Skip to main content

Advertisement

SpringerLink
Log in

Identification of promoter motifs regulating ZmeIF4E expression level involved in maize rough dwarf disease resistance in maize (Zea Mays L.)

  • Review
  • Published:
Molecular Genetics and Genomics Aims and scope Submit manuscript

Abstract

Maize rough dwarf disease (MRDD, a viral disease) results in significant grain yield losses, while genetic basis of which is largely unknown. Based on comparative genomics, eukaryotic translation initiation factor 4E (eIF4E) was considered as a candidate gene for MRDD resistance, validation of which will help to understand the possible genetic mechanism of this disease. ZmeIF4E (orthologs of eIF4E gene in maize) encodes a protein of 218 amino acids, harboring five exons and no variation in the cDNA sequence is identified between the resistant inbred line, X178 and susceptible one, Ye478. ZmeIF4E expression was different in the two lines plants treated with three plant hormones, ethylene, salicylic acid, and jasmonates at V3 developmental stage, suggesting that ZmeIF4E is more likely to be involved in the regulation of defense gene expression and induction of local and systemic resistance. Moreover, four cis-acting elements related to plant defense responses, including DOFCOREZM, EECCRCAH1, GT1GAMSCAM4, and GT1CONSENSUS were detected in ZmeIF4E promoter for harboring sequence variation in the two lines. Association analysis with 163 inbred lines revealed that one SNP in EECCRCAH1 is significantly associated with CSI of MRDD in two environments, which explained 3.33 and 9.04 % of phenotypic variation, respectively. Meanwhile, one SNP in GT-1 motif was found to affect MRDD resistance only in one of the two environments, which explained 5.17 % of phenotypic variation. Collectively, regulatory motifs respectively harboring the two significant SNPs in ZmeIF4E promoter could be involved in the defense process of maize after viral infection. These results contribute to understand maize defense mechanisms against maize rough dwarf virus.

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

Similar content being viewed by others

References

  • Aranzana MJ, Kim S, Zhao K, Bakker E, Horton M, Jakob K, Lister C, Molitor J, Shindo C, Tang C (2005) Genome-wide association mapping in Arabidopsis identifies previously known flowering time and pathogen resistance genes. PLoS Genet 1:0531–0539

    Article  CAS  Google Scholar 

  • Bari R, Jones JDG (2009) Role of plant hormones in plant defence responses. Plant Mol Biol 69:473–488

    Article  PubMed  CAS  Google Scholar 

  • Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, Buckler ES (2007) TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23:2633–2635

    Article  PubMed  CAS  Google Scholar 

  • Custers J (2007) General introduction: plant defence mechanisms and the use of the hypersensitive response to engineer broad-spectrum disease resistance. In: Custers J (ed) Engineering disease resistance in plants. Wageningen Universiteit, Holland, pp 32–33

    Google Scholar 

  • De Benedetti A, Graff JR (2004) eIF-4E expression and its role in malignancies and metastases. Oncogene 23:3189–3199

    Article  PubMed  Google Scholar 

  • Di DP, Miao HQ, Lu YG, Tian LZ (2005) Study on the method of inoculation and identification for the resistance of maize to maize rough dwarf virus. J Agric Univ Hebei 28:76–78

    Google Scholar 

  • Di DP, Miao HQ, Lu YG, Tian LZ (2008) Analysis of correlation between the symptomatic leaf age and severity of maize rough dwarf disease. J Hebei Agric Sci 12(51–52):60

    Google Scholar 

  • Dong X (1998) SA, JA, ethylene, and disease resistance in plants. Curr Opin Plant Biol 1:316–323

    Article  PubMed  CAS  Google Scholar 

  • Epple P, Apel K, Bohlmann H (1997) Overexpression of an endogenous thionin enhances resistance of Arabidopsis against Fusarium oxysporum. Plant Cell 9:509–520

    PubMed  CAS  Google Scholar 

  • Fechter I, Hausmann L, Daum M, Sörensen TR, Viehöver P, Weisshaar B, Töpfer R (2012) Candidate genes within a 143 kb region of the flower sex locus in Vitis. Mol Genet Genomics 287:247–259

    Article  PubMed  CAS  Google Scholar 

  • Gao Z, Johansen E, Eyers S, Thomas CL, Noel Ellis T, Maule AJ (2004) The potyvirus recessive resistance gene, sbm1, identifies a novel role for translation initiation factor eIF4E in cell-to-cell trafficking. Plant J 40:376–385

    Article  PubMed  CAS  Google Scholar 

  • Gebhardt C, Ballvora A, Walkemeier B, Oberhagemann P, Schüler K (2004) Assessing genetic potential in germplasm collections of crop plants by marker-trait association: a case study for potatoes with quantitative variation of resistance to late blight and maturity type. Mol Breed 13:93–102

    Article  CAS  Google Scholar 

  • Gingras AC, Raught B, Sonenberg N (1999) eIF4 initiation factors: effectors of mRNA recruitment to ribosomes and regulators of translation. Annu Rev Biochem 68:913–963

    Article  PubMed  CAS  Google Scholar 

  • Han B, Zhang G (2010) Causes and prevention measures of maize rough dwarf disease in Xuzhou district. China Acad J 27:1578–1579

    Google Scholar 

  • Hershey JWB, Merrick WC (2000) Pathway and mechanism of initiation of protein synthesis. In: Sonenberg N, Hershey JWB, Mathews MB (eds) Translational control of gene expression. Cold Spring Harbor Laboratory, New York, pp 33–88

    Google Scholar 

  • Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database: 1999. Nucleic Acids Res 27:297–300

    Article  PubMed  CAS  Google Scholar 

  • Jones MW, Redinbaugh MG, Anderson RJ, Louie R (2004) Identification of quantitative trait loci controlling resistance to maize chlorotic dwarf virus. Theor Appl Genet 110:48–57

    Article  PubMed  CAS  Google Scholar 

  • Kang BC, Yeam I, Frantz JD, Murphy JF, Jahn MM (2005) The pvr1 locus in Capsicum encodes a translation initiation factor eIF4E that interacts with Tobacco etch virus VPg. Plant J 42:392–405

    Article  PubMed  CAS  Google Scholar 

  • Koornneef A, Rindermann K, Gatz C, Pieterse CMJ (2008) Histone modifications do not play a major role in salicylate-mediated suppression of jasmonate-induced PDF1.2 gene expression. Commun Integr Biol 1:143–145

    Article  PubMed  Google Scholar 

  • Kump KL, Bradbury PJ, Wisser RJ, Buckler ES, Belcher AR, Oropeza-Rosas MA, Zwonitzer JC, Kresovich S, McMullen MD, Ware D (2011) Genome-wide association study of quantitative resistance to southern leaf blight in the maize nested association mapping population. Nat Gen 43:163–168

    Google Scholar 

  • Lellis AD, Kasschau KD, Whitham SA, Carrington JC (2002) Loss-of-susceptibility mutants of Arabidopsis thaliana reveal an essential role for eIF (iso) 4E during Potyvirus infection. Curr Biol 12:1046–1051

    Article  PubMed  CAS  Google Scholar 

  • Li ZH, Guo XQ, Ye BH, Guo YK (2002) Ultrastructural alteration of maize plants infected with maize rough dwarf virus. Scienta Agricultura Sinica 35:264–266

    CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408

    Google Scholar 

  • Malosetti M, van der Linden CG, Vosman B, van Eeuwijk FA (2007) A mixed-model approach to association mapping using pedigree information with an illustration of resistance to Phytophthora infestans in potato. Genetics 175:879–889

    Article  PubMed  CAS  Google Scholar 

  • Mandadi KK, Misra A, Ren S, McKnight TD (2009) BT2, a BTB protein, mediates multiple responses to nutrients, stresses, and hormones in Arabidopsis. Plant Physiol 150:1930–1939

    Article  PubMed  CAS  Google Scholar 

  • Manicacci D, Camus-Kulandaivelu L, Fourmann M, Arar C, Barrault S, Rousselet A, Feminias N, Consoli L, Francès L, Méchin V (2009) Epistatic interactions between Opaque2 transcriptional activator and its target gene CyPPDK1 control kernel trait variation in maize. Plant Physiol 150:506–520

    Article  PubMed  CAS  Google Scholar 

  • Marcon A, Kaeppler S, Jensen S, Senior L, Stuber C (1999) Loci controlling resistance to high plains virus and wheat streak mosaic virus in a B73 x Mo17 population of maize. Crop Sci 39:1171–1177

    Article  Google Scholar 

  • McMullen MD, Jones MW, Simcox KD, Louie R (1994) Three genetic loci control resistance to wheat streak mosaic virus in the maize inbred Pa405. MPMI-Mol Plant Microbe Interact 7:708–712

    Article  CAS  Google Scholar 

  • Meng Y, Meng F, Han T, Liu K (2008) Causes and prevention measures of maize rough dwarf disease in Yellow and Huai River valleys of China. China Acad J 7:29–31

    Google Scholar 

  • Ming R, Brewbaker J, Pratt R, Musket T, McMullen M (1997) Molecular mapping of a major gene conferring resistance to maize mosaic virus. Theor Appl Genet 95:271–275

    Article  CAS  Google Scholar 

  • Miyoshi H, Suehiro N, Tomoo K, Muto S, Takahashi T, Tsukamoto T, Ohmori T, Natsuaki T (2006) Binding analyses for the interaction between plant virus genome-linked protein (VPg) and plant translational initiation factors. Biochimie 88:329–340

    Article  PubMed  CAS  Google Scholar 

  • Nicaise V, German-Retana S, Sanjuán R, Dubrana MP, Mazier M, Maisonneuve B, Candresse T, Caranta C, LeGall O (2003) The eukaryotic translation initiation factor 4E controls lettuce susceptibility to the potyvirus lettuce mosaic virus. Plant Physiol 132:1272–1282

    Article  PubMed  CAS  Google Scholar 

  • Nieto C, Morales M, Orjeda G, Clepet C, Monfort A, Sturbois B, Puigdomenech P, Pitrat M, Caboche M, Dogimont C (2006) An eIF4E allele confers resistance to an uncapped and non-polyadenylated RNA virus in melon. Plant J 48:452–462

    Article  PubMed  CAS  Google Scholar 

  • Palaisa KA, Morgante M, Williamsb M, Rafalski A (2003) Contrasting effects of selection on sequence diversity and linkage disequilibrium at two phytoene synthase loci. Plant Cell 15:1795–1806

    Article  PubMed  CAS  Google Scholar 

  • Park YS, Kunze S, Ni X, Feussner I, Kolomiets MV (2010) Comparative molecular and biochemical characterization of segmentally duplicated 9-lipoxygenase genes ZmLOX4 and ZmLOX5 of maize. Planta 231:1425–1437

    Article  PubMed  CAS  Google Scholar 

  • Penninckx IAMA, Thomma BPHJ, Buchala A, Métraux JP, Broekaert WF (1998) Concomitant activation of jasmonate and ethylene response pathways is required for induction of a plant defensin gene in Arabidopsis. Plant Cell 10:2103–2114

    PubMed  CAS  Google Scholar 

  • Poland JA, Bradbury PJ, Buckler ES, Nelson RJ (2011) Genome-wide nested association mapping of quantitative resistance to northern leaf blight in maize. Proc Natl Acad Sci 108:6893

    Article  PubMed  CAS  Google Scholar 

  • Redinbaugh MG, Jones MW, Gingery RE (2004) The genetics of virus resistance in maize (Zea Mays L.). Maydica 49:183–190

    Google Scholar 

  • Remington DL, Thornsberry JM, Matsuoka Y, Wilson LM, Whitt SR, Doebley J, Kresovich S, Goodman MM, Buckler ES (2001) Structure of linkage disequilibrium and phenotypic associations in the maize genome. Proc Natl Acad Sci 98:11479–11484

    Article  PubMed  CAS  Google Scholar 

  • Reymond P, Weber H, Damond M, Farmer EE (2000) Differential gene expression in response to mechanical wounding and insect feeding in Arabidopsis. Plant Cell 12:707–720

    PubMed  CAS  Google Scholar 

  • Robaglia C, Caranta C (2006) Translation initiation factors: a weak link in plant RNA virus infection. Trends Plant Sci 11:40–45

    Article  PubMed  CAS  Google Scholar 

  • Röder MS, Korzun V, Wendehake K, Plaschke J, Tixier MH, Leroy P, Ganal MW (1998) A microsatellite map of wheat. Genetics 149:2007–2023

    PubMed  Google Scholar 

  • Ruffel S, Gallois J, Lesage M, Caranta C (2005) The recessive potyvirus resistance gene pot-1 is the tomato orthologue of the pepper pvr2-eIF4E gene. Mol Genet Genomics 274:346–353

    Article  PubMed  CAS  Google Scholar 

  • Ryals JA, Neuenschwander UH, Willits MG, Molina A, Steiner HY, Hunt MD (1996) Systemic acquired resistance. Plant Cell 8:1809–1819

    PubMed  CAS  Google Scholar 

  • Saghai-Maroof M, Soliman K, Jorgensen RA, Allard R (1984) Ribosomal DNA spacer-length polymorphisms in barley: Mendelian inheritance, chromosomal location, and population dynamics. Proc Natl Acad Sci 81:8014–8018

    Article  PubMed  CAS  Google Scholar 

  • Sas I (1999) SAS/STAT User’s guide, Version 8. SAS Institute, Cary

    Google Scholar 

  • Shi LY, Li XH, Xie CX, Hao ZF, Weng JF, Zhang SH, Pan GT (2011) Development of SCARs from AFLP markers linked to resistance to maize rough dwarf virus (MRDV) using bulked segregant analysis in maize. Scientia Agricultura Sinica 44:1763–1774

    CAS  Google Scholar 

  • Shi LY, Hao ZF, Weng JF, Xie CX, Liu CL, Zhang DG, Li MS, Bai L, Li XH, Zhang SH (2012) Identification of a major quantitative trait locus for resistance to maize rough dwarf virus in a Chinese maize inbred line X178 using a linkage map based on 514 gene-derived single nucleotide polymorphisms. Mol Breed 30:615–625. doi:10.1007/s11032-011-9652-0

    Article  CAS  Google Scholar 

  • Simko I, Costanzo S, Haynes K, Christ B, Jones R (2004) Linkage disequilibrium mapping of a Verticillium dahliae resistance quantitative trait locus in tetraploid potato (Solanum tuberosum) through a candidate gene approach. Theor Appl Genet 108:217–224

    Article  PubMed  CAS  Google Scholar 

  • Stein N, Perovic D, Kumlehn J, Pellio B, Stracke S, Streng S, Ordon F, Graner A (2005) The eukaryotic translation initiation factor 4E confers multiallelic recessive Bymovirus resistance in Hordeum vulgare (L.). Plant J 42:912–922

    Article  PubMed  CAS  Google Scholar 

  • Stuiver MH, Custers JHHV (2001) Engineering disease resistance in plants. Nature 411:865–868

    Article  PubMed  CAS  Google Scholar 

  • Su J, Huang J, Liu H, Zhang J (2008) Causes and prevention measures of maize rough dwarf disease in Yellow and Huai River valleys of China. China Acad J 23:169–170

    Google Scholar 

  • Thomma BPHJ, Penninckx IAMA, Cammue B, Broekaert WF (2001) The complexity of disease signaling in Arabidopsis. Curr Opin Immunol 13:63–68

    Article  PubMed  CAS  Google Scholar 

  • Thornsberry JM, Goodman MM, Doebley J, Kresovich S, Nielsen D, Buckler ES (2001) Dwarf8 polymorphisms associate with variation in flowering time. Nat Genet 28:286–289

    Google Scholar 

  • Tian Z, Qian Q, Liu Q, Yan M, Liu X, Yan C, Liu G, Gao Z, Tang S, Zeng D (2009) Allelic diversities in rice starch biosynthesis lead to a diverse array of rice eating and cooking qualities. Proc Natl Acad Sci 106:21760–21765

    Article  PubMed  CAS  Google Scholar 

  • Weng J, Liu X, Wang Z, Wang J, Zhang L, Hao Z, Xie C, Li M, Zhang D, Bai L (2012) Molecular mapping of the major resistance quantitative trait locus qHS2. 09 with simple sequence repeat and single nucleotide polymorphism markers in maize. Phytopathology 102:692–699

    Article  PubMed  CAS  Google Scholar 

  • Wilson LM, Whitt SR, Ibáñez AM, Rocheford TR, Goodman MM, Buckler IVES (2004) Dissection of maize kernel composition and starch production by candidate gene association. Plant Cell 16:2719–2733

    Article  PubMed  CAS  Google Scholar 

  • Xia X, Melchinger AE, Kuntze L, Lübberstedt T (1999) Quantitative trait loci mapping of resistance to sugarcane mosaic virus in maize. Phytopathology 89:660–667

    Article  PubMed  CAS  Google Scholar 

  • Xie C, Zhang S, Li M, Li X, Hao Z, Bai L, Zhang D, Liang Y (2007) Inferring genome ancestry and estimating molecular relatedness among 187 Chinese maize inbred lines. J Genet Genomics 34:738–748

    Article  PubMed  Google Scholar 

  • Xu M, Melchinger A, Xia X, Lübberstedt T (1999) High-resolution mapping of loci conferring resistance to sugarcane mosaic virus in maize using RFLP, SSR, and AFLP markers. Mol General Genet MGG 261:574–581

    Article  CAS  Google Scholar 

  • Yan J, Kandianis CB, Harjes CE, Bai L, Kim EH, Yang X, Skinner DJ, Fu Z, Mitchell S, Li Q (2010) Rare genetic variation at Zea mays crtRB1 increases β-carotene in maize grain. Nat Genet 42:322–327

    Google Scholar 

  • Yeam I, Cavatorta JR, Ripoll DR, Kang BC, Jahn MM (2007) Functional dissection of naturally occurring amino acid substitutions in eIF4E that confers recessive potyvirus resistance in plants. Plant Cell 19:2913–2928

    Article  PubMed  CAS  Google Scholar 

  • Yu J, Buckler ES (2006) Genetic association mapping and genome organization of maize. Curr Opin Biotechnol 17:155–160

    Article  PubMed  CAS  Google Scholar 

  • Zhang Y (2010) Characteristic and prevention measures of maize rough dwarf disease in coastal areas of Jiansu province, China in 2009. China Acad J 23:171

    CAS  Google Scholar 

  • Zhu J, Zhang X (2012) Causes and prevention measures of maize rough dwarf disease. J Seed Ind Guide 1:20–21

    Google Scholar 

Download references

Acknowledgments

This study is jointly funded by National Hi-Tech Research Program (2012AA101104), and National Natural Science Foundation of China (30771350).

Author information

Authors and Affiliations

  1. National Key Facility of Crop Gene Resources and Genetic Improvement, Institute of Crop Science, Chinese Academy of Agricultural Sciences, 12 Zhong-guan-cun South St, 100081, Beijing, People’s Republic of China

    Liyu Shi, Jianfeng Weng, Changlin Liu, Xinyuan Song, Zhuanfang Hao, Chuanxiao Xie, Mingshun Li, Degui Zhang, Li Bai, Xinhai Li & Shihuang Zhang

  2. Institute of Plant Protection, Hebei Academy of Agricultural and Forestry Sciences, 071000, Baoding, People’s Republic of China

    Hongqin Miao

  3. Maize Research Institute, Sichuan Agricultural University, 625014, Ya’an, People’s Republic of China

    Guangtang Pan

Authors
  1. Liyu Shi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jianfeng Weng
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Changlin Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xinyuan Song
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Hongqin Miao
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Zhuanfang Hao
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Chuanxiao Xie
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Mingshun Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Degui Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Li Bai
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Guangtang Pan
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Xinhai Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Shihuang Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Xinhai Li or Shihuang Zhang.

Additional information

Communicated by A. K. Tyagi.

L. Shi and J. Weng contributed equally to this article.

Sequence data of ZmeIF4E in this article are available in the GenBank data libraries with accession number GU723473.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Shi, L., Weng, J., Liu, C. et al. Identification of promoter motifs regulating ZmeIF4E expression level involved in maize rough dwarf disease resistance in maize (Zea Mays L.). Mol Genet Genomics 288, 89–99 (2013). https://doi.org/10.1007/s00438-013-0737-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00438-013-0737-9

Keywords

Search

Navigation