Skip to main content
SpringerLink
Log in

Wheat wounding-responsive HD-Zip IV transcription factor GL7 is predominantly expressed in grain and activates genes encoding defensins

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

A Correction to this article was published on 01 July 2019

This article has been updated

Abstract

Key message

Several classes of transcription factors are involved in the activation of defensins. A new type of the transcription factor responsible for the regulation of wheat grain specific defensins was characterised in this work.

Abstract

HD-Zip class IV transcription factors constitute a family of multidomain proteins. A full-length cDNA of HD-Zip IV, designated TaGL7 was isolated from the developing grain of bread wheat, using a specific DNA sequence as bait in the Y1H screen. 3D models of TaGL7 HD complexed with DNA cis-elements rationalised differences that underlined accommodations of binding and non-binding DNA, while the START-like domain model predicted binding of lipidic molecules inside a concave hydrophobic cavity. The 3′-untranslated region of TaGL7 was used as a probe to isolate the genomic clone of TdGL7 from a BAC library prepared from durum wheat. The spatial and temporal activity of the TdGL7 promoter was tested in transgenic wheat, barley and rice. TdGL7 was expressed mostly in ovary at fertilisation and its promoter was active in a liquid endosperm during cellularisation and later in the endosperm transfer cells, aleurone, and starchy endosperm. The pattern of TdGL7 expression resembled that of genes that encode grain-specific lipid transfer proteins, particularly defensins. In addition, GL7 expression was upregulated by mechanical wounding, similarly to defensin genes. Co-bombardment of cultured wheat cells with TdGL7 driven by constitutive promoter and seven grain or root specific defensin promoters fused to GUS gene, revealed activation of four promoters. The data confirmed the previously proposed role of HD-Zip IV transcription factors in the regulation of genes that encode lipid transfer proteins involved in lipid transport and defence. The TdGL7 promoter could be used to engineer cereal grains with enhanced resistance to insects and fungal infections.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

Change history

  • 01 July 2019

    Due to an unfortunate turn of events, the panels O to S are missing in Fig. 8 of the original publication. The correct Fig. 8 and its caption is published here and should be treated as definitive.

Abbreviations

AP2:

APETALA2

bZIP:

Basic leucine zipper

CPL:

1-Palmitoyl-2-linoleoyl-sn-glycero-3-phosphocholine

DAP:

Days after pollination

DLP:

1,2-Dilinoleolyl-sn-glycero-3-phosphocholine

ERF:

Ethylene-responsive element binding factor

GL2:

GLABRA

GL7:

GLABRA2-like clone 7

HD:

Homeodomain

HSF:

Heat-shock transcription factor

MYB:

Myeloblastosis

PDB:

Protein data bank

PDF1:

PROTODERMAL FACTOR1

SEM:

Standard errors of mean

START:

Steroidogenic acute regulatory protein-related lipid-transfer

TF(s):

Transcription factor(s)

UTR:

3′ Untranslated region

ZIP:

Leucine zipper

ZLZ:

Zipper-loop-zipper

Y1H:

Yeast-1-hybrid

Y2H:

Yeast-2-hybrid

References

  • Abe M, Takahashi T, Komeda Y (2001) Identification of a cis-regulatory element for L1 layer-specific gene expression, which is targeted by an L1-specific homeodomain protein. Plant J 26:487–494

    Article  CAS  PubMed  Google Scholar 

  • Abe M, Katsumata H, Komeda Y, Takahashi T (2003) Regulation of shoot epidermal cell differentiation by a pair of homeodomain proteins in Arabidopsis. Development 130:635–643

    Article  CAS  PubMed  Google Scholar 

  • Andreeva A, Howorth D, Chandonia J-M, Brenner SE, Hubbard TJP, Chothia C, Murzin AG (2008) Data growth and its impact on the SCOP database: new developments. Nucleic Acids Res 36:D419–D425

    Article  CAS  PubMed  Google Scholar 

  • Ariel FD, Manavella PA, Dezar CA, Chan RL (2007) The true story of the HD-Zip family. Trends Plant Sci 12:419–426

    Article  CAS  PubMed  Google Scholar 

  • Baima S, Possenti M, Matteucci A, Wisman E, Altamura MM, Ruberti I, Morelli G (2001) The Arabidopsis ATHB-8 HD-Zip protein acts as a differentiation-promoting transcription factor of the vascular meristems. Plant Physiol 126:643–655

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bi H, Luang S, Li Y, Bazanova N, Morran S, Song Z, Perera MA, Hrmova M, Borisjuk N, Lopato S (2016) Identification and characterization of wheat drought-responsive MYB transcription factors involved in the regulation of cuticle biosynthesis. J Exp Bot 67:5363–5380

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boutrot F, Meynard D, Guiderdoni E, Joudrier P, Gautier MF (2007) The Triticum aestivum non-specific lipid transfer protein (TaLtp) gene family: comparative promoter activity of six TaLtp genes in transgenic rice. Planta 225:843–862

    Article  CAS  PubMed  Google Scholar 

  • Brown RL, Kazan K, McGrath KC, Maclean DJ, Manners JM (2003) A role for the GCC-box in jasmonate-mediated activation of the PDF1.2 gene of Arabidopsis. Plant Physiol 132:1020–1032

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bru C, Courcelle E, Carrère S, Beausse Y, Dalmar S, Kahn D (2005) The ProDom database of protein domain families: more emphasis on 3D. Nucleic Acids Res 33:D212–D215

    Article  CAS  PubMed  Google Scholar 

  • Bürglin TR, Affolter M (2016) Homeodomain proteins: an update. Chromosoma 125:497–521

    Article  CAS  PubMed  Google Scholar 

  • Burton RA, Shirley NJ, King BJ, Harvey AJ, Fincher GB (2004) The CesA gene family of barley. Quantitative analysis of transcripts reveals two groups of co-expressed genes. Plant Physiol 134:224–236

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cenci A, Chantret N, Kong X, Gu Y, Anderson OD, Fahima T, Distelfeld A, Dubcovsky J (2003) Construction and characterization of a half million clone BAC library of durum wheat (Triticum turgidum ssp. durum). Theor Appl Genet 107:931–939

    Article  CAS  PubMed  Google Scholar 

  • Chew W, Hrmova M, Lopato S (2013) Role of Homeodomain leucine zipper (HD-Zip) IV transcription factors in plant development and plant protection from deleterious environmental factors. Intern J Mol Sci 14:8122–8147

    Article  CAS  Google Scholar 

  • Ciarbelli AR, Ciolfi A, Salvucci S, Ruzza V, Possenti M, Carabelli M, Fruscalzo A, Sessa G, Morelli G, Ruberti I (2008) The Arabidopsis homeodomain-leucine zipper II gene family: diversity and redundancy. Plant Mol Biol 68:465–478

    Article  CAS  PubMed  Google Scholar 

  • Curtis MD, Grossniklaus U (2003) A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol 133:462–469

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • de Carvalho AO, Gomes VM (2009) Plant defensins—prospects for the biological functions and biotechnological properties. Peptides 30:1007–1020

    Article  CAS  Google Scholar 

  • Depège-Fargeix N, Javelle M, Chambrier P, Frangne N, Gerentes D, Perez P, Rogowsky PM, Vernoud V (2011) Functional characterization of the HD-ZIP IV transcription factor OCL1 from maize. J Exp Bot 62:293–305

    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

    Article  CAS  PubMed  Google Scholar 

  • Dwivedi KK, Roche DJ, Clemente TE, Ge Z, Carman JG (2014) The OCL3 promoter from Sorghum bicolor directs gene expression to abscission and nutrient-transfer zones at the bases of floral organs. Annals Bot 114:489–498

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eini O, Yang N, Pyvovarenko T, Pillman K, Bazanova N, Tikhomirov N, Eliby S, Shirley N, Sivasankar S, Tingey S, Langridge P, Hrmova M, Lopato S (2013) Complex regulation by Apetala2 domain-containing transcription factors revealed through analysis of the stress-responsive TdCor410b promoter from durum wheat. PLoS ONE 8:e58713

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Emsley P, Cowtan K (2004) Coot: model-building tools for molecular graphics. Acta Cryst D 60:2126–2132

    Article  CAS  Google Scholar 

  • Guan XY, Li QJ, Shan CM, Wang S, Mao YB, Wang LJ, Chen XY (2008) The HD-Zip IV gene GaHOX1 from cotton is a functional homologue of the Arabidopsis GLABRA2. Physiol Plant 134:174–182

    Article  CAS  PubMed  Google Scholar 

  • Harris JC, Sornaraj P, Taylor M, Bazanova N, Baumann U, Lovell B, Langridge P, Lopato S, Hrmova M (2016) Molecular interactions of the γ-clade homeodomain-leucine zipper class I transcription factors during the wheat response to water deficit. Plant Mol Biol 90:435–452

    Article  CAS  PubMed  Google Scholar 

  • Henikoff S, Henikoff JG (1991) Automated assembly of protein blocks for database searching. Nucleic Acids Res 19:6565–6572

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ingouff M, Farbos I, Lagercrantz U, Arnold S (2001) PaHB1 is an evolutionary conserved HD-GL2 homeobox gene expressed in the protoderm during Norway spruce embryo development. Genesis 30:220–230

    Article  CAS  PubMed  Google Scholar 

  • Ingouff M, Farbos I, Wiweger M, von Arnold S (2003) The molecular characterization of PaHB2, a homeobox gene of the HD-GL2 family expressed during embryo development in Norway spruce. J Exp Bot 54:1343–1350

    Article  CAS  PubMed  Google Scholar 

  • Ingram GC, Boisnard-Lorig C, Dumas C, Rogowsky PM (2000) Expression patterns of genes encoding HD-ZipIV homeo domain proteins define specific domains in maize embryos and meristems. Plant J 22:401–414

    Article  CAS  PubMed  Google Scholar 

  • Ismagul A, Yang N, Maltseva E, Iskakova G, Mazonka I, Skiba Y, Bi H, Eliby S, Jatayev S, Shavrukov Y, Borisjuk N, Langridge P (2018) A biolistic method for high-throughput production of transgenic wheat plants with single gene insertions. BMC Plant Biol 18:135

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ito M, Sentoku N, Nishimura A, Hong SK, Sato Y, Matsuoka M (2002) Position dependent expression of GL2-type homeobox gene, Roc1: significance for protoderm differentiation and radial pattern formation in early rice embryogenesis. Plant J 29:497–507

    Article  CAS  PubMed  Google Scholar 

  • Javelle M, Vernoud V, Depège-Fargeix N, Arnould C, Oursel D, Domergue F, Sarda X, Rogowsky PM (2010) Overexpression of the epidermis-specific homeodomain-leucine zipper IV transcription factor Outer Cell Layer1 in maize identifies target genes involved in lipid metabolism and cuticle biosynthesis. Plant Physiol 154:273–286

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Javelle M, Klein-Cosson C, Vernoud V, Boltz V, Maher C, Timmermans M, Depège-Fargeix N, Rogowsky PM (2011) Genome-wide characterization of the HD-ZIP IV transcription factor family in maize: preferential expression in the epidermis. Plant Physiol 157:790–803

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: β-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6:3901–3907

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jha S, Chattoo BB (2010) Expression of a plant defensin in rice confers resistance to fungal phytopathogens. Transgenic Res 19:373–384

    Article  CAS  PubMed  Google Scholar 

  • Kamata N, Okada H, Komeda Y, Takahashi T (2013) Mutations in epidermis-specific HD-ZIP IV genes affect floral organ identity in Arabidopsis thaliana. Plant J 75:430–440

    Article  CAS  PubMed  Google Scholar 

  • Kanzaki H, Nirasawa S, Saitoh H, Ito M, Nishihara M, Terauchi R, Nakamura I (2002) Overexpression of the wasabi defensin gene confers enhanced resistance to blast fungus (Magnaporthe grisea) in transgenic rice. Theor Appl Genetics 105:809–814

    Article  CAS  Google Scholar 

  • Kaur J, John F, Adholeya A, Velivelli S, El-Mounadi Kaoutar, Natalya N, Thomas C, Shah D (2016) Expression of apoplast-targeted plant defensin MtDef4.2 confers resistance to leaf rust pathogen Puccinia triticina but does not affect mycorrhizal symbiosis in transgenic wheat. Transgenic Res 26:37–49

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kovalchuk N, Smith J, Pallotta M, Singh R, Ismagul A, Eliby S, Bazanova N, Milligan AS, Hrmova M, Langridge P, Lopato S (2009) Characterization of the wheat endosperm transfer cell-specific protein TaPR60. Plant Mol Biol 71:81–98

    Article  CAS  PubMed  Google Scholar 

  • Kovalchuk N, Li M, Wittek F, Reid N, Singh R, Shirley N, Ismagul A, Eliby S, Johnson A, Milligan AS, Hrmova M, Langridge P, Lopato S (2010) Defensin promoters as potential tools for engineering disease resistance in cereal grains. Plant Biotechnol J 8:47–64

    Article  CAS  PubMed  Google Scholar 

  • Kovalchuk N, Smith J, Bazanova N, Pyvovarenko T, Singh R, Shirley N, Ismagul A, Johnson A, Milligan AS, Hrmova M, Langridge P, Lopato S (2012a) Characterization of the wheat gene encoding a grain-specific lipid transfer protein TdPR61, and promoter activity in wheat, barley and rice. J Exp Bot 63:2025–2040

    Article  CAS  PubMed  Google Scholar 

  • Kovalchuk N, Wu W, Eini O, Bazanova N, Pallotta M, Shirley N, Singh R, Ismagul A, Eliby S, Johnson A, Langridge P, Lopato S (2012b) The scutellar vascular bundle-specific promoter of the wheat HD-Zip IV transcription factor shows similar spatial and temporal activity in transgenic wheat, barley and rice. Plant Biotechnol J 10:43–53

    Article  CAS  PubMed  Google Scholar 

  • Krieger E, Joo K, Lee J, Lee J, Raman S, Thompson J, Tyka M, Baker D, Karplus K (2009) Improving physical realism, stereochemistry, and side-chain accuracy in homology modeling: four approaches that performed well in CASP8. Proteins 77:114–122

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kubo H, Peeters AJ, Aarts MG, Pereira A, Koornneef M (1999) ANTHOCYANINLESS2, a homeobox gene affecting anthocyanin distribution and root development in Arabidopsis. Plant Cell 11:1217–1226

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • LaRonde-LeBlanc NA, Wolberger C (2003) Structure of HoxA9 and Pbx1 bound to DNA: hox hexapeptide and DNA recognition anterior to posterior. Gen Dev 17:2060–2072

    Article  CAS  Google Scholar 

  • Laskowski RA, MacArthur MW, Moss DS, Thornton JM (1993) PROCHECK: a program to check the stereochemical quality of protein structures. J Appl Cryst 26:283–291

    Article  CAS  Google Scholar 

  • Letunic I, Doerks T, Bork P (2009) SMART 6: recent updates and new developments. Nucleic Acids Res 37:D229–D232

    Article  CAS  PubMed  Google Scholar 

  • Li M, Singh R, Bazanova N, Milligan AS, Shirley N, Langridge P, Lopato S (2008) Spatial and temporal expression of endosperm transfer cell-specific promoters in transgenic rice and barley. Plant Biotechnol J 6:465–476

    Article  CAS  PubMed  Google Scholar 

  • Li Z, Zhou M, Zhang Z, Ren L, Du L, Zhang B, Xu H, Xin Z (2011) Expression of a radish defensin in transgenic wheat confers increased resistance to Fusarium graminearum and Rhizoctonia cerealis. Funct Integr Genomics 11:63–70

    Article  CAS  PubMed  Google Scholar 

  • Li S, Wang X, He S, Li J, Huang Q, Imaizumi T, Qu L, Qin G, Qu LJ, Gu H (2016) CFLAP1 and CFLAP2 are two bHLH transcription factors participating in synergistic regulation of AtCFL1-mediated cuticle development in Arabidopsis. PLoS Genet 12:e1005744

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lu P, Porat R, Nadeau JA, O’Neill SD (1996) Identification of a meristem L1 layer-specific gene in Arabidopsis that is expressed during embryonic pattern formation and defines a new class of homeobox genes. Plant Cell 8:2155–2168

    CAS  PubMed  PubMed Central  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

    Article  CAS  PubMed  Google Scholar 

  • Matthews PR, Wang MB, Waterhouse PM, Thornton S, Fieg SJ, Gubler F, Jacobsen JV (2001) Marker gene elimination from transgenic barley, using co-transformation with adjacent ‘twin T-DNAs’ on a standard Agrobacterium transformation vector. Mol Breed 7:195–202

    Article  CAS  Google Scholar 

  • Morran S, Eini O, Pyvovarenko T, Parent B, Singh R, Ismagul A, Eliby S, Shirley N, Langridge P, Lopato S (2011) Improvement of stress tolerance of wheat and barley by modulation of expression of DREB/CBF factors. Plant Biotechnol J 9:230–249

    Article  CAS  PubMed  Google Scholar 

  • Nakamura M, Katsumata H, Abe M, Yabe N, Komeda Y, Yamamoto KT, Takahashi T (2006) Characterization of the class IV Homeodomain-Leucine Zipper gene family in Arabidopsis. Plant Physiol 141:1363–1375

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Needleman SB, Wunsch CD (1970) A general method applicable to the search for similarities in the amino acid sequence of two proteins. J Mol Biol 48:443–453

    Article  CAS  PubMed  Google Scholar 

  • Ohashi Y, Oka A, Rodrigues-Pousada R, Possenti M, Ruberti I, Morelli G, Aoyama T (2003) Modulation of phospholipid signaling by GLABRA2 in root-hair pattern formation. Science 300:1427–1430

    Article  CAS  PubMed  Google Scholar 

  • Page RDM (1996) TreeView: an application to display phylogenetic trees on personal computers. Comp Appl Biosci 12:357–358

    CAS  PubMed  Google Scholar 

  • Parisi K, Shafee TMA, Quimbar P, van der Weerden NL, Bleackley MR, Anderson MA (2019) The evolution, function and mechanisms of action for plant defensins. Semin Cell Dev Biol 88:107–118

    Article  CAS  PubMed  Google Scholar 

  • Pei J, Kim B-H, Grishin NV (2008) PROMALS3D: a tool for multiple sequence and structure alignment. Nucleic Acids Res 36:2295–2300

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pyvovarenko T, Lopato S (2011) Isolation of plant transcription factors using a yeast one-hybrid system. Meth Mol Biol 754:45–66

    Article  CAS  Google Scholar 

  • Ramachandran GN, Ramakrishnan C, Sasisekharan V (1963) Stereochemistry of polypeptide chain configurations. J Mol Biol 7:95–99

    Article  CAS  PubMed  Google Scholar 

  • Ré DA, Dezar CA, Chan RL, Baldwin IT, Bonaventure G (2011) Nicotiana attenuata NaHD20 plays a role in leaf ABA accumulation during water stress, benzylacetone emission from flowers, and the timing of bolting and flower transitions. J Exp Bot 62:155–166

    Article  CAS  PubMed  Google Scholar 

  • Rerie WG, Feldmann KA, Marks MD (1994) The GLABRA2 gene encodes a homeo domain protein required for normal trichome development in Arabidopsis. Genes Dev 8:1388–1399

    Article  CAS  PubMed  Google Scholar 

  • Roderick SL, Chan WW, Agate DS, Olsen LR, Vetting MW, Rajashankar KR, Cohen DE (2002) Structure of human phosphatidylcholine transfer protein in complex with its ligand. Nat Struct Biol 9:507–511

    CAS  PubMed  Google Scholar 

  • Sali A, Blundell TL (1993) Comparative protein modeling by satisfaction of spatial restrains. J Mol Biol 234:779–815

    Article  CAS  PubMed  Google Scholar 

  • Sanchez R, Sali A (1998) Large-scale protein structure modeling of the Saccharomyces cerevisiae genome. Proc Natl Acad Sci USA 95:13597–13602

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sasaki K, Kuwabara C, Umeki N, Fujioka M, Saburi W, Matsui H, Abe F, Imai R (2016) The cold-induced defensin TAD1 confers resistance against snow mold and Fusarium head blight in transgenic wheat. J Biotechnol 228:3–7

    Article  CAS  PubMed  Google Scholar 

  • Sessa G, Steindler C, Morelli G, Ruberti I (1998) The Arabidopsis Athb-8, -9, -14 genes are members of a small gene family coding for highly related HD-ZIP proteins. Plant Mol Biol 38:609–622

    Article  CAS  PubMed  Google Scholar 

  • Shimada TT, Sasakuma T, Tsunewaki K (1969) In vitro culture of wheat tissues. I. Callus formation, organ redifferentiation and single cell culture. Can J Genet Cytol 11:294–304

    Article  CAS  Google Scholar 

  • Sippl MJ (1993) Recognition of errors in three-dimensional structures of proteins. Proteins 17:355–362

    Article  CAS  PubMed  Google Scholar 

  • Sippl MJ, Wiederstein M (2008) A note on difficult structure alignment problems. Bioinformatics 24:426–427

    Article  CAS  PubMed  Google Scholar 

  • Stotz HU, Thomson JG, Wang Y (2009) Plant defensins: defense, development and application. Plant Signal Behav 4:1010–1012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tang SS, Prodhan ZH, Biswas SK, Le CF, Sekaran SD (2018) Antimicrobial peptides from different plant sources: isolation, characterisation, and purification. Phytochemistry 154:94–105

    Article  CAS  PubMed  Google Scholar 

  • Thorsell AG, Lee WH, Persson C, Siponen M, Nilsson M, Busam RD, Kotenyova T, Schüler H, Lehtiö L (2011) Comparative structural analysis of lipid binding START domains. PLoS ONE 6:e19521

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tian W, Chen C, Lei X, Zhao J, Liang J (2018) CASTp 3.0: computed atlas of surface topography of proteins. Nucleic Acids Res 46:W363–W367

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tingay S, McElroy D, Kalla R, Fieg S, Wang MB, Thornton S, Brettell R (1997) Agrobacterium tumefaciens-mediated barley transformation. Plant J 11:1369–1376

    Article  CAS  Google Scholar 

  • Tominaga-Wada R, Iwata M, Sugiyama J, Kotake T, Ishida T, Yokoyama R, Nishitani K, Okada K, Wada T (2009) The GLABRA2 homeodomain protein directly regulates CESA5 and XTH17 gene expression in Arabidopsis roots. Plant J 60:564–574

    Article  CAS  PubMed  Google Scholar 

  • Tron AE, Bertoncini CW, Palena CM, Chan RL, Gonzalez DH (2001) Combinatorial interactions of two amino acids with a single base pair define target site specificity in plant dimeric homeodomain proteins. Nucleic Acids Res 29:4866–4872

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tron AE, Bertoncini CW, Chan RL, Gonzalez DH (2002) Redox regulation of plant homeodomain transcription factors. J Biol Chem 277:34800–34807

    Article  CAS  PubMed  Google Scholar 

  • Vernoud V, Laigle G, Rozier F, Meeley RB, Perez P, Rogowsky PM (2009) The HD-ZIP IV transcription factor OCL4 is necessary for trichome patterning and anther development in maize. Plant J 59:883–894

    Article  CAS  PubMed  Google Scholar 

  • Vlahovicek K, Kajan L, Agoston V, Pongor S (2005) The SBASE domain sequence resource, release 12: prediction of protein domain-architecture using support vector machines. Nucleic Acids Res 33:D223–D225

    Article  CAS  PubMed  Google Scholar 

  • Wei J, Choi H, Jin P, Wu Y, Yoon J, Lee YS, Quan T, An G (2016) GL2-type homeobox gene Roc4 in rice promotes flowering time preferentially under long days by repressing Ghd7. Plant Sci 252:133–143

    Article  CAS  PubMed  Google Scholar 

  • Yan T, Li L, Xie L, Chen M, Shen Q, Pan Q, Fu X, Shi P, Tang Y, Huang H, Huang Y, Huang Y, Tang K (2018) A novel HD-ZIP IV/MIXTA complex promotes glandular trichome initiation and cuticle development in Artemisia annua. New Phytol 218:567–578

    Article  CAS  PubMed  Google Scholar 

  • Yang JY, Chung MC, Tu CY, Leu WM (2002) OSTF1: a HD-GL2 family homeobox gene is developmentally regulated during embryogenesis in rice. Plant Cell Physiol 43:628–638

    Article  CAS  PubMed  Google Scholar 

  • Yang Y, Luang S, Harris J, Riboni M, Li Y, Bazanova N, Hrmova M, Haefele S, Kovalchuk N, Lopato S (2018) Overexpression of the class I homeodomain transcription factor TaHDZipI-5 increases drought and frost tolerance in transgenic wheat. Plant Biotechnol J 16:1227–1240

    Article  CAS  PubMed  Google Scholar 

  • Zarei A, Körbes AP, Younessi P, Montiel G, Champion A, Memelink J (2011) Two GCC boxes and AP2/ERF-domain transcription factor ORA59 in jasmonate/ethylene-mediated activation of the PDF1.2 promoter in Arabidopsis. Plant Mol Biol 75:321–331

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang F, Zuo K, Zhang J, Liu X, Zhang L, Sun X, Tang K (2010) An L1 box binding protein, GbML1, interacts with GbMYB25 to control cotton fibre development. J Exp Bot 61:3599–3613

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We acknowledge the contributions of Ainur Ismagul and Serik Eliby in plant transformation. We thank Margaret Pallotta for technical assistance with BAC library screening and promoter cloning. Ursula Langridge, Lorraine Carruthers and Alex Kovalchuk are thanked for their assistance with growing of plants in the glasshouse. This work was supported by the Australian Research Council (Grant No. LP120100201 to M.H. and S.L.), the Grains Research and Development Corporation and the Government of South Australia.

Author information

Author notes

  1. Wei Wu

    Present address: Agronomy College, Sichuan Agricultural University, Ya’an, 625014, China

  2. Natalia Bazanova

    Present address: Commonwealth Scientific and Industrial Research Organisation, Glen Osmond, 5064, SA, Australia

Authors and Affiliations

  1. School of Agriculture, Food and Wine, University of Adelaide, Glen Osmond, SA, 5064, Australia

    Nataliya Kovalchuk, Wei Wu, Natalia Bazanova, Nicolas Reid, Rohan Singh, Neil Shirley, Peter Langridge, Maria Hrmova & Sergiy Lopato

  2. Department of Plant Protection, School of Agriculture, University of Zanjan, Zanjan, Iran

    Omid Eini

  3. School of BioSciences, The University of Melbourne, Melbourne, VIC, 3010, Australia

    Alexander A. T. Johnson

  4. School of Life Sciences, Huaiyin Normal University, Huai’an, China

    Maria Hrmova

Authors
  1. Nataliya Kovalchuk
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Wei Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Natalia Bazanova
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Nicolas Reid
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Rohan Singh
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Neil Shirley
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Omid Eini
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Alexander A. T. Johnson
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Peter Langridge
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Maria Hrmova
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Sergiy Lopato
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Conceived, designed experiments and analysed data: NK and SL. Cloning and Y1H: NB and WW. Transient expression assays: NR and OE. Q-PCR experiments: NS. Plant transformation and analysis: RS, AATJ, NK. 3D molecular modelling and bioinformatics: MH. Discussed the data: SL, NK, PL and MH. Writing of the manuscript: SL. Contributed to writing: MH.

Corresponding author

Correspondence to Maria Hrmova.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

GenBank Database (https://www.ncbi.nlm.nih.gov/genbank/) accession numbers: TaGL7 cDNA—MK583312; TdGL7 cDNA—MK583313; TdGL7 promoter—MK583314. Accessions will be released upon publication.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 201 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kovalchuk, N., Wu, W., Bazanova, N. et al. Wheat wounding-responsive HD-Zip IV transcription factor GL7 is predominantly expressed in grain and activates genes encoding defensins. Plant Mol Biol 101, 41–61 (2019). https://doi.org/10.1007/s11103-019-00889-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-019-00889-9

Keywords

Search

Navigation