Skip to main content
Log in

Differential expression of four soybean bZIP genes during Phakopsora pachyrhizi infection

  • Original Paper
  • Published:
Functional & Integrative Genomics Aims and scope Submit manuscript

Abstract

Asian soybean rust (ASR), caused by the obligate biotrophic fungus Phakopsora pachyrhizi, is one of most important diseases in the soybean (Glycine max (L.) Merr.) agribusiness. The identification and characterization of genes related to plant defense responses to fungal infection are essential to develop ASR-resistant plants. In this work, we describe four soybean genes, GmbZIP62, GmbZIP105, GmbZIPE1, and GmbZIPE2, which encode transcription factors containing a basic leucine zipper (bZIP) domain from two divergent classes, and that are responsive to P. pachyrhizi infection. Molecular phylogenetic analyses demonstrated that these genes encode proteins similar to bZIP factors responsive to pathogens. Yeast transactivation assays showed that only GmbZIP62 has strong transactivation activity in yeast. In addition, three of the bZIP transcription factors analyzed were also differentially expressed by plant defense hormones, and all were differentially expressed by fungal attack, indicating that these proteins might participate in response to ASR infection. The results suggested that these bZIP proteins are part of the plant defense response to P. pachyrhizi infection, by regulating the gene expression related to ASR infection responses. These bZIP genes are potential targets to obtain new soybean genotypes resistant to ASR.

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

Similar content being viewed by others

Abbreviations

GmbZIP:

Glycine max basic/leucine zipper protein

References

  • Albani D, Hammond-Kosack MC, Smith C, Conlan S, Colot V, Holdsworth M, Bevan MW (1997) The wheat transcriptional activator SPA: A seed-specific bZIP protein that recognizes the GCN4-like motif in the bifactorial endosperm box of prolamin genes. Plant Cell 9:171–184

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Alves MS, Dadalto SP, Gonçalves AB, De Souza GB, Barros VA, Fietto LG (2013) Plant bZIP transcription factors responsive to pathogens: a review. Int J Mol Sci 14:7815–7828

    Article  PubMed Central  PubMed  Google Scholar 

  • Amberg DC, Burke DJ, Strathern JN (2005) Assay of β-galactosidase in yeast: assay of crude extracts. Methods in yeast genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor

    Google Scholar 

  • Benko-Iseppon AM, Nepomuceno AL, Abdelnoor RV (2012) GENOSOJA—the Brazilian soybean genome consortium: high throughput omics and beyond. Genet Mol Biol 35(1 (suppl)):i–iv

    Article  PubMed Central  PubMed  Google Scholar 

  • Bhuiyan NH, Liu W, Liu G, Selvaraj G, Wei Y, King J (2007) Transcriptional regulation of genes involved in the pathways of biosynthesis and supply of methyl units in response to powdery mildew attack and abiotic stresses in wheat. Plant Mol Biol 64:305–318

    Article  CAS  PubMed  Google Scholar 

  • Bhuiyan NH, Selvaraj G, Wei Y, King J (2009) Gene expression profiling and silencing reveal that monolignol biosynthesis plays a critical role in penetration defence in wheat against powdery mildew invasion. J Exp Bot 60:509–521

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bromfield KR (1984) Soybean rust. American Phytopathological Society, St. Paul

    Google Scholar 

  • Bromfield KR, Hartwig EE (1980) Resistance to soybean rust and mode of inheritance. Crop Sci 20:254–255

    Article  Google Scholar 

  • Campe R, Loehrer M, Conrath U, Goellner K (2014) Phakopsora pachyrhizi induces defense marker genes to necrotrophs in Arabidopsis thaliana. Physiol Mol Plant Pathol 87:1–8

    Article  CAS  Google Scholar 

  • Cheng YW, Chan KL (1968) The breeding of rust resistant soybean Tainung 3. J Taiwan Agr Res 17:30–34

  • Chern MS, Eiben HG, Bustos MM (1996) The developmentally regulated bZIP factor ROM1 modulates transcription from lectin and storage protein genes in bean embryos. Plant J 10:135–148

    Article  CAS  PubMed  Google Scholar 

  • Chuang CF, Running MP, Williams RW, Meyerowitz EM (1999) The PERIANTHIA gene encodes a bZIP protein involved in the determination of floral organ number in Arabidopsis thaliana. Genes Dev 13:334–344

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Dietrich K, Weltmeier F, Ehlert A, Weiste C, Stahl M, Harter K, Dröge-Laser W (2011) Heterodimers of the Arabidopsis transcription factors bZIP1 and bZIP53 reprogram amino acid metabolism during low energy stress. Plant Cell 23(1):381–395

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Dröge-Laser W, Kaiser A, Lindsay WP, Halkier BA, Loake GJ, Doerner P, Dixon R, Lamb C (1997) Rapid stimulation of a soybean protein-serine kinase that phosphorylates a novel bZIP DNA-binding protein, G/HBF-1, during the induction of early transcription-dependent defenses. EMBO J 16:726–738

    Article  PubMed Central  PubMed  Google Scholar 

  • Freitas RL, Carvalho CM, Fietto LG, Loureiro ME, Almeida AM, Fontes EP (2007) Distinct repressing modules on the distal region of the SBP2 promoter contribute to its vascular tissue-specific expression in different vegetative organs. Plant Mol Biol 65(5):603–614

    Article  CAS  PubMed  Google Scholar 

  • Fukazawa J, Sakai T, Ishida S, Yamaguchi I, Kamiya Y, Takahashi Y (2000) Repression of shoot growth, a bZIP transcriptional activator, regulates cell elongation by controlling the level of gibberellins. Plant Cell 12:901–915

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Garcia A et al (2008) Molecular mapping of soybean rust (Phakopsora pachyrhizi) resistance genes: discovery of a novel locus and alleles. Theor Appl Genet 117:545–553

    Article  CAS  PubMed  Google Scholar 

  • Goellner K et al (2010) Phakopsora pachyrhizi, the causal agent of Asian soybean rust. Mol Plant Pathol 11:169–177

    Article  CAS  PubMed  Google Scholar 

  • Hartman GL, Miles MR, Frederick RD (2005) Breeding for resistance to soybean rust. Plant Dis 89:664–666

    Article  Google Scholar 

  • Hartwig EE (1986) Identification of a fourth major gene conferring resistance to soybean rust. Crop Sci 26:1135–1136

  • Hartwig EE, Bromfield KR (1983) Relationships among 3 genes conferring specific resistance to rust in soybeans. Crop Sci 23:237–239

    Article  Google Scholar 

  • Hidayat OO, Somaatmadja S (1977) Screening of soybean breeding lines for resistance to soybean rust (Phakopsora pachyrhizi Sydow). Soybean Rust Newsl 1:9–22

  • Hoefle C, Loehrer M, Schaffrath U, Frank M, Schultheiss H, Hückelhoven R (2009) Transgenic suppression of cell death limits penetration success of the soybean rust fungus Phakopsora pachyrhizi into epidermal cells of barley. Phytopathology 99:220–226

    Article  CAS  PubMed  Google Scholar 

  • Huang J, Wang J, Zhang H (2005) Rice ZFP15 gene encoding for a novel C2H2-type zinc finger protein lacking DLN box, is regulated by spike development but not by abiotic stresses. Mol Biol Rep 32(3):177–183

    Article  CAS  PubMed  Google Scholar 

  • Hyten DL et al (2007) Map location of the Rpp1 locus that confers resistance to soybean rust in soybean. Crop Sci 47:837–838

    Article  CAS  Google Scholar 

  • Jakoby M et al (2002) bZIP transcription factors in Arabidopsis. Trends Plant Sci 7:106–111

    Article  CAS  PubMed  Google Scholar 

  • Katagiri F, Lain E, Chua NH (1989) Two tobacco DNA-binding proteins with homology to the nuclear factor CREB. Nature 340:727–730

    Article  CAS  PubMed  Google Scholar 

  • Kim KS et al (2012) Molecular mapping of soybean rust resistance in soybean accession PI 561356 and SNP haplotype analysis of the Rpp1 region in diverse germplasm. Theor Appl Genet 125(6):1339–1352

    Article  CAS  PubMed  Google Scholar 

  • Lee SJ et al (2002) PPI1: a novel pathogen-induced basic region-leucine zipper (bZIP) transcription factor from pepper. Mol Plant Microbe Interact 15:540–548

    Article  CAS  PubMed  Google Scholar 

  • Li S, Smith JR, Ray JD, Frederick RD (2012) Identification of a new soybean rust resistance gene in PI 567102B. Theor Appl Genet 125(1):133–142

  • Loake GJ, Faktor O, Lamb CJ, Dixon RA (1992) Combination of H-box [CCTACC(N), CT] and G-box (CACGTG) cis elements is necessary for feed-forward stimulation of a chalcone synthase promoter by the phenylpropanoid-pathway intermediate p-coumaric acid. Proc Natl Acad Sci U S A 89:9230–9234

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Miao ZH, Liu X, Lam E (1994) TGA3 is a distinct member of the TGA family of bZIP transcription factors in Arabidopsis thaliana. Plant Mol Biol 25:1–11

    Article  CAS  PubMed  Google Scholar 

  • Monteros MJ et al (2007) Mapping and confirmation of the ‘Hyuuga’ red-brown lesion resistance gene for Asian soybean rust. Crop Sci 47:829–834

    Article  CAS  Google Scholar 

  • Morceli TGS et al (2008) Identification and validation of microsatellite markers linked to the Rpp5 gene conferring resistance to Asian soybean rust. Pesq Agrop Brasileira 43:1533–1541

    Article  Google Scholar 

  • Nakagawa H, Ohmiya K, Hattori T (1996) A rice bZIP protein, designated OSBZ8, is rapidly induced by abscisic acid. Plant J 9:217–227

    Article  CAS  PubMed  Google Scholar 

  • Nakashima K, Yamaguchi-Shinozaki K (2006) Regulons involved in osmotic stress-responsive and cold stress-responsive gene expression in plants. Physiol Plant 126:62–71

    Article  CAS  Google Scholar 

  • Oyama T, Shimura Y, Okada K (1997) The Arabidopsis HY5 gene encodes a bZIP protein that regulates stimulus-induced development of root and hypocotyl. Genes Dev 11:2983–2995

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pandey AK et al (2011) Functional analysis of the Asian soybean rust resistance pathway mediated by Rpp2. Mol Plant Microbe Interact 24(2):194–206

    Article  CAS  PubMed  Google Scholar 

  • Patil VS, Wuike RV, Thakare CS, Chirame BB (1997) Viability of uredospores of Phakopsora pachyrhizi Syd. at different storage conditions. J Maharashtra Agric Univ 22:260–261

    Google Scholar 

  • Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 1:29–45

    Article  Google Scholar 

  • Pfaffl MW, Horgan GW, Dempfle L (2002) Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 1:30–36

    Google Scholar 

  • Reymond P, Farmer EE (1998) Jasmonate and salicylate as global signals for defense gene expression. Curr Opin Plant Biol 1:404–411

    Article  CAS  PubMed  Google Scholar 

  • Schindler U, Beckman H, Cashmore AR (1992) TGA I and G-box binding factors: two distinct classes of Arabidopsis leucine zipper proteins compete for the G-box like element TGACGTGG. Plant Cell 4:1309–1319

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Schneider KT et al (2011) Biphasic gene expression changes elicited by Phakopsora pachyrhizi in soybean correlate with fungal penetration and haustoria formation. Plant Physiol 157(1):355–371

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Singh K, Foley RC, Oñate-Sánchez L (2002) Transcription factors in plant defense and stress responses. Curr Opin Plant Biol 5:430–436

    Article  CAS  PubMed  Google Scholar 

  • Tak H, Mhatre M (2012) Cloning and molecular characterization of a putative bZIP transcription factor VvbZIP23 from Vitis vinifera. Protoplasma 250:333–345

  • Umezawa T, Fujita M, Fujita Y, Yamaquchi-Shinozaki K, Shinozaki K (2006) Engineering drought tolerance in plants: discovering and tailoring genes to unlock the future. Curr Opin Biotechnol 17:113–122

    Article  CAS  PubMed  Google Scholar 

  • Vance CP, Kirk TK, Sherwood RT (1980) Lignification as a mechanism of disease resistance. Annu Rev Phytopathol 18:259–288

    Article  CAS  Google Scholar 

  • Weisshaar B et al (1991) Light-inducible and constitutively expressed DNA-binding proteins recognizing a plant promder element with functional relevance in light responsiveness. EMBO J 10:1777–1786

    PubMed Central  CAS  PubMed  Google Scholar 

  • Xia N et al (2010) Characterization of a novel wheat NAC transcription factor gene involved in defense responseagainst stripe rust pathogen infection and abiotic stresses. Mol Biol Rep 37(8):3703–3712

    Article  CAS  PubMed  Google Scholar 

  • Yamaguchi-Shinozaki K, Shinozaki K (2005) Organization of cis-acting regulatory elements in osmotic- and cold-stress responsive promoters. Trends Plant Sci 10:88–94

    Article  CAS  PubMed  Google Scholar 

  • Yamaguchi-Shinozaki K, Shinozaki K (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol 57:781–803

    Article  CAS  PubMed  Google Scholar 

  • Yin Y et al (1997) RF2a, a bZIP transcriptional activator of the phloem-specific rice tungro bacilliform virus promoter, functions in vascular development. EMBO J 16:5247–5259

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhang Y et al (2009) Cloning and characterization of a bZIP transcription factor gene in wheat and its expression in response to stripe rust pathogen infection and abiotic stresses. Physiol Mol Plant Pathol 73:88–94

    Article  Google Scholar 

Download references

Acknowledgments

The authors thank Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (Capes), Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG), and the Universidade Federal de Viçosa, Brazil.

Conflict of interest

The authors declare that they have no conflict of interest.

Author contribution statement

MSA and LGF conceived and designed research. MSA, ZGS, PMPV, AMPP, and LNA conducted the experiments. MSA, PMPV, EGB, RVA, FCMG, and LGF analyzed the data. MSA wrote the manuscript. All authors read and approved the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Luciano G. Fietto.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Online Resource 1

Supplementary material describing the phylogenetic analysis of soybean bZIP proteins. (DOCX 882 kb)

Online Resource 2

Spreadsheet describing PFAM data (pfam.sanger.ac.uk/) from 148 bZIP protein sequences in Glycine max, selected from the GenBank database (http://blast.ncbi.nlm.nih.gov) (XLSX 28 kb)

Online Resource 3

Statistical analysis of the REST2009 output (XLSX 46 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Alves, M.S., Soares, Z.G., Vidigal, P.M.P. et al. Differential expression of four soybean bZIP genes during Phakopsora pachyrhizi infection. Funct Integr Genomics 15, 685–696 (2015). https://doi.org/10.1007/s10142-015-0445-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10142-015-0445-0

Keywords

Navigation