Skip to main content
Log in

Sunflower germin-like protein HaGLP1 promotes ROS accumulation and enhances protection against fungal pathogens in transgenic Arabidopsis thaliana

  • Original Paper
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

Key message

The novel sunflower gene HaGLP1 is the first germin-like protein characterized from the family Asteraceae. It alters the host redox status and confers protection against Sclerotinia sclerotiorum and Rhizoctonia solani.

Abstract

Germin-like proteins (GLPs) are a large, diverse and ubiquitous family of plant glycoproteins belonging to the Cupin super family. These proteins have been widely studied because of their diverse roles in important plant processes, including defence. The novel sunflower gene HaGLP1 encodes the first germin-like protein characterized from the family Asteraceae. To analyse whether constitutive in vivo expression of the HaGLP1 gene may lead to disease tolerance, we developed transgenic Arabidopsis plants that were molecularly characterized and biologically assessed after inoculation with Sclerotinia sclerotiorum or Rhizoctonia solani. HaGLP1 expression in Arabidopsis plants conferred tolerance to S. sclerotiorum at the first stages of disease and interfered with R. solani infection, thus giving rise to significant protection against the latter. Furthermore, HaGLP1 expression in Arabidopsis plants elevated endogenous ROS levels. HaGLP1-induced tolerance does not appear to be related to a constitutive induction of the plant defence or the ROS-related genes examined here. In conclusion, our data suggest that HaGLP1 is an interesting candidate for the engineering of plants with increased fungal tolerance and that this gene could also be useful for the selection of naturally overexpressing sunflower genotypes for conventional breeding purposes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Abbreviations

AOX1a :

Alternative oxidase 1a gene

ET:

Ethylene

GLP:

Germin-like protein

HaGLP1/HaGLP1:

Helianthus annuus germin-like protein 1 gene/protein

HvGER:

Hordeum vulgare germin-like protein

JA:

Jasmonic acid

LOX2 :

Lipoxygenase 2 gene

MLM:

Mixed-linear model

NptII:

Neomycin phosphototransferase II gene

Pnos:

Nopaline synthase promoter

PDF-1.2 :

Plant defensin 1.2 gene

PDF-1.4 :

Plant defensin 1.4 gene

PR-1 :

Pathogenesis-related protein 1 gene

ROS:

Reactive oxygen species

SA:

Salicylic acid

SOD:

Superoxide dismutase

Tnos:

Nopaline synthase terminator

VvGLP:

Vitis vinifera germin-like protein

WRKY70 :

WRKY70 transcription factor gene

WRKY25 :

WRKY25 transcription factor gene

References

  • Almasia NI (2009) Estudio genómico y funcional del péptido antimicrobiano SNAKIN-1. Ph.D. Dissertation, Universidad de Buenos Aires

  • Almasia NI, Bazzini A, Hopp HE, Vazquez-Rovere C (2008) Overexpression of snakin-1 gene enhances resistance to Rhizoctonia solani and Erwinia carotovora in transgenic potato plants. Mol Plant Pathol 9:329–338. doi:10.1111/j.1364-3703.2008.00469.x

    Article  CAS  PubMed  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. doi:10.1016/S0981-9428(01)01285-2

    Article  CAS  Google Scholar 

  • Blom N, Gammeltoft S, Brunak S (1999) Sequence and structure-based prediction of eukaryotic protein phosphorylation sites. J Mol Biol 294:1351–1362. doi:10.1006/jmbi.1999.3310

    Article  CAS  PubMed  Google Scholar 

  • Boland GJ, Hall R (1994) Index of plant hosts of Sclerotinia sclerotiorum. Can J Plant Pathol 16:93–108. doi:10.1080/07060669409500766

    Article  Google Scholar 

  • Canut H, Carrasco A, Galaud JP, Cassan C, Bouyssou H, Vita N, Ferrara P, Pont-Lezica R (1998) High affinity RGD-binding sites at the plasma membrane of Arabidopsis thaliana links the cell wall. Plant J 16:63–71

    Article  CAS  PubMed  Google Scholar 

  • Carter C, Thornburg RW (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. doi:10.1074/jbc.M006461200

    Article  CAS  PubMed  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 

  • Cessna SG, Sears VE, Dickman MB, Low PS (2000) Oxalic acid, a pathogenicity factor for Sclerotinia sclerotiorum, suppresses the oxidative burst of the host plant. Plant Cell 12:2191–2200. doi:10.1105/tpc.12.11.2191

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chauhan JS, Rao A, Raghava GPS (2013) In silico platform for prediction of N-, O- and C-glycosites in eukaryotic protein sequences. PLoS ONE 8:e67008. doi:10.1371/journal.pone.0067008

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Christensen AB, Thordal-Christensen H, Zimmermann G, Gjetting T, Lyngkjaer MF, Dudler R, Schweizer P (2004) The germin-like 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. doi:10.1094/MPMI.2004.17.1.109

    Article  CAS  PubMed  Google Scholar 

  • Custers JHHV, Harrison SJ, Sela-Buurlage MB, van Deventer E, Lageweg W, Howe PW, van der Meijs PJ, Ponstein AS, Simons BH, Melchers LS, Stuiver MH (2004) Isolation and characterisation of a class of carbohydrate oxidases from higher plants, with a role in active defence. Plant J 39:147–160. doi:10.1111/j.1365-313X.2004.02117.x

    Article  CAS  PubMed  Google Scholar 

  • Dai F, Xu T, Wolf GA, He Z (2006) Physiological and Molecular Features of the Pathosystem Arabidopsis thaliana L. -Sclerotinia sclerotiorum Libert. J Integr Plant Biol 48:44–52

    Article  CAS  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. doi:10.1016/j.plantsci.2009.08.012

    Article  CAS  Google Scholar 

  • Dezar CA, Gago GM, Gonzalez DH, Chan RL (2005) Hahb-4, a sunflower homeobox-leucine zipper gene, is a developmental regulator and confers drought tolerance to Arabidopsis thaliana plants. Transgenic Res 14:429–440

    Article  CAS  PubMed  Google Scholar 

  • Dezar CA, Giacomelli JI, Manavella PA, Ré DA, Alves-Ferreira M, Baldwin IT, Bonaventure G, Chan RL (2011) HAHB10, a sunflower HD-Zip II transcription factor, participates in the induction of flowering and in the control of phytohormone-mediated responses to biotic stress. J Exp Bot 62:1061–1076. doi:10.1093/jxb/erq339

    Article  CAS  PubMed  Google Scholar 

  • Di Rienzo JA (2009) fgstatistics version 2009. Accessed November 2014

  • Di Rienzo JA, Guzman AW, Casanoves F (2002) A multiple-comparisons method based on the distribution of the root node distance of a binary tree. J Agric Biol Environ Stat 7:129–142. doi:10.1198/10857110260141193

    Article  Google Scholar 

  • Di Rienzo JA, Casanoves F, Balzarini M, Gonzalez L, Tablada M, Robledo CW (2013) Infostat version 2013. http://www.infostat.com.ar/Accessed October 2013

  • Donaldson PA, Anderson T, Lane BG, Davidson AL, Simmonds DH (2001) Soybean plants expressing an active oligomeric oxalate oxidase from the wheat gf-2.8 (germin) gene are resistant to the oxalate-secreting pathogen Sclerotina sclerotiorum. Physiol Mol Plant Pathol 59:297–307. doi:10.1006/pmpp.2001.0369

    Article  CAS  Google Scholar 

  • Dong X, Ji R, Guo X, Foster SJ, Chen H, Dong C, Liu Y, Hu Q, Liu S (2008) Expressing a gene encoding wheat oxalate oxidase enhances resistance to Sclerotinia sclerotiorum in oilseed rape (Brassica napus). Planta 228:331–340. doi:10.1007/s00425-008-0740-2

    Article  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. doi:10.1073/pnas.022627999

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Dunwell JM (1998) Cupins: a new superfamily of functionally diverse proteins that include germins and plant storage proteins. Biotechnol Genet Eng Rev 15:1–32

    Article  CAS  PubMed  Google Scholar 

  • Dunwell JM, Gibbings JG, Mahmood T, Saqlan Naqvi SM (2008) Germin and germin-like proteins: evolution, structure, and function. CRC Crit Rev Plant Sci 27:342–375. doi:10.1080/07352680802333938

    Article  CAS  Google Scholar 

  • Ehrenbolger GF, Beracochea V, Pelufo L, Almasia NI, Vazquez Rovere C, Hopp HE, Paniego NB, Heinz RA, Lia VV (2012) Sunflower germin-like proteins: evolution, gene structure and functional characterization. In: ASAGIR (ed) Proc. 18th Int. Sunflower Conf. ASAGIR, Mar del Plata, Argentina, pp 586–592

  • Fernández P, Paniego N, Lew S, Hopp HE, Heinz RA (2003) Differential representation of sunflower ESTs in enriched organ-specific cDNA libraries in a small scale sequencing project. BMC Genom 4:40. doi:10.1186/1471-2164-4-40

    Article  Google Scholar 

  • Foley RC, Gleason CA, Anderson JP, Hamann T, Singh KB (2013) Genetic and Genomic Analysis of Rhizoctonia solani Interactions with Arabidopsis; Evidence of Resistance Mediated through NADPH Oxidases. PLoS One 8:e56814. doi:10.1371/journal.pone.0056814

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Frohman MA, Dush MK, Martin GR (1988) Rapid production of full-length cDNAs from rare transcripts: amplification using a single gene-specific oligonucleotide primer. Proc Natl Acad Sci U S A 85:8998–9002

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gee EPS, Ingber DE, Stultz CM (2008) Fibronectin unfolding revisited: modeling cell traction-mediated unfolding of the tenth type-III repeat. PLoS One 3:e2373. doi:10.1371/journal.pone.0002373

    Article  PubMed Central  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. doi:10.1094/MPMI-20-9-1112

    Article  CAS  PubMed  Google Scholar 

  • Godoy G, Steadman JR, Dickman MB, Dam R (1990) Use of mutants to demonstrate the role of oxalic acid in pathogenicity of Sclerotinia sclerotiorum on Phaseolus vulgaris. Physiol Mol Plant Pathol 37:179–191. doi:10.1016/0885-5765(90)90010-U

    Article  CAS  Google Scholar 

  • Guan C, Ji J, Jin C, Wang G, Li X, Guan W (2014) Expression of cholera toxin B subunit lumbrokinase in edible sunflower seeds-the use of transmucosal carrier to enhance its fusion protein’s effect on protection of rats and mice against thrombosis. Biotechnol Prog 30:1029–1039. doi:10.1002/btpr.1963

    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. doi:10.1093/jxb/erl282

    Article  CAS  PubMed  Google Scholar 

  • Guo X, Stotz HU (2007) Defense against Sclerotinia sclerotiorum in Arabidopsis is dependent on jasmonic acid, salicylic acid, and ethylene signaling. Mol Plant Microbe Interact 20:1384–1395. doi:10.1094/MPMI-20-11-1384

    Article  CAS  PubMed  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Hu X, Bidney DL, Yalpani N, Duvick JP, Crasta O, Folkerts O, Lu G (2003) Overexpression of a gene encoding hydrogen peroxide- generating oxalate oxidase evokes defense responses in sunflower 1. Plant Physiol 133:170–181. doi:10.1104/pp.103.024026

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hu Y, Dong Q, Yu D (2012) Arabidopsis WRKY46 coordinates with WRKY70 and WRKY53 in basal resistance against pathogen Pseudomonas syringae. Plant Sci 185–186:288–297. doi:10.1016/j.plantsci.2011.12.003

    Article  PubMed  Google Scholar 

  • Karimi M, Inzé D, Depicker A (2002) GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci 7:193–195

    Article  CAS  PubMed  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. doi:10.1094/MPMI-23-4-0446

    Article  CAS  PubMed  Google Scholar 

  • Kyte J, Doolittle RF (1982) A simple method for displaying the hydropathic character of a protein. J Mol Biol 157:105–132

    Article  CAS  PubMed  Google Scholar 

  • Lane BG (1994) Oxalate, germin, and the extracellular matrix of higher plants. FASEB J 8:294–301

    CAS  PubMed  Google Scholar 

  • Legendre L, Rueter S, Heinstein PF, Low PS (1993) Characterization of the Oligogalacturonide-Induced Oxidative Burst in Cultured Soybean (Glycine max) Cells. Plant Physiol 102:233–240

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • León-Galván F, de Jesús Joaquín-Ramos A, 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. doi:10.3390/ijms12117301

    Article  PubMed Central  PubMed  Google Scholar 

  • Liu B, Zhang S, Zhu X, Yang Q, Wu S, Mei M, Mauleon R, Leach J, Mew T, Leung H (2004) Candidate defense genes as predictors of quantitative blast resistance in rice. Mol Plant Microbe Interact 17:1146–1152. doi:10.1094/MPMI.2004.17.10.1146

    Article  CAS  PubMed  Google Scholar 

  • Livingstone DM, Hampton JL, Phipps PM, Grabau EA (2005) Enhancing resistance to Sclerotinia minor in peanut by expressing a barley oxalate oxidase gene. Plant Physiol 137:1354–1362. doi:10.1104/pp.104.057232

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Manavella PA, Dezar CA, Bonaventure G, Baldwin IT, Chan RL (2008) HAHB4, a sunflower HD-Zip protein, integrates signals from the jasmonic acid and ethylene pathways during wounding and biotic stress responses. Plant J 56:376–388. doi:10.1111/j.1365-313X.2008.03604.x

    Article  CAS  PubMed  Google Scholar 

  • Manavella PA, Chan RL (2009) Transient transformation of sunflower leaf discs via an Agrobacterium-mediated method: applications for gene expression and silencing studies. Nat Protoc 4:1699–1707. doi:10.1038/nprot.2009.178

    Article  CAS  PubMed  Google Scholar 

  • Manavella PA, Arce AL, Dezar CA, Bitton F, Renou J-P, Crespi M, Chan RL (2006) Cross-talk between ethylene and drought signalling pathways is mediated by the sunflower Hahb-4 transcription factor. Plant J 48:125–137. doi:10.1111/j.1365-313X.2006.02865.x

    Article  CAS  PubMed  Google Scholar 

  • Manning VA, Hamilton SM, Karplus PA, Ciuffetti LM (2008) The Arg-Gly-Asp-containing, solvent-exposed loop of Ptr ToxA is required for internalization. Mol Plant Microbe Interact 21:315–325. doi:10.1094/MPMI-21-3-0315

    Article  CAS  PubMed  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. doi:10.1104/pp.108.128348

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Marino D, Dunand C, Puppo A, Pauly N (2012) A burst of plant NADPH oxidases. Trends Plant Sci 17:9–15. doi:10.1016/j.tplants.2011.10.001

    Article  CAS  PubMed  Google Scholar 

  • Moretti S, Armougom F, Wallace IM, Higgins DG, Jongeneel CV, Notredame C (2007) The M-Coffee web server: a meta-method for computing multiple sequence alignments by combining alternative alignment methods. Nucleic Acids Res W645-8

  • Pan H-Y, Whittaker MM, Bouveret R, Berna A, Bernier F, Whittaker JW (2007) Characterization of wheat germin (oxalate oxidase) expressed by Pichia pastoris. Biochem Biophys Res Commun 356:925–929. doi:10.1016/j.bbrc.2007.03.097

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Patnaik BB, Kim DH, Oh SH, Song YS, Chanh NDM, Kim JS, Jung WJ, 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. doi:10.1371/journal.pone.0050900

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Peleg-Grossman S, Melamed-Book N, Cohen G, Levine A (2010) Cytoplasmic H2O2 prevents translocation of NPR1 to the nucleus and inhibits the induction of PR genes in Arabidopsis. Plant Signal Behav 5:1401–1406. doi:10.4161/psb.5.11.13209

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Peluffo L (2010) Caracterizacion de los mecanismos de defensa a Sclerotinia sclerotiorum agente causal de la podredumbre humeda de capitulo de girasol a traves del estudio de perfiles metabolicos y transcripcionales. Ph.D. Dissertation, Universidad de Buenos Aires

  • Perchepied L, Balagué C, Riou C, Claudel-Renard C, Rivière N, Grezes-Besset B, Roby D, Lipm IP, Cnrs-inra UMR, Genomics U, Team T, Brezet ZI, Lumière F (2010) Nitric oxide participates in the complex interplay of defense-related signaling pathways controlling disease resistance to Sclerotinia sclerotiorum in Arabidopsis thaliana. Mol Plant Microbe Interact 23:846–860

    Article  CAS  PubMed  Google Scholar 

  • Personat J-M, Tejedor-Cano J, Prieto-Dapena P, Almoguera C, Jordano J (2014) Cooverexpression of two Heat Shock Factors results in enhanced seed longevity and in synergistic effects on seedling tolerance to severe dehydration and oxidative stress. BMC Plant Biol 14:56. doi:10.1186/1471-2229-14-56

    Article  PubMed Central  PubMed  Google Scholar 

  • Petersen TN, Brunak S, von Heijne G, Nielsen H (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8:785–786. doi:10.1038/nmeth.1701

    Article  CAS  PubMed  Google Scholar 

  • Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29(9): e45

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Radonic LM, Zimmermann JM, Zavallo D, Lopez N, Lopez Bilbao M (2006) Rooting in Km selective media as efficient in vitro selection method for sunflower genetic transformation. Electron J Biotechnol. doi:10.2225/vol9-issue3-fulltext-19

    Google Scholar 

  • Ramakers C, Ruijter JM, Deprez RHL, Moorman AFM (2003) Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci Lett 339:62–66

    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. doi:10.1093/jxb/ers203

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Schwartz MA (1992) Transmembrane signalling by integrins. Trends Cell Biol 2:304–308. doi:10.1016/0962-8924(92)90120-C

    Article  CAS  PubMed  Google Scholar 

  • Shetty NP, Mehrabi R, Lütken H, Haldrup A, Kema GHJ, Collinge DB, Jørgensen HJL (2007) Role of hydrogen peroxide during the interaction between the hemibiotrophic fungal pathogen Septoria tritici and wheat. New Phytol 174:637–647. doi:10.1111/j.1469-8137.2007.02026.x

    Article  CAS  PubMed  Google Scholar 

  • Shetty NP, Jørgensen HJL, Jensen JD, Collinge DB, Shetty HS (2008) Roles of reactive oxygen species in interactions between plants and pathogens. Eur J Plant Pathol 121:267–280. doi:10.1007/s10658-008-9302-5

    Article  CAS  Google Scholar 

  • Sujatha M, Vijay S, Vasavi S, Veera Reddy P, Chander Rao S (2012) Agrobacterium-mediated transformation of cotyledons of mature seeds of multiple genotypes of sunflower (Helianthus annuus L.). Plant Cell, Tissue Organ Cult 110:275–287. doi:10.1007/s11240-012-0149-2

    Article  Google Scholar 

  • Walz A, Zingen-Sell I, Loeffler M, Sauer M (2008) Expression of an oxalate oxidase gene in tomato and severity of disease caused by Botrytis cinerea and Sclerotinia sclerotiorum. Plant Pathol 57:453–458. doi:10.1111/j.1365-3059.2007.01815.x

    Article  CAS  Google Scholar 

  • Wang Z, Tan X, Zhang Z, Gu S, Li G, Shi H (2012) Defense to Sclerotinia sclerotiorum in oilseed rape is associated with the sequential activations of salicylic acid signaling and jasmonic acid signaling. Plant Sci 184:75–82. doi:10.1016/j.plantsci.2011.12.013

    Article  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. doi:10.1371/journal.pone.0061722

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wei Y, Zhang Z, Andersen CH, Schmelzer E, Gregersen PL, Collinge DB, Smedegaard-Petersen V, Thordal-Christensen H (1998) An epidermis/papilla-specific oxalate oxidase like protein in the defence response of barley attacked by the powdery mildew fungus. Plant Mol Biol 36:101–112

    Article  CAS  PubMed  Google Scholar 

  • Weigel D, Glazebrook J (2006) In planta transformation of Arabidopsis. CSH Protoc 006:pdb.prot4668–. doi: 10.1101/pdb.prot4668

  • Williams B, Kabbage M, Kim HJ, Britt R, Dickman MB (2011) Tipping the balance: sclerotinia sclerotiorum secreted oxalic acid suppresses host defenses by manipulating the host redox environment. PLoS Pathog 7:e1002107. doi:10.1371/journal.ppat.1002107

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wohlgemuth H, Mittelstrass K, Kschieschan S, Bender J, Weigel H-J, Overmyer K, Kangasjarvi J, Sandermann H, Langebartels C (2002) Activation of an oxidative burst is a general feature of sensitive plants exposed to the air pollutant ozone. Plant Cell Environ 25:717–726. doi:10.1046/j.1365-3040.2002.00859.x

    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 

  • Zhou F, Zhang Z, Gregersen PL, Mikkelsen JD, De Neergaard E, Collinge DB, Thordal-Christensen H (1998) Molecular characterization of the oxalate oxidase involved in the response of barley to the powdery mildew fungus 1. Plant Physiol 117:33–41

    Article  PubMed Central  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. doi:10.1104/pp.106.083824

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zubrzycki J (2015) Estudio de la resistencia a Sclerotinia sclerotiorum en líneas endocriadas de girasol. Ph.D. Dissertation, Universidad de Buenos Aires

Download references

Acknowledgments

The authors wish to thank Ing. Dora Barreto for her valuable guidance during infection assays, and Teresa Cabrera, Matias Rodriguez, and Juan Carlos Torres for technical support. We are also grateful to Dr. Janet Higgins for helping us improve the English of the manuscript, and to Dr. Carlos Manacorda and Dr. Sebastián Asurmendi for kindly providing several primers for real-time qPCR experiments. The comments and suggestions of two anonymous reviewers are gratefully acknowledged. This research was supported by the Agencia Nacional de Promoción Científica y Tecnológica (ANPCYT PAE-31700 PID 2008 0073; PICT 2011 1365; PICT 2007 727) and the Instituto Nacional de Tecnología Agropecuaria (INTA PNBIO1131023; PNBIO1131043; AEBIO4461). VVL, RAH, CVR and NBP are career members of the Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET). Dr. HEH is a career member of the Comisión de Investigaciones Científicas de la Provincia de Buenos Aires (CIC).

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to V. V. Lia.

Additional information

Communicated by C.-H. Dong.

The sequence used for this study has been deposited at GenBank under accession number KM488198.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Beracochea, V.C., Almasia, N.I., Peluffo, L. et al. Sunflower germin-like protein HaGLP1 promotes ROS accumulation and enhances protection against fungal pathogens in transgenic Arabidopsis thaliana . Plant Cell Rep 34, 1717–1733 (2015). https://doi.org/10.1007/s00299-015-1819-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-015-1819-4

Keywords

Navigation