWH319 strain odc\u2212 null mutant","volume":"26","year":"2004","journal-title":"Biotechnol. Lett"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"1091","DOI":"10.1104\/pp.107.4.1091","article-title":"Tissue-specific expression of germin-like oxalate oxidase during development and fungal infection of barley seedlings","volume":"107","author":"Dumas","year":"1995","journal-title":"Plant Physiol"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"276","DOI":"10.1016\/0003-2697(71)90370-8","article-title":"Superoxide dismutase: Improved assays and an assay applicable to acrylamide gels","volume":"44","author":"Beauchamp","year":"1971","journal-title":"Anal. Biochem"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"139","DOI":"10.21273\/HORTSCI.36.1.139","article-title":"Characterization of resistance to pepper huasteco geminivirus in chili Peppers from Yucat\u00e1n, M\u00e9xico","volume":"36","year":"2001","journal-title":"Hortscience"},{"key":"ref_31","unstructured":"Available online: http:\/\/expasy.org\/tools\/proteomics\/post-translational_modification."}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/12\/11\/7301\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T21:57:49Z","timestamp":1760219869000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/12\/11\/7301"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2011,10,25]]},"references-count":31,"journal-issue":{"issue":"11","published-online":{"date-parts":[[2011,11]]}},"alternative-id":["ijms12117301"],"URL":"https:\/\/doi.org\/10.3390\/ijms12117301","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2011,10,25]]}}}