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Versatility of germin-like proteins in their sequences, expressions, and functions

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Abstract

Germin-like proteins (GLPs) are evolutionary conserved ubiquitous plant glycoproteins belonging to the cupin superfamily. A large number of GLP family members have been identified from different higher and lower plant species, and those have been classified into different subfamilies. Although three histidine residues (H) and one glutamate residue (E) in germin box B and C were conserved among all the GLP subfamily members, how the sequences of one subfamily member differ from the other is unclear. Progress in the field of genomics, transcriptomics, and proteomics has made it possible to understand the variation at gene level among different GLP members from diverse genera and also their biological significances. GLPs from different plant species were found to have various enzymatic properties including oxalate oxidase (OxO), superoxide dismutase (SOD), ADP glucose pyrophosphatase/phosphodiesterase (AGPPase), and polyphenol oxidase (PPO) activities. ‘Omics’ study demonstrated the expression as well as involvement of GLP family members in almost every part of higher plants as well as in lower plants. Additionally, GLPs from different species were reported to be involved in biotic as well as abiotic stresses and also in the growth and development. This review describes the present research status of GLPs from different plant species, their expressions, and functional significances. Sequence variation was detected among GLP subfamily members at the amino acid level, and based on the sequence variation and phylogenetic analyses, two new GLP subfamilies have been proposed in this review.

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References

  • Abebe T, Skadsen RW, Kaeppler HF (2004) Cloning and identification of highly expressed genes in barley lemma and palea. Crop Sci 44:942–950

    Article  CAS  Google Scholar 

  • Alexandrov NN, Brover VV, Freidin S, Troukhan ME, Tatarinova TV, Zhang H, Swaller TJ, Lu YP, Bouck J, Flavell RB, Feldmann KA (2009) Insights into corn genes derived from large-scale cDNA sequencing. Plant Mol Biol 69:179–194

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Alvarez S, Marsh EL, Schroeder SG, Schachtman DP (2008) Metabolomic and proteomic changes in the xylem sap of maize under drought. Plant Cell Environ 31:325–340

    Article  CAS  PubMed  Google Scholar 

  • Anaya-López JL, Pérez-Mora E, Torres-Pacheco I, González-Chavira M, Muñoz-Sánchez CI, Guevara-Olvera L, Guevara-González RG, Ochoa-Alejo N, Rivera-Bustamante RF (2005) Inducible gene expression by Pepper huasteco virus in Capsicum chinense plants with resistance to geminivirus infections. Can J Plant Pathol 27:276–282

    Article  Google Scholar 

  • Armstrong JS, Abdel-Mageed H, Fokar M, Allen R, Adamczyk JJ (2013) Dietary effects of cotton tissue expressing germin like protein on beet armyworm (Lepidoptera: Noctuidae) growth, survival and pupation. Fla Entomol 96:693–700

    Article  CAS  Google Scholar 

  • Aubry C, Morere-Le Paven M-C, Chateigner-Boutin A-L, Teulat-Merah B, Ricoult C, Peltier D, Jalouzot R, Limami AM (2003) A gene encoding a germin-like protein, identified by a cDNA-AFLP approach, is specifically expressed during germination of Phaseolus vulgaris. Planta 217:466–475

    Article  CAS  PubMed  Google Scholar 

  • Banerjee J, Das N, Dey P, Maiti MK (2010) Transgenically expressed rice germin-like protein1 in tobacco causes hyper-accumulation of H2O2 and reinforcement of the cell wall components. Biochem Biophys Res Commun 402:637–643

    Article  CAS  PubMed  Google Scholar 

  • Banerjee J, Magnani R, Nair M, Dirk LM, DeBolt S, Maiti IB, Houtz RL (2013) Calmodulin-mediated signal transduction pathways in Arabidopsis are fine-tuned by methylation. Plant Cell 25:4493–4511

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Banerjee J, Maiti MK (2010) Functional role of rice germin-like protein1 in regulation of plant height and disease resistance. Biochem Biophys Res Commun 394:178–183

    Article  CAS  PubMed  Google Scholar 

  • Barrera-Pacheco A, Joaquin-Ramos A, Torres-Pacheco I, Gonzalez-Chavira MM, Perez-Perez MC, Guevara-Olvera L, Guevara-Gonzalez RG (2008) Analysis of transcriptional expression induced in Capsicum chinense BG-3821 under conditions of biotic and abiotic stress. Agrociencia 42:95–106

    Google Scholar 

  • Bernier F, Berna A (2001) Germins and germin-like proteins: plant do-all proteins. But what do they do exactly? Plant Physiol Biochem 39:545–554

    Article  CAS  Google Scholar 

  • Bishop-Hurley S, Gardner R, Walter C (2003) Isolation and molecular characterization of genes expressed during somatic embryo development in Pinus radiata. Plant Cell Tissue Org Cult 74:267–281

    Article  CAS  Google Scholar 

  • Bolwell GP, Butt VS, Davies DR, Zimmerlin A (1995) The origin of the oxidative burst in plants. Free Radic Res 23:517–532

    Article  CAS  PubMed  Google Scholar 

  • Bonasera JM, Beer SV (2002) Gene expression in apple in response to inoculation with Erwinia amylovora. Acta Horticult (ISHS) 590:7

    Google Scholar 

  • Breen J, Bellgard M (2010) Germin-like proteins (GLPs) in cereal genomes: gene clustering and dynamic roles in plant defence. Funct Integr Genomics 10(4):463–476

    Article  CAS  PubMed  Google Scholar 

  • Bruno L, Spadafora ND, Iaria D, Chiappetta A, Bitonti MB (2014) Developmental stimuli and stress factors affect expression of ClGLP1, an emerging allergen-related gene in Citrus limon. Plant Physiol Biochem 79:31–40

    Article  CAS  PubMed  Google Scholar 

  • Campbell MA, Herrmann LM, Colvin J (1998) The electronic plant gene register. Plant Physiol 118:711–712

    Article  Google Scholar 

  • Canales J, Avila C, Cánovas FM (2011) A maritime pine antimicrobial peptide involved in ammonium nutrition. Plant Cell Environ 34:1443–1453

    Article  CAS  PubMed  Google Scholar 

  • Cannon SB, Mitra A, Baumgarten A, Young ND, May G (2004) The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana. BMC Plant Biol 4:10

    Article  PubMed Central  PubMed  Google Scholar 

  • Carrillo M, Goodwin P, Leach J, Leung H, Vera Cruz C (2009) Phylogenomic relationships of rice oxalate oxidases to the cupin superfamily and their association with disease resistance QTL. Rice 2:67–79

    Article  Google Scholar 

  • Carter C, Graham RA, Thornburg RW (1998) Arabidopsis thaliana contains a large family of germin-like proteins: characterization of cDNA and genomic sequences encoding 12 unique family members. Plant Mol Biol 38:929–943

    Article  CAS  PubMed  Google Scholar 

  • Carter C, Graham RA, Thornburg RW (1999) Nectarin I is a novel, soluble germin-like protein expressed in the nectar of Nicotiana sp. Plant Mol Biol 41:207–216

    Article  CAS  PubMed  Google Scholar 

  • Carter C, Thornburg R (1999) Germin-like proteins: structure, phylogeny, and function. J Plant Biol 42:97–108

    Article  CAS  Google Scholar 

  • Carter C, Thornburg RW (2000) Tobacco nectarin I. Purification and characterization as a germin-like, manganese superoxide dismutase implicated in the defense of floral reproductive tissues. J Biol Chem 275:36726–36733

    Article  CAS  PubMed  Google Scholar 

  • Chakrabarty D, Trivedi PK, Shri M, Misra P, Asif MH, Dubey S, Kumar S, Rai A, Tiwari M, Shukla D, Pandey A, Nigam D, Tripathi RD, Tuli R (2010) Differential transcriptional expression following thidiazuron-induced callus differentiation developmental shifts in rice. Plant Biol (Stuttg) 12:46–59

    Article  CAS  Google Scholar 

  • Chandrika NNP, Sundaravelpandian K, Yu S-M, Schmidt W (2013) ALFIN-LIKE 6 is involved in root hair elongation during phosphate deficiency in Arabidopsis. New Phytol 198:709–720

    Article  CAS  PubMed  Google Scholar 

  • Chattopadhyay T (2014) In silico analysis of the germinlike protein multigene family members of tomato with predicted oxalate oxidase activity. Int J Agric Environ Biotechnol 7:10

    Google Scholar 

  • Che P, Lall S, Howell S (2007) Developmental steps in acquiring competence for shoot development in Arabidopsis tissue culture. Planta 226:1183–1194

    Article  CAS  PubMed  Google Scholar 

  • Chee KY, Tan PL, Nadarajah K (2012) Characterisation of the barley oxalate oxidase gene and generation of rice transformant. Biotechnol 11(5):263–271

    Article  CAS  Google Scholar 

  • Chen X, Wang M, Holbrook C, Culbreath A, Liang X, Brenneman T, Guo B (2011) Identification and characterization of a multigene family encoding germin-like proteins in cultivated peanut (Arachis hypogaea L.). Plant Mol Biol Report 29:389–403

    Article  CAS  Google Scholar 

  • Cheng X, Huang X, Liu S, Tang M, Hu W, Pan S (2014) Characterization of germin-like protein with polyphenol oxidase activity from Satsuma mandarine. Biochem Biophys Res Commun 449:313–318

    Article  CAS  PubMed  Google Scholar 

  • Chitteti BR, Peng Z (2007) Proteome and phosphoproteome dynamic change during cell dedifferentiation in Arabidopsis. Proteomics 7:1473–1500

    Article  CAS  PubMed  Google Scholar 

  • Christensen AB, Thordal-Christensen H, Zimmermann G, Gjetting T, Lyngkjaer MF, Dudler R, Schweizer P (2004) The germinlike protein GLP4 exhibits superoxide dismutase activity and is an important component of quantitative resistance in wheat and barley. Mol Plant Microbe Interact 17:109–117

    Article  CAS  PubMed  Google Scholar 

  • Davidson R, Manosalva P, Snelling J, Bruce M, Leung H, Leach J (2010) Rice germin-like proteins: allelic diversity and relationships to early stress responses. Rice 3:43–55

    Article  Google Scholar 

  • Davidson RM, Reeves PA, Manosalva PM, Leach JE (2009) Germins: a diverse protein family important for crop improvement. Plant Sci 177:499–510

    Article  CAS  Google Scholar 

  • De Carvalho MCDCG, Caldas DGG, Carneiro RT, Moon DH, Salvatierra GR, Franceschini LM, De Andrade A, Celedon PAF, ODA S, Labate CA (2008) SAGE transcript profiling of the juvenile cambial region of Eucalyptus grandis. Tree Physiol 28:905–919

    Article  Google Scholar 

  • Delporte F, Muhovski Y, Pretova A, Watillon B (2013) Analysis of expression profiles of selected genes associated with the regenerative property and the receptivity to gene transfer during somatic embryogenesis in Triticum aestivum L. Mol Biol Rep 40:5883–5906

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Doll J, Hause B, Demchenko K, Pawlowski K, Krajinski F (2003) A member of the germin-like protein family is a highly conserved mycorrhiza-specific induced gene. Plant Cell Physiol 44:1208–1214

    Article  CAS  PubMed  Google Scholar 

  • Domon JM, Dumas B, Lainé E, Meyer Y, David A, David H (1995) Three glycosylated polypeptides secreted by several embryogenic cell cultures of pine show highly specific serological affinity to antibodies directed against the wheat germin apoprotein monomer. Plant Physiol 108:141–148

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Druka A, Kudrna D, Kannangara CG, von Wettstein D, Kleinhofs A (2002) Physical and genetic mapping of barley (Hordeum vulgare) germin-like cDNAs. Proc Natl Acad Sci U S A 99:850–855

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Dumas B, Sailland A, Cheviet JP, Freyssinet G, Pallett K (1993) Identification of barley oxalate oxidase as a germin-like protein. C R Acad Sci III 316:793–798

    CAS  PubMed  Google Scholar 

  • Dunwell JM, Gibbings JG, Mahmood T, Saqlan Naqvi SM (2008) Germin and germin-like proteins: evolution, structure, and function. Crit Rev Plant Sci 27:342–375

    Article  CAS  Google Scholar 

  • El-Sharkawy I, Mila I, Bouzayen M, Jayasankar S (2010) Regulation of two germin-like protein genes during plum fruit development. J Exp Bot 61(6):1761–1770

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Faghani E, Gharechahi J, Komatsu S, Mirzaei M, Ali Khavarinejad R, Najafi F, Karimi Farsad L, Hosseini Salekdeh G (2015) Data in support of comparative physiology and proteomic analysis of two wheat genotypes contrasting in drought tolerance. Data Brief 2:26–28

    Article  PubMed Central  PubMed  Google Scholar 

  • Fan Z, Gu H, Chen X, Song H, Wang Q, Liu M, Qu L-J, Chen Z (2005) Cloning and expression analysis of Zmglp1, a new germin-like protein gene in maize. Biochem Biophys Res Commun 331:1257–1263

    Article  CAS  PubMed  Google Scholar 

  • Fernandez P, Paniego N, Lew S, Hopp H, Heinz R (2003) Differential representation of sunflower ESTs in enriched organ-specific cDNA libraries in a small scale sequencing project. BMC Genomics 4:40

    Article  PubMed Central  PubMed  Google Scholar 

  • Ferrarini A, De Stefano M, Baudouin E, Pucciariello C, Polverari A, Puppo A, Delledonne M (2008) Expression of Medicago truncatula genes responsive to nitric oxide in pathogenic and symbiotic conditions. Mol Plant Microbe Interact 21:781–790

    Article  CAS  PubMed  Google Scholar 

  • Ficke A, Gadoury DM, Seem RC, Godfrey D, Dry IB (2004) Host barriers and responses to Uncinula necator in developing grape berries. Phytopathology 94(5):438–445

    Article  PubMed  Google Scholar 

  • Friedmann M, Ralph SG, Aeschliman D, Zhuang J, Ritland K, Ellis BE, Bohlmann J, Douglas CJ (2007) Microarray gene expression profiling of developmental transitions in Sitka spruce (Picea sitchensis) apical shoots. J Exp Bot 58:593–614

    Article  CAS  PubMed  Google Scholar 

  • Fujii H, Shimada T, Sugiyama A, Nishikawa F, Endo T, Nakano M, Ikoma Y, Shimizu T, Omura M (2007) Profiling ethylene-responsive genes in mature mandarin fruit using a citrus 22K oligoarray. Plant Sci 173:340–348

    Article  CAS  Google Scholar 

  • Gion J-M, Lalanne C, Le Provost G, Ferry-Dumazet H, Paiva J, Chaumeil P, Frigerio J-M, Brach J, Barré A, de Daruvar A, Claverol S, Bonneu M, Sommerer N, Negroni L, Plomion C (2005) The proteome of maritime pine wood forming tissue. Proteomics 5:3731–3751

    Article  CAS  PubMed  Google Scholar 

  • Godfrey D, Able AJ, Dry IB (2007) Induction of a grapevine germin-like protein (VvGLP3) gene is closely linked to the site of Erysiphe necator infection: a possible role in defense? Mol Plant Microbe Interact 20:1112–1125

    Article  CAS  PubMed  Google Scholar 

  • Groover AT, Mansfield SD, DiFazio SP, Dupper G, Fontana JR, Millar R, Wang Y (2006) The Populus homeobox gene ARBORKNOX1 reveals overlapping mechanisms regulating the shoot apical meristem and the vascular cambium. Plant Mol Biol 61:917–932

    Article  CAS  PubMed  Google Scholar 

  • Gucciardo S, Wisniewski J-P, Brewin NJ, Bornemann S (2007) A germin-like protein with superoxide dismutase activity in pea nodules with high protein sequence identity to a putative rhicadhesin receptor. J Exp Bot 58:1161–1171

    Article  CAS  PubMed  Google Scholar 

  • Guevara-Olvera L, Ruíz-Nito ML, Rangel-Cano RM, Torres-Pacheco I, Rivera-Bustamante RF, Muñoz-Sánchez CI, González-Chavira MM, Cruz-Hernandez A, Guevara-González RG (2012) Expression of a germin-like protein gene (CchGLP) from a geminivirus-resistant pepper (Capsicum chinense Jacq.) enhances tolerance to geminivirus infection in transgenic tobacco. Physiol Mol Plant Pathol 78:45–50

    Article  CAS  Google Scholar 

  • Güimil S, Chang H-S, Zhu T, Sesma A, Osbourn A, Roux C, Ioannidis V, Oakeley EJ, Docquier M, Descombes P, Briggs SP, Paszkowski U (2005) Comparative transcriptomics of rice reveals an ancient pattern of response to microbial colonization. Proc Natl Acad Sci U S A 102:8066–8070

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Ham B-K, Li G, Kang B-H, Zeng F, Lucas WJ (2012) Overexpression of Arabidopsis plasmodesmata germin-like proteins disrupts root growth and development. Plant Cell 24:3630–3648

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Heintzen C, Fischer R, Melzer S, Kappeler K, Apel K, Staiger D (1994) Circadian oscillations of a transcript encoding a germin-like protein that is associated with cell walls in young leaves of the long-day plant Sinapis alba L. Plant Physiol 106:905–915

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Himmelbach A, Liu L, Zierold U, Altschmied L, Maucher H, Beier F, Müller D, Hensel G, Heise A, Schützendübel A, Kumlehn J, Schweizer P (2010) Promoters of the barley germin-like GER4 gene cluster enable strong transgene expression in response to pathogen attack. Plant Cell 22:937–952

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Holmes-Davis R, Tanaka CK, Vensel WH, Hurkman WJ, McCormick S (2005) Proteome mapping of mature pollen of Arabidopsis thaliana. Proteomics 5:4864–4884

    Article  CAS  PubMed  Google Scholar 

  • Hu Y, Sun G (2010) Leaf nitrogen dioxide uptake coupling apoplastic chemistry, carbon/sulfur assimilation, and plant nitrogen status. Plant Cell Rep 29:1069–1077

    Article  CAS  PubMed  Google Scholar 

  • Hwang J, Oh CS, Kang BC (2013) Translation elongation factor 1B (eEF1B) is an essential host factor for tobacco mosaic virus infection in plants. Virology 439:105–114

    Article  CAS  PubMed  Google Scholar 

  • Jiang Y, Yang B, Harris NS, Deyholos MK (2007) Comparative proteomic analysis of NaCl stress-responsive proteins in Arabidopsis roots. J Exp Bot 58:3591–3607

    Article  CAS  PubMed  Google Scholar 

  • Ke Y, Han G, He H, Li J (2009) Differential regulation of proteins and phosphoproteins in rice under drought stress. Biochem Biophys Res Commun 379:133–138

    Article  CAS  PubMed  Google Scholar 

  • Khuri S, Bakker FT, Dunwell JM (2001) Phylogeny, function, and evolution of the cupins, a structurally conserved, functionally diverse superfamily of proteins. Mol Biol Evol 18(4):593–605

    Article  CAS  PubMed  Google Scholar 

  • Kim HJ, Pesacreta TC, Triplett BA (2004) Cotton-fiber germinlike protein. II: immunolocalization, purification, and functional analysis. Planta 218:525–535

    Article  CAS  PubMed  Google Scholar 

  • Kim HJ, Triplett BA (2004) Cotton fiber germin-like protein I. Molecular cloning and gene expression. Planta 218(4):516–524

    Article  CAS  PubMed  Google Scholar 

  • Kishi-Kaboshi M, Muto H, Takeda A, Murata T, Hasebe M, Watanabe Y (2014) Localization of tobacco germin-like protein 1 in leaf intercellular space. Plant Physiol Biochem 85C:1–8

    Article  CAS  Google Scholar 

  • Kleczkowski LA (2001) A new player in the starch field. Plant Physiol Biochem 39:759–761

    Article  CAS  Google Scholar 

  • Knecht K, Seyffarth M, Desel C, Thurau T, Sherameti I, Lou B, Oelmüller R, Cai D (2010) Expression of BvGLP-1 encoding a germin-like protein from sugar beet in Arabidopsis thaliana leads to resistance against phytopathogenic fungi. Mol Plant Microbe Interact 23:446–457

    Article  CAS  PubMed  Google Scholar 

  • Kondo K, Yamada K, Nakagawa A, Takahashi M, Morikawa H, Sakamoto A (2008) Molecular characterization of atmospheric NO2-responsive germin-like proteins in azalea leaves. Biochem Biophys Res Commun 377:857–861

    Article  CAS  PubMed  Google Scholar 

  • Kottapalli KR, Rakwal R, Satoh K, Shibato J, Kottapalli P, Iwahashi H, Kikuchi S (2007) Transcriptional profiling of indica rice cultivar IET8585 (Ajaya) infected with bacterial leaf blight pathogen Xanthomonas oryzae pv oryzae. Plant Physiol Biochem 45:834–850

    Article  CAS  PubMed  Google Scholar 

  • Krugman T, Chagué V, Peleg Z, Balzergue S, Just J, Korol AB, Nevo E, Saranga Y, Chalhoub B, Fahima T (2010) Multilevel regulation and signalling processes associated with adaptation to terminal drought in wild emmer wheat. Funct Integr Genomics 10:167–186

    Article  CAS  PubMed  Google Scholar 

  • Kukavica B, Vucinić Z, Vuletić M (2005) Superoxide dismutase, peroxidase, and germin-like protein activity in plasma membranes and apoplast of maize roots. Protoplasma 226:191–197

    Article  CAS  PubMed  Google Scholar 

  • Lane BG, Dunwell JM, Ray JA, Schmitt MR, Cuming AC (1993) Germin, a protein marker of early plant development, is an oxalate oxidase. J Biol Chem 268:12239–12242

    CAS  PubMed  Google Scholar 

  • León-Galván F, de Jesús J-RA, Torres-Pacheco I, Barba de la Rosa AP, Guevara-Olvera L, González-Chavira MM, Ocampo-Velazquez RV, Rico-García E, Guevara-González RG (2011) A germin-like protein gene (CchGLP) of Capsicum chinense Jacq. is induced during incompatible interactions and displays Mn-superoxide dismutase activity. Int J Mol Sci 12:7301–7313

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Li H-F, Zhu F-H, Li H-Y, Zhu W, Chen X-P, Hong Y-B, Liu H-Y, Wu H, Liang X-Q (2013) Proteomic identification of gravitropic response genes in peanut gynophores. J Proteomics 93:303–313

    Article  CAS  PubMed  Google Scholar 

  • Little D, Gouhier-Darimont C, Bruessow F, Reymond P (2007) Oviposition by pierid butterflies triggers defense responses in Arabidopsis. Plant Physiol 143:784–800

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Liu G, Greenshields DL, Sammynaiken R, Hirji RN, Selvaraj G, Wei Y (2007) Targeted alterations in iron homeostasis underlie plant defense responses. J Cell Sci 120(4):596–605

    Article  CAS  PubMed  Google Scholar 

  • Lou P, Kang J, Zhang G, Bonnema G, Fang Z, Wang X (2007) Transcript profiling of a dominant male sterile mutant (Ms-cd1) in cabbage during flower bud development. Plant Sci 172:111–119

    Article  CAS  Google Scholar 

  • Lou Y, Baldwin IT (2006) Silencing of a germin-like gene in Nicotiana attenuata improves performance of native herbivores. Plant Physiol 140:1126–1136

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lu M, Han YP, Gao JG, Wang XJ, Li WB (2010) Identification and analysis of the germin-like gene family in soybean. BMC Genomics 11:620

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Mago R, Tabe L, Vautrin S, Šimková H, Kubaláková M, Upadhyaya N, Berges H, Kong X, Breen J, Doležel J, Appels R, Ellis JG, Spielmeyer W (2014) Major haplotype divergence including multiple germin-like protein genes, at the wheat Sr2 adult plant stem rust resistance locus. BMC Plant Biol 14:379

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Mandelc S, Timperman I, Radišek S, Devreese B, Samyn B, Javornik B (2013) Comparative proteomic profiling in compatible and incompatible interactions between hop roots and Verticillium albo-atrum. Plant Physiol Biochem 68:23–31

    Article  CAS  PubMed  Google Scholar 

  • Manjasetty BA, Niesen FH, Scheich C, Roske Y, Goetz F, Behlke J, Sievert V, Heinemann U, Büssow K (2005) X-ray structure of engineered human aortic preferentially expressed protein-1 (APEG-1). BMC Struct Biol 5:21

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Manosalva PM, Davidson RM, Liu B, Zhu X, Hulbert SH, Leung H, Leach JE (2009) A germin-like protein gene family functions as a complex quantitative trait locus conferring broad-spectrum disease resistance in rice. Plant Physiol 149:286–296

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Masclaux-Daubresse C, Purdy S, Lemaitre T, Pourtau N, Taconnat L, Renou J-P, Wingler A (2007) Genetic variation suggests interaction between cold acclimation and metabolic regulation of leaf senescence. Plant Physiol 143:434–446

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Mathieu M, Lelu-Walter MA, Blervacq AS, David H, Hawkins S, Neutelings G (2006) Germin-like genes are expressed during somatic embryogenesis and early development of conifers. Plant Mol Biol 61:615–627

    Article  CAS  PubMed  Google Scholar 

  • Membre N, Bernier F, Staiger D, Berna A (2000) Arabidopsis thaliana germin-like proteins: common and specific features point to a variety of functions. Planta 211:345–354

    Article  CAS  PubMed  Google Scholar 

  • Membré N, Bernier F (1998) The rice genome expresses at least six different genes for oxalate oxidase/germinlike proteins (GenBank AF032971, AF032972, AF032973, AF032974, AF032975, AF032976) (PGR98-021). Plant Physiol 116:868

    Google Scholar 

  • Membré N, Berna A, Neutelings G, David A, David H, Staiger D, Sáez Vásquez J, Raynal M, Delseny M, Bernier F (1997) cDNA sequence, genomic organization and differential expression of three Arabidopsis genes for germin/oxalate oxidase-like proteins. Plant Mol Biol 35:459–469

    Article  PubMed  Google Scholar 

  • Michalowski CB, Bohnert HJ (1992) Nucleotide sequence of a root-specific transcript encoding a germin-like protein from the halophyte Mesembryanthemum crystallinum. Plant Physiol 100:537–538

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Morel A, Teyssier C, Trontin J-F, Eliášová K, Pešek B, Beaufour M, Morabito D, Boizot N, Le Metté C, Belal-Bessai L, Reymond I, Harvengt L, Cadene M, Corbineau F, Vágner M, Label P, Lelu-Walter M-A (2014) Early molecular events involved in Pinus pinaster Ait. somatic embryo development under reduced water availability: transcriptomic and proteomic analyses. Physiol Plant 152:184–201

    Article  CAS  PubMed  Google Scholar 

  • Müller R, Morant M, Jarmer H, Nilsson L, Nielsen TH (2007) Genome-wide analysis of the Arabidopsis leaf transcriptome reveals interaction of phosphate and sugar metabolism. Plant Physiol 143:156–171

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Nakata M, Shiono T, Watanabe Y, Satoh T (2002) Salt stress-induced dissociation from cells of a germin-like protein with Mn-SOD activity and an increase in its mRNA in a moss, Barbula unguiculata. Plant Cell Physiol 43:1568–1574

    Article  CAS  PubMed  Google Scholar 

  • Nakata M, Watanabe Y, Sakurai Y, Hashimoto Y, Matsuzaki M, Takahashi Y, Satoh T (2004) Germin-like protein gene family of a moss, Physcomitrella patens, phylogenetically falls into two characteristic new clades. Plant Mol Biol 56:381–395

    Article  CAS  PubMed  Google Scholar 

  • Neutelings G, Domon JM, Membré N, Bernier F, Meyer Y, David A, David H (1998) Characterization of a germin-like protein gene expressed in somatic and zygotic embryos of pine (Pinus caribaea Morelet). Plant Mol Biol 38:1179–1190

    Article  CAS  PubMed  Google Scholar 

  • Noguero M, Le Signor C, Vernoud V, Bandyopadhyay K, Sanchez M, Fu C, Torres-Jerez I, Wen J, Mysore KS, Gallardo K, Udvardi M, Thompson R, Verdier J (2015) DASH transcription factor impacts Medicago truncatula seed size by its action on embryo morphogenesis and auxin homeostasis. Plant J 81:453–466

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Noir S, Bräutigam A, Colby T, Schmidt J, Panstruga R (2005) A reference map of the Arabidopsis thaliana mature pollen proteome. Biochem Biophys Res Commun 337:1257–1266

    Article  CAS  PubMed  Google Scholar 

  • Ohmiya A, Tanaka Y, Kadowaki K, Hayashi T (1998) Cloning of genes encoding auxin-binding proteins (ABP19/20) from peach: significant peptide sequence similarity with germin-like proteins. Plant Cell Physiol 39:492–499

    Article  CAS  PubMed  Google Scholar 

  • Ono M, Sage-Ono K, Inoue M, Kamada H, Harada H (1996) Transient increase in the level of mRNA for a germin-like protein in leaves of the short-day plant Pharbitis nil during the photoperiodic induction of flowering. Plant Cell Physiol 37:855–861

    Article  CAS  PubMed  Google Scholar 

  • Park C-J, An J-M, Shin Y-C, Kim K-J, Lee B-J, Paek K-H (2004) 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. Planta 219:797–806

    CAS  PubMed  Google Scholar 

  • Patnaik BB, Kim DH, Oh SH, Song Y-S, Chanh NDM, Kim JS, W-j J, Saha AK, Bindroo BB, Han YS (2012) Molecular cloning and characterization of novel Morus alba germin-like protein gene which encodes for a silkworm gut digestion-resistant antimicrobial protein. PLoS One 7:e50900

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Patnaik D, Khurana P (2001) Germins and germin like proteins: an overview. Indian J Exp Biol 39:191–200

    CAS  PubMed  Google Scholar 

  • Puppo A, Pauly N, Boscari A, Mandon K, Brouquisse R (2013) Hydrogen peroxide and nitric oxide: key regulators of the Legume-Rhizobium and mycorrhizal symbioses. Antioxid Redox Signal 18:2202–2219

    Article  CAS  PubMed  Google Scholar 

  • Reilly K, Bernal D, Cortés DF, Gómez-Vásquez R, Tohme J, Beeching JR (2007) Towards identifying the full set of genes expressed during cassava post-harvest physiological deterioration. Plant Mol Biol 64:187–203

    Article  CAS  PubMed  Google Scholar 

  • Rietz S, Bernsdorff FEM, Cai D (2012) Members of the germin-like protein family in Brassica napus are candidates for the initiation of an oxidative burst that impedes pathogenesis of Sclerotinia sclerotiorum. J Exp Bot 63:5507–5519

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Rodríguez-López M, Baroja-Fernández E, Zandueta-Criado A, Moreno-Bruna B, Muñoz FJ, Akazawa T, Pozueta-Romero J (2001) Two isoforms of a nucleotide-sugar pyrophosphatase/phosphodiesterase from barley leaves (Hordeum vulgare L.) are distinct oligomers of HvGLP1, a germin-like protein. FEBS Lett 490:44–48

    Article  PubMed  Google Scholar 

  • Rotthues A, Kappler J, Lichtfuss A, Kloos DU, Stahl DJ, Hehl R (2008) Post-harvest regulated gene expression and splicing efficiency in storage roots of sugar beet (Beta vulgaris L.). Planta 227:1321–1332

    Article  CAS  PubMed  Google Scholar 

  • Salvo SAGD, Hirsch CN, Buell CR, Kaeppler SM, Kaeppler HF (2014) Whole transcriptome profiling of maize during early somatic embryogenesis reveals altered expression of stress factors and embryogenesis-related genes. PLoS One 9:e111407

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Sarkar A, Rakwal R, Bhushan Agrawal S, Shibato J, Ogawa Y, Yoshida Y, Kumar Agrawal G, Agrawal M (2010) Investigating the impact of elevated levels of ozone on tropical wheat using integrated phenotypical, physiological, biochemical, and proteomics approaches. J Proteome Res 9:4565–4584

    Article  CAS  PubMed  Google Scholar 

  • Schweizer P, Christoffel A, Dudler R (1999) Transient expression of members of the germin-like gene family in epidermal cells of wheat confers disease resistance. Plant J 20:541–552

    Article  CAS  PubMed  Google Scholar 

  • Tabuchi T, Kumon T, Azuma T, Nanmori T, Yasuda T (2003) The expression of a germin-like protein with superoxide dismutase activity in the halophyte Atriplex lentiformis is differentially regulated by wounding and abscisic acid. Physiol Plant 118:523–531

    Article  CAS  Google Scholar 

  • Theologis A, Ecker JR, Palm CJ, Federspiel NA, Kaul S, White O, Alonso J, Altafi H, Araujo R, Bowman CL, Brooks SY, Buehler E, Chan A, Chao Q, Chen H, Cheuk RF, Chin CW, Chung MK, Conn L, Conway AB, Conway AR, Creasy TH, Dewar K, Dunn P, Etgu P, Feldblyum TV, Feng J, Fong B, Fujii CY, Gill JE, Goldsmith AD, Haas B, Hansen NF, Hughes B, Huizar L, Hunter JL, Jenkins J, Johnson-Hopson C, Khan S, Khaykin E, Kim CJ, Koo HL, Kremenetskaia I, Kurtz DB, Kwan A, Lam B, Langin-Hooper S, Lee A, Lee JM, Lenz CA, Li JH, Li Y, Lin X, Liu SX, Liu ZA, Luros JS, Maiti R, Marziali A, Militscher J, Miranda M, Nguyen M, Nierman WC, Osborne BI, Pai G, Peterson J, Pham PK, Rizzo M, Rooney T, Rowley D, Sakano H, Salzberg SL, Schwartz JR, Shinn P, Southwick AM, Sun H, Tallon LJ, Tambunga G, Toriumi MJ, Town CD, Utterback T, Van Aken S, Vaysberg M, Vysotskaia VS, Walker M, Wu D, Yu G, Fraser CM, Venter JC, Davis RW (2000) Sequence and analysis of chromosome 1 of the plant Arabidopsis thaliana. Nature 408:816–820

    Article  PubMed  Google Scholar 

  • Tucker MR, Roodbarkelari F, Truernit E, Adamski NM, Hinze A, Lohmüller B, Würschum T, Laux T (2013) Accession-specific modifiers act with ZWILLE/ARGONAUTE10 to maintain shoot meristem stem cells during embryogenesis in Arabidopsis. BMC Genomics 14:809

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Vallelian-Bindschedler L, Mösinger E, Métraux JP, Schweizer P (1998) Structure, expression and localization of a germin-like protein in barley (Hordeum vulgare L.) that is insolubilized in stressed leaves. Plant Mol Biol 37:297–308

    Article  CAS  PubMed  Google Scholar 

  • Villalobos D, Diaz-Moreno S, Said E-S, Canas R, Osuna D, Van Kerckhoven SH, Bautista R, Claros M, Canovas F, Canton F (2012) Reprogramming of gene expression during compression wood formation in pine: coordinated modulation of S-adenosylmethionine, lignin and lignan related genes. BMC Plant Biol 12:100

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wang T, Chen X, Zhu F, Li H, Li L, Yang Q, Chi X, Yu S, Liang X (2013) Characterization of peanut germin-like proteins, AhGLPs in plant development and defense. PLoS One 8:e61722

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Whittaker MM, Whittaker JW (2002) Characterization of recombinant barley oxalate oxidase expressed by Pichia pastoris. J Biol Inorg Chem 7:136–145

    Article  CAS  PubMed  Google Scholar 

  • Wissel K, Pettersson F, Berglund A, Jansson S (2003) What affects mRNA levels in leaves of field-grown aspen? A study of developmental and environmental influences. Plant Physiol 133:1190–1197

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wu S, Druka A, Horvath H, Kleinhofs A, Gamini Kannangara C, von Wettstein D (2000) Functional characterization of seed coat-specific members of the barley germin gene family. Plant Physiol Biochem 38:685–698

    Article  CAS  Google Scholar 

  • Yamahara T, Shiono T, Suzuki T, Tanaka K, Takio S, Sato K, Yamazaki S, Satoh T (1999) Isolation of a germin-like protein with manganese superoxide dismutase activity from cells of a moss, Barbula unguiculata. J Biol Chem 274:33274–33278

    Article  CAS  PubMed  Google Scholar 

  • Yang H, Kaur N, Kiriakopolos S, McCormick S (2006) EST generation and analyses towards identifying female gametophyte-specific genes in Zea mays L. Planta 224:1004–1014

    Article  CAS  PubMed  Google Scholar 

  • Zimmermann G, Bäumlein H, Mock H-P, Himmelbach A, Schweizer P (2006) The multigene family encoding germin-like proteins of barley. Regulation and function in basal host resistance. Plant Physiol 142:181–192

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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Acknowledgments

The authors like to acknowledge Bidhan Chandra Krishi Viswavidyalaya and Director of Research (BCKV) for providing the basic support needed for this review article.

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Correspondence to Joydeep Banerjee.

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Barman, A.R., Banerjee, J. Versatility of germin-like proteins in their sequences, expressions, and functions. Funct Integr Genomics 15, 533–548 (2015). https://doi.org/10.1007/s10142-015-0454-z

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