Skip to main content

Advertisement

SpringerLink
Log in

Differential expression of genes in soybean in response to the causal agent of Asian soybean rust (Phakopsora pachyrhizi Sydow) is soybean growth stage-specific

  • Original Paper
  • Published:
Theoretical and Applied Genetics Aims and scope Submit manuscript

Abstract

Understanding plant host response to a pathogen such as Phakopsora pachyrhizi, the causal agent of Asian soybean rust (ASR), under different environmental conditions and growth stages is crucial for developing a resistant plant variety. The main objective of this study was to perform global transcriptome profiling of P. pachyrhizi-exposed soybean (Glycine max) with susceptible reaction to the pathogen from two distinct developmental growth stages using whole genome Affymetrix microarrays of soybean followed by confirmation using a resistant genotype. Soybean cv. 5601T (susceptible to ASR) at the V4 and R1 growth stages and Glycine tomentella (resistant to ASR) plants were inoculated with P. pachyrhizi and leaf samples were collected after 72 h of inoculation for microarray analysis. Upon analyzing the data using Array Assist software at 5% false discovery rate (FDR), a total of 5,056 genes were found significantly differentially expressed at V4 growth stage, of which 2,401 were up-regulated, whereas 579 were found differentially expressed at R1 growth stage, of which 264 were up-regulated. There were 333 differentially expressed common genes between the V4 and R1 growth stages, of which 125 were up-regulated. A large difference in number of differentially expressed genes between the two growth stages indicates that the gene expression is growth-stage-specific. We performed real-time RT-PCR analysis on nine of these genes from both growth stages and both plant species and found results to be congruent with those from the microarray analysis.

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

  • Akashi T, Aoki T, S Ayabe (1999) Cloning and functional expression of a cytochrome P450 cDNA encoding 2-hydroxyisoflavanone synthase involved in biosynthesis of the isoflavonoid skeleton in licorice. Plant Physiol 121:821–828

    Article  PubMed  CAS  Google Scholar 

  • Bohnert H-J, Ayoubi P, Borchert C, Bressan R-A, Burnap R-L, Cushman J-C, Cushman M-A, Deyholos M, Fischer R, Galbraith D-W, Hasegawa P-M, Jenks M, Kawasaki S, Koiwa H, Kore-eda S, Lee B-H, Michalowski C-B, Misawa E, Nomura M, Ozturk N, Postier B, Prade R, Song C-P, Tanaka Y, Wang H, Zhu J-K (2001) A genomics approach towards salt stress tolerance. Plant Physiol Biochem (Paris) 39:295–311

    Article  CAS  Google Scholar 

  • Cassab GI, Nieto Sotelo J, Cooper JB (1985) A developmentally regulated hydroxyproline-rich glycoprotein from the cell walls of soybean seed coats. Plant Physiol 77:532–535

    Article  PubMed  CAS  Google Scholar 

  • Chong J, Pierrel M-A, Atanassova R, Werck-Reichhart D, Fritig B, Saindrenan P (2001) Free and conjugated benzoic acid in tobacco plants and cell cultures. Induced accumulation upon elicitation of defense responses and role as salicylic acid precursors. Plant Physiol 125:318–328

    Article  PubMed  CAS  Google Scholar 

  • Coenen C, Bierfreund N, Luthen H (2002) Developmental regulation of H+-ATPase-dependent auxin responses in the diageotropica mutant of tomato (Lycopersicon esculentum). Physiol Plantarum 114:461–471

    Article  CAS  Google Scholar 

  • Davies C, Boss PK, Robinson SP (1997) Treatment of grape berries, a nonclimacteric fruit with a synthetic auxin, retards ripening and alters the expression of developmentally regulated genes. Plant Physiol 115:1155–1161

    PubMed  CAS  Google Scholar 

  • DeMortel MV, Recknor JC, Graham MA, Nettleton D, Dittman JD, Nelson RT, Godoy CV, Abdelnoor RV, Almeida ÁMR, Baum TJ, Whitham SA (2007a) Distinct biphasic mRNA changes in response to Asian soybean rust infection. MPMI 20:887–899

    Article  CAS  Google Scholar 

  • DeMortel MV, Schneider KT, Bancroft T, Nettleton D, Frederick RD, Baum TJ, Whitham SA (2007b) Gene expression in a soybean cultivar containing the Rpp3 gene for resistance to Phakopsora pachyrhizi. Phytopathology 97:S117–S118

    Google Scholar 

  • Dhaubhadel S, Gijzen M, Moy P, Farhangkhoee M (2007) Transcriptome analysis reveals a critical role of CHS7 and CHS8 genes for isoflavonoid synthesis in soybean seeds. Plant Physiol 143:326–338

    Article  PubMed  CAS  Google Scholar 

  • Dong JZ, Dunstan DI (1996) Characterization of three heat-shock-protein genes and their developmental regulation during somatic embryogenesis in white spruce {Picea glauca (Moench) Voss}. Planta 200:85–91

    Article  PubMed  CAS  Google Scholar 

  • Fehr WR, Caviness CE (1977) Stages of soybean development. Special Report 80, Cooperative Extension Services. Iowa State University, Ames, IA, p 7

  • Frederick RD, Snyder CL, Peterson GL, Bonde MR (2002) Polymerase chain reaction assays for the detection and discrimination of the soybean rust pathogens Phakopsora pachyrhizi and P. meibomiae. Phytopathology 92:217–227

    Article  PubMed  CAS  Google Scholar 

  • Guenther JF, Chanmanivone N, Galetovic MP, Wallace IS, Cobb JA, Roberts DM (2003) Phosphorylation of soybean nodulin 26 on serine 262 enhances water permeability and is regulated developmentally and by osmotic signals. Plant Cell 15:981–991

    Article  PubMed  CAS  Google Scholar 

  • Gupta GK, Ansari M, Karmakar P, Husain S, Ramteke R (1999) Resurrection of soybean rust (Phakopsora pachyrhizi) in India. In: Kauffman HE (ed) World soybean research conference VI. University of Illinois, Chicago, p 617

    Google Scholar 

  • Halkier BA, Gershenzon J (2006) Biology and biochemistry of Glucosinolates. Annu Rev Plant Biol 57:303–333

    Article  PubMed  CAS  Google Scholar 

  • Hartman GL, Wang TC, Hymowitz T (1992) Sources of resistance to soybean rust in perennial Glycine species. Plant Dis 76:396–399

    Google Scholar 

  • Hartman GL, Wang TC, Tschanz AT (1991) Soybean rust development and the quantitative relationship between rust severity and soybean yield. Plant Dis 75:596–600

    Google Scholar 

  • Higgins CF (1992) ABC transporters: from microorganisms to man. Annu Rev Cell Biol 8:67–113

    Article  PubMed  CAS  Google Scholar 

  • Horiguchi G, Kawakami N, Kusumi K (1998) Developmental regulation of genes for microsome and plastid w-3 fatty acid desaturases in wheat (Triticum aestivum L.). Plant Cell Physiol 39:540–544

    CAS  Google Scholar 

  • Hyten DL, Hartman GL, Nelson RL, Frederick RD, Concibido VC, Narvel JM, Cregan PB (2007) Map location of the Rpp1 locus that confers resistance to soybean rust in soybean. Crop Sci 47:837–840

    CAS  Google Scholar 

  • Jasinski M, Stukkens Y, Degand H, Purnelle B, Marchand-Brynaert J, Boutry M (2001) A plant plasma membrane ATP binding cassette-type transporter is involved in antifungal terpenoid secretion. Plant Cell 13:1095–1108

    Article  PubMed  CAS  Google Scholar 

  • Jung W, Yu O, Lau S-MC, O’Keefe DP, Odell J, Fader G, McGonigle B (2000) Identification and expression of isoflavone synthase, the key enzyme for biosynthesis of isoflavones in legumes. Nat Biotechnol 18:208–212

    Article  PubMed  CAS  Google Scholar 

  • Kawasaki S, Borchert C, Deyholos M, Wang H, Brazille S, Kawai K, Galbraith D, Bohnert H-J (2001) Gene expression profiles during the initial phase of salt stress in rice. Plant Cell 13:889–905

    Article  PubMed  CAS  Google Scholar 

  • Kus JV, Zaton K, Sarkar R, Cameron RK (2002) Age-related resistance in Arabidopsis is a developmentally regulated defense response to Pseudomonas syringae. Plant Cell 14:479–490

    Article  PubMed  CAS  Google Scholar 

  • Lee S, Kim S-Y, Chung E, Joung Y-H, Pai H-B, Hur C-G, Choi D (2004) EST and microarray analyses of pathogen-responsive genes in hot pepper (Capsicum annuum L.) non-host resistance against soybean pustule pathogen (Xanthomonas axonopodis pv. glycines). Funct Integr Genomics 4:196–205

    Article  PubMed  Google Scholar 

  • León J, Sánchez-Serrano JJ (1999) Molecular biology of jasmonic acid biosynthesis in plants. Plant Physiol Biochem 37:373–380

    Article  Google Scholar 

  • Luan S (2003) Protein phosphatases in plants. Annu Rev Plant Biol 54:63–92

    Article  PubMed  CAS  Google Scholar 

  • Luo M, Liang XQ, Dang P, Holbrook CC, Bausher MG, Lee RD, Guo BZ (2005) Microarray-based screening of differentially expressed genes in peanut in response to Aspergillus parasiticus infection and drought stress. Plant Sci 169:695–703

    Article  CAS  Google Scholar 

  • Martin GB, Bogdanove AJ, Sessa G (2003) Understanding the functions of plant disease resistance proteins. Annu Rev Plant Biol 54:23–61

    Article  PubMed  CAS  Google Scholar 

  • Monteros MJ, Missaoui AM, Phillips DV, Walker DR, Boerma HR (2007) Mapping and confirmation of the ‘Hyuuga’ red-brown lesion resistance gene for Asian soybean rust. Crop Sci 47:829–836

    CAS  Google Scholar 

  • Moy P, Qutob D, Chapman BP, Atkinson I, Gijzen M (2004) Patterns of gene expression upon infection of soybean plants by Phytophthora sojae. MPMI 17:1051–1062

    Article  PubMed  CAS  Google Scholar 

  • Panthee DR, Yuan JS, Wright DL, Marois JJ, Mailhot D Jr, NS C (2007) Gene expression analysis in soybean in response to the causal agent of Asian soybean rust (Phakopsora pachyrhizi Sydow) in an early growth stage. Funct Integr Genomics 7:291–301

    Article  PubMed  CAS  Google Scholar 

  • Pasquer F, Isidore E, Zarn J, Keller B (2005) Specific patterns of changes in wheat gene expression after treatment with three antifungal compounds. Plant Mol Biol 57:693–707

    Article  PubMed  CAS  Google Scholar 

  • Puthoff D-P, Nettleton D, Rodermel S-R, Baum T-J (2003) Arabidopsis gene expression changes during cyst nematode parasitism revealed by statistical analyses of microarray expression profiles. Plant J 33:911–921

    Article  PubMed  CAS  Google Scholar 

  • Rahangdale SR, Raut VM (2003) Evaluation of soybean germplasm lines for rust (Phakopsora pachyrhizi) resistance. Indian J Agric Sci 73:120–121

    Google Scholar 

  • Ramteke R, Karmakar PG, Gupta GK, Singh RK, Khan IR (2003) Resistance genes for rust and yellow mosaic diseases in soybean—a review. J Oilseeds Res 20:195–203

    Google Scholar 

  • Rea PA (2007) Plant ATP-binding cassette transporters. Annu Rev Plant Biol 58:347–375

    Article  PubMed  CAS  Google Scholar 

  • Ribnicky DM, Shulaev V, Raskin I (1998) Intermediates of salicylic acid biosynthesis in tobacco. Plant Physiol 118:565–572

    Article  PubMed  CAS  Google Scholar 

  • Rojas A, Almoguera C, Carranco R (2002) Selective activation of the developmentally regulated Ha hsp17.6 G1 promoter by heat stress transcription factors. Plant Physiol 129:1207–1215

    Article  PubMed  CAS  Google Scholar 

  • Schenk PM, Kazan K, Wilson I, Anderson JP, Richmond T, Somerville SC, Manners JM (2000) Coordinated plant defense responses in Arabidopsis revealed by microarray analysis. PNAS 97:11655–11660

    Article  PubMed  CAS  Google Scholar 

  • Schilmiller AL, Koo AJK, Howe GA (2007) Functional diversification of acyl-coenzyme A oxidases in jasmonic acid biosynthesis and action. Plant Physiol 143:812–824

    Article  PubMed  CAS  Google Scholar 

  • Schneider KT, DeMortel MV, Nettleton D, Frederick RD, Baum TJ, Whitham SA (2006) Microarray analysis of Rpp3-mediated resistance to soybean rust infection. In: National soybean rust symposium, The American Phytopathological Society, 3340 Pilot Knob Road, St. Paul, MN, 5512, St. Loius, MO

  • Schoen DJ, Burdon JJ, Brown AHD (1992) Resistance of Glycine tomentella to soybean leaf rust Phakopsora pachyrhizi in relation to ploidy level and geographic distribution. Theor Appl Genet 83:827–832

    Article  Google Scholar 

  • Schuler MA, Werck-Reichhart D (2003) Functional genomics of P450s. Annu Rev Plant Biol 54:629–667

    Article  PubMed  CAS  Google Scholar 

  • Shen H, Chen J, Wang Z, Yang C, Sasaki T, Yamamoto Y, Matsumoto H, Yan X (2006) Root plasma membrane H+-ATPase is involved in the adaptation of soybean to phosphorus starvation. J Exp Bot 57:1353–1362

    Article  PubMed  CAS  Google Scholar 

  • Shimada N, Akashi T, Aoki T, S Ayabe (2000) Induction of isoflavonoid pathway in the model legume Lotus japonicus: molecular characterization of enzymes involved in phytoalexin biosynthesis. Plant Sci 160:37–47

    Article  PubMed  CAS  Google Scholar 

  • Soytech Inc. (2006) Oilseed statistics. 2006 Soy and oilseed blue book: the annual directory of the world oilseed directory. Soytech Inc., Bar Harbor, pp 314–358

    Google Scholar 

  • Stewart CN Jr, Via LE (1993) A rapid CTAB DNA isolation technique useful for RAPD fingerprinting and other PCR applications. Biotechniques 14:748–751

    PubMed  CAS  Google Scholar 

  • Subramanian S, Graham MY, Yu O, Graham TL (2005) RNA interference of soybean isoflavone synthase genes leads to silencing in tissues distal to the transformation site and to enhanced susceptibility to Phytophthora sojae. Plant Physiol 137:1345–1353

    Article  PubMed  CAS  Google Scholar 

  • Tian L, Wang J, Fong MP (2003) Genetic control of developmental changes induced by disruption of Arabidopsis histone deacetylase 1 (AtHD1) expression. Genetics 165:399–409

    PubMed  CAS  Google Scholar 

  • Tian ZD, Liu J, Wang BL, Xie CH (2006) Screening and expression analysis of Phytophthora infestans induced genes in potato leaves with horizontal resistance. Plant Cell Rep 25:1094–1103

    Article  PubMed  CAS  Google Scholar 

  • Tschanz A, Shanmugasundaram S (1984) Soybean rust. In: Shibles R (ed) World soybean research conference III. Westview Press Inc., London, pp 562–567

    Google Scholar 

  • Wasternack C, Miersch O, Kramell R, Hause B, Ward J, Beale M, Boland W, Parthier B, Feussner I (1998) Jasmonic acid: biosynthesis, signal transduction, gene expression. Fett/Lipid 100:139–146

    Article  CAS  Google Scholar 

  • Wildermuth MC, Dewdney J, Wu G, Ausubel FM (2001) Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414:562–565

    Article  PubMed  CAS  Google Scholar 

  • Winkel-Shirley B (2001) Flavonoid biosynthesis. A colorful model for genetics, biochemistry, cell biology, and biotechnology. Plant Physiol 126:485–493

    Article  PubMed  CAS  Google Scholar 

  • Wu Z, Irizarry R, Gentleman R, Martinez Murillo F, Spencer F (2004) A model based background adjustment for oligonucleotide expression arrays. J Am Stat Assoc 99:909–917

    Article  Google Scholar 

  • Yen S-K, Chung M-C, Chen P-C, Yen HE (2001) Environmental and developmental regulation of the wound-induced cell wall protein WI12 in the halophyte ice plant. Plant Physiol 127:517–528

    Article  PubMed  CAS  Google Scholar 

  • Yu O, Shi J, Hession AO, Maxwell CA, McGonigle B, Odell JT (2003) Metabolic engineering to increase isoflavone concentration in soybean seeds. Phytochemistry 63:753–763

    Article  PubMed  CAS  Google Scholar 

  • Yuan JS, Reed A, Chen F Jr, NS C (2006) Statistical analysis of real-time PCR data. BMC Bioinformatics I7:85

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This study was supported by Tennessee Soybean Promotion Board and funds from the Tennessee Agricultural Experiment Station. Julia Gouffon at the Affymetrix Core Center of the University of Tennessee, is sincerely acknowledged for her help in conducting the microarray experiment. We appreciate the collaborations and conversations with Vince Pantalone, Kurt Lamour, and Mitra Mazarei. Minimum information about a microarray experiment (MIAME) guidelines were followed in this study.

Author information

Author notes

  1. Dilip R. Panthee

    Present address: Department of Horticultural Science, Mountain Horticultural Crops Research and Extension Center, North Carolina State University, 455 Research Drive, Mills River, NC, 28759, USA

Authors and Affiliations

  1. Department of Plant Sciences, 252 Ellington Plant Sciences, The University of Tennessee, 2431 Joe Johnson Dr., Knoxville, TN, 37996, USA

    Dilip R. Panthee, Joshua S. Yuan & C. Neal Stewart Jr

  2. North Florida Agriculture Research and Education Center, The University of Florida, Quincy, FL, 32351, USA

    James J. Marois, David L. Wright & Dario Narváez

Authors
  1. Dilip R. Panthee
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. James J. Marois
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. David L. Wright
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Dario Narváez
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Joshua S. Yuan
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. C. Neal Stewart Jr
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Dilip R. Panthee.

Additional information

Communicated by D. A. Lightfoot.

Electronic supplementary material

Below is the link to the electronic supplementary material.

122_2008_905_MOESM1_ESM.xls

Table S-1 Differentially expressed genes in soybean in response to Phakopsora pachyrhizi at V4 growth stage (XLS 934 kb)

122_2008_905_MOESM2_ESM.xls

Table S-2 Differentially expressed genes in soybean in response to Phakopsora pachyrhizi at R1 growth stage (XLS 123 kb)

122_2008_905_MOESM3_ESM.xls

Table S-3 Number of transcripts of a gene or a gene family expressed differentially at V4 and R1 growth stage of soybean cv. 5601T in response to Phakopsora pachyrhizi (XLS 173 kb)

122_2008_905_MOESM4_ESM.xls

Table S-4 Differentially expressed unique known genes at V4 growth stage of soybean in response to Phakopsora pachyrhizi (XLS 413 kb)

122_2008_905_MOESM5_ESM.xls

Table S-5 Differentially expressed unique known genes at R1 growth stage of soybean in response to Phakopsora pachyrhizi (XLS 43 kb)

122_2008_905_MOESM6_ESM.xls

Table S-6 Differentially expressed common genes at V4 and R1 growth stages of soybean in response to Phakopsora pachyrhizi (XLS 77 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Panthee, D.R., Marois, J.J., Wright, D.L. et al. Differential expression of genes in soybean in response to the causal agent of Asian soybean rust (Phakopsora pachyrhizi Sydow) is soybean growth stage-specific. Theor Appl Genet 118, 359–370 (2009). https://doi.org/10.1007/s00122-008-0905-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-008-0905-1

Keywords

Search

Navigation