Skip to main content

Advertisement

Log in

Differential transcript accumulation in chickpea during early phases of compatible interaction with a necrotrophic fungus Ascochyta rabiei

  • Published:
Molecular Biology Reports Aims and scope Submit manuscript

Abstract

The initial phases of the disease establishment are very crucial for the compatible interactions. Pathogens must overcome the responses generated by the host for the onset of disease invasion. The compatible interaction is inadequately represented in plant-pathogen interaction studies. To gain broader insight into the early responses elicited by chickpea blight fungus Ascochyta rabiei during compatible interaction; we isolated early responsive genes of chickpea using PCR based suppression subtractive hybridization (SSH) strategy. We obtained ~250 unique genes after homology search and redundancy elimination. Based on their potential cellular functions, these genes were broadly classified into eleven different categories viz. stress, signaling, gene regulation, cellular metabolism and genes of unknown functions. Present study revealed few unexpected genes which have a possible role in induced immunity and disease progression. We employed macroarray, northern blot, real-time PCR and cluster analysis to develop transcript profiles. Most of the genes analyzed were early induced and were transcriptionally upregulated upon 24 h post inoculation. Our approach has rendered the isolation of early responsive genes involved in signaling and regulation of metabolic changes upon fungal infection. The information obtained will help to dissect the molecular mechanisms during compatible chickpea–Ascochyta interactions.

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

Similar content being viewed by others

References

  1. Feng H, Wang X, Sun Y, Wang X, Chen X, Guo J, Duan Y, Huang L, Kang Z (2011) Cloning and characterization of a calcium binding EF-hand protein gene TaCab1 from wheat and its expression in response to Puccinia striiformis f. sp. tritici and abiotic stresses. Mol Biol Rep 38:3857–3866

    Article  PubMed  CAS  Google Scholar 

  2. Oliver RP, Ipcho SVS (2004) Arabidopsis pathology breathes new life into the necrotrophs-vs. biotrophs classification of fungal pathogens. Mol Plant Pathol 5:347–352

    Article  PubMed  CAS  Google Scholar 

  3. Markham JE, Hille J (2001) Host selective toxins as agents of cell death in plant–fungus interactions. Mol Plant Pathol 2:229–239

    Article  PubMed  CAS  Google Scholar 

  4. Wolpert TJ, Dunkle LD, Ciuffetti LM (2002) Host-selective toxins and avirulence determinants: what’s in a name? Annu Rev Phytopathol 40:251–285

    Article  PubMed  CAS  Google Scholar 

  5. Staples RC, Mayer AM (2003) Suppression of host resistance by fungal plant pathogens. Isr J Plant Sci 51:175–186

    Article  Google Scholar 

  6. Govrin EM, Levine A (2000) The hypersensitive response facilitates plant infection by the necrotrophic pathogen Botrytis cinerea. Curr Biol 10:751–757

    Article  PubMed  CAS  Google Scholar 

  7. Jones JDG, Dangl JL (2006) The plant immune system. Nature 444:323–329

    Article  PubMed  CAS  Google Scholar 

  8. Chisholm ST, Coaker G, Day B, Staskawicz BJ (2006) Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124:803–814

    Article  PubMed  CAS  Google Scholar 

  9. Faris JD, Zhang Z, Lu H, Reddy L, Cloutier S, Fellers JP, Meinhardt SW, Rasmussen JB, Xu SS, Oliver RP, Simons KJ, Friesen TL (2010) A unique wheat disease resistance-like gene governs effector triggered susceptibility to necrotrophic pathogens. Proc Natl Acad Sci USA 107:13544–13549

    Article  PubMed  CAS  Google Scholar 

  10. Panstruga R (2003) Establishing compatibility between plants and obligate biotrophic pathogens. Curr Opin Plant Biol 6:320–326

    Article  PubMed  CAS  Google Scholar 

  11. Nene YL, Reddy MV (1987) Chickpea diseases and their control. In: Saxena MC, Singh KB (eds) The chickpea. CAB International, UK, pp 233–270

    Google Scholar 

  12. Gaur RB, Singh RD (1996) Effects of Ascochyta blight on grain yield and protein in chickpea. Indian J Mycol Plant Pathol 26:259–262

    Google Scholar 

  13. Jayakumar P, Gossen BD, Gan YT, Warkentin TD, Banniza S (2005) Ascochyta blight of chickpea: infection and host resistance mechanisms. Can J Plant Pathol 27:499–509

    Article  CAS  Google Scholar 

  14. Armstromg-Cho C, Gossen BD (2005) Impact of glandular hair exudates on infection of chickpea by Ascochyta rabiei. Can J Bot 83:22–27

    Article  Google Scholar 

  15. Daniel S, Tiemann K, Wittkampf U, Bless W, Hinderer W, Barz W (1990) Elicitor-induced metabolic changes in cell cultures of chickpea (Cicer arietinum L.) cultivars resistant and susceptible to Ascochyta rabiei: I. Investigations of enzyme activities involved in isoflavone and pterocarpan phytoalexin biosynthesis. Planta 182:270–278

    Article  CAS  Google Scholar 

  16. Kessmann H, Barz W (1987) Accumulation of isoflavone and pterocarpan phytoalexins in cell suspension cultures of different cultivars of chickpea. Plant Cell Rep 6:55–59

    Article  CAS  Google Scholar 

  17. Khirbat SK, Jalali BL (1998) Production of phytoalexin in the leaves of chickpea (Cicer arietinum L.) after inoculation with Ascochyta rabiei. Legume Res 21:135–143

    Google Scholar 

  18. Cobos MJ, Rubio J, Strange RN, Moreno MT, Gil J, Millan T (2006) A new QTL for ascochyta blight resistance in an RIL population derived from an interspecific cross in chickpea. Euphytica 149:105–111

    Article  Google Scholar 

  19. Flandez-Galvez H, Ades PK, Ford R, Pang ECK, Taylor PWJ (2003) QTL analysis for ascochyta blight resistance in an intraspecific population of chickpea (Cicer arietinum L.). Theor Appl Genet 107:1257–1265

    Article  PubMed  CAS  Google Scholar 

  20. Iruela M, Rubio J, Barro F, Cubero JI, Millan T, Gil J (2006) Detection of two quantitative trait loci for resistance to ascochyta blight in an intra-specific cross of chickpea (Cicer arietinum L.): development of SCAR markers associated with resistance. Theor Appl Genet 112:278–287

    Article  PubMed  CAS  Google Scholar 

  21. Santra DK, Tekeoglu M, Ratnaparkhe M, Kaiser WJ, Muehlbauer FJ (2000) Identification and mapping of QTLs conferring resistance to ascochyta blight in chickpea. Crop Sci 40:1606–1612

    Article  CAS  Google Scholar 

  22. Tekeoglu M, Isik M, Muehlbauer FJ (2004) QTL analysis of ascochyta blight resistance in chickpea. Turk J Agric For 28:183–187

    CAS  Google Scholar 

  23. Mantri NL, Ford R, Coram TE, Pang ECK (2007) Transcriptional profiling of chickpea genes differentially regulated in response to high-salinity, cold and drought. BMC Genomics 8:303

    Article  PubMed  Google Scholar 

  24. Singh A, Singh IK, Verma PK (2008) Differential transcript accumulation in Cicer arietinum L. in response to a chewing insect Helicoverpa armigera and defence regulators correlate with reduced insect performance. J Exp Bot 59:2379–2392

    Article  PubMed  CAS  Google Scholar 

  25. Ashraf N, Ghai D, Barman P, Basu S, Gangisetty N, Mandal MK, Chakraborty N, Datta A, Chakraborty S (2009) Comparative analyses of genotype dependent expressed sequence tags and stress-responsive transcriptome of chickpea wilt illustrate predicted and unexpected genes and novel regulators of plant immunity. BMC Genomics 10:415

    Article  PubMed  Google Scholar 

  26. Huang JY, Jie ZJ, Wang LJ, Yan XH, Wei WH (2011) Analysis of the differential expression of the genes related to Brassica napus seed development. Mol Biol Rep 38:1055–1061

    Article  PubMed  CAS  Google Scholar 

  27. Sun P, Guo Y, Qi J, Zhou L, Li X (2010) Isolation and expression analysis of tuberous root development related genes in Rehmannia glutinosa. Mol Biol Rep 37:1069–1079

    Article  PubMed  CAS  Google Scholar 

  28. Gu L, Xu D, You T, Li X, Yao S, Chen S, Zhao J, Lan H, Zhang F (2011) Analysis of gene expression by ESTs from suppression subtractive hybridization library in Chenopodium album L. under salt stress. Mol Biol Rep. doi:10.1007/s11033-011-0678-5

  29. Sharma K, Mishra AK, Misra RS (2009) Identification and characterization of differentially expressed genes in the resistance reaction in taro infected with Phytophthora colocasiae. Mol Biol Rep 36:1291–1297

    Article  PubMed  CAS  Google Scholar 

  30. Coram TE, Pang ECK (2006) Expression profiling of chickpea genes differentially regulated during a resistance response to Ascochyta rabiei. Plant Biotechnol J 4:647–666

    Article  PubMed  CAS  Google Scholar 

  31. Cornels H, Ichinose Y, Barz W (2000) Characterization of cDNAs encoding two glycine-rich proteins in chickpea (Cicer arietinum L.): accumulation in response to fungal infection and other stress factors. Plant Sci 154:83–88

    Article  PubMed  CAS  Google Scholar 

  32. Ichinose YK, Toyoda BarzW (1999) cDNA cloning and gene expression of three small GTP-binding proteins in defense response of chickpea. Biochim Biophys Acta 1489:462–466

    PubMed  CAS  Google Scholar 

  33. Hanselle T, Ichinose Y, Barz W (2001) Biochemical and molecular biological studies on infection (Ascochyta rabiei)-induced thaumatin-like proteins from chickpea plants (Cicer arietinum L.). Z Naturforsch 56:1095–1107

    CAS  Google Scholar 

  34. Rea G, Metoui O, Infantino A, Federico R, Angelini R (2002) Copper amine oxidase expression in defense responses to wounding and Ascochyta rabiei invasion. Plant Physiol 128:865–875

    Article  PubMed  CAS  Google Scholar 

  35. Boominathan P, Shukla R, Kumar A, Manna D, Negi D, Verma PK, Chattopadhyay D (2004) Long term transcript accumulation during the development of dehydration adaptation in Cicer arietinum. Plant Physiol 135:1608–1620

    Article  PubMed  CAS  Google Scholar 

  36. Sambrook J, Russell DW (2001) Molecular cloning-a laboratory manual, 3rd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor

    Google Scholar 

  37. Diatchenko L, Lau YF, Campbell AP, Chenchik A, Moqadam F, Huang B, Lukyanov S, Lukyanov K, Gurskaya N, Sverdlov ED, Siebert PD (1996) Suppression subtractive hybridization: a method for generating differentially regulated or tissue-specific cDNA probes and libraries. Proc Natl Acad Sci USA 93:6025–6030

    Article  PubMed  CAS  Google Scholar 

  38. Shi J-l, Wang Y-j, Zhu Z-g, Zhang C-h (2010) The EST Analysis of a suppressive subtraction cDNA library of chinese wild Vitis pseudoreticulata inoculated with Uncinula necator. Agric Sci China 9:233–241

    Article  CAS  Google Scholar 

  39. Fossdal CG, Nagy NE, Johnsen O, Dalen LS (2007) Local and systemic stress responses in Norway spruce: similarities in gene expression between a compatible pathogen interaction and drought stress. Physiol Mol Plant Pathol 70:161–173

    Article  CAS  Google Scholar 

  40. Thomma BPHJ, Eggermont K, Penninckx IAMA, Mauch-Mani B, Vogelsang R, Cammue BPA, Broekaert WF (1998) Separate jasmonate-dependent and salicylate-dependent defense-response pathways in Arabidopsis are essential for resistance to distinct microbial pathogens. Proc Natl Acad Sci USA 95:15107–15111

    Article  PubMed  CAS  Google Scholar 

  41. Xie D, Feys BF, James S, Nieto-Rostro M, Turner JG (1998) COI1: an Arabidopsis gene required for jasmonate-regulated defense and fertility. Science 280:1091–1094

    Article  PubMed  CAS  Google Scholar 

  42. Yan J, Zhang C, Gu M, Bai Z, Zhang W, Qi T, Cheng Z, Peng W, Luo H, Nan F, Wang Z, Xie D (2009) The Arabidopsis CORONATINE INSENSITIVE1 protein is a jasmonate receptor. Plant Cell 21:2220–2236

    Article  PubMed  CAS  Google Scholar 

  43. Devoto A, Nieto-Rostro M, Xie D, Ellis C, Harmston R, Patrick E, Davis J, Sherratt L, Coleman M, Turner JG (2002) COI1 links jasmonate signalling and fertility to the SCF ubiquitin-ligase complex in Arabidopsis. Plant J 32:457–466

    Article  PubMed  CAS  Google Scholar 

  44. Steele CL, Gijzen M, Qutob D, Dixon RA (1999) Molecular characterization of the enzyme catalyzing the aryl migration reaction of isoflavonoid biosynthesis in soybean. Arch Biochem Biophys 367:146–150

    Article  PubMed  CAS  Google Scholar 

  45. Aoki T, Akashi T, Ayabe S (2000) Flavonoids of leguminous plants: structure, biological activity, and biosynthesis. J Plant Res 113:475–488

    Article  Google Scholar 

  46. Cheng NH, Hirschi KD (2003) Cloning and characterization of CXIP1, a novel PICOT domain containing Arabidopsis protein that associates with CAX1. J Biol Chem 278:6503–6509

    Article  PubMed  CAS  Google Scholar 

  47. Munns R (2005) Genes and salt tolerance: bringing them together. New Phytol 167:645–663

    Article  PubMed  CAS  Google Scholar 

  48. Fry SC, Smith RC, Renwick KF, Martin DJ, Hodge SK, Matthews KJ (1992) Xyloglucan endotransglycosylase, a new wall-loosening enzyme activity from plants. Biochem J 282:821–828

    PubMed  CAS  Google Scholar 

  49. Eklof JM, Brumer H (2010) The XTH gene family: an update on enzyme structure, function, and phylogeny in xyloglucan remodeling. Plant Physiol 153:456–466

    Article  PubMed  Google Scholar 

  50. Hunter T (1995) Protein kinases and phosphatases: the yin and yang of protein phosphorylation and signaling. Cell 80:225–236

    Article  PubMed  CAS  Google Scholar 

  51. Pandey SP, Somssich IE (2009) The role of WRKY transcription factors in plant immunity. Plant Physiol 150:1648–1655

    Article  PubMed  CAS  Google Scholar 

  52. Shimada Y, Wu GJ, Watanabe A (1998) A protein encoded by din1, a dark-inducible and senescence-associated gene of radish, can be imported by isolated chloroplasts and has sequence similarity to sulfide dehydrogenase and other small stress proteins. Plant Cell Physiol 39:139–143

    PubMed  CAS  Google Scholar 

  53. He YH, Gan SS (2002) A gene encoding an acyl hydrolase is involved in leaf senescence in Arabidopsis. Plant Cell 14:805–815

    Article  PubMed  CAS  Google Scholar 

  54. Quirino BF, Normanly J, Amasino RM (1999) Diverse range of gene activity during Arabidopsis thaliana leaf senescence includes pathogen-independent induction of defense-related genes. Plant Mol Biol 40:267–278

    Article  PubMed  CAS  Google Scholar 

  55. Buchanan-Wollaston V, Ainsworth C (1997) Leaf senescence in Brassica napus: cloning of senescence related genes by subtractive hybridization. Plant Mol Biol 33:821–834

    Article  PubMed  CAS  Google Scholar 

  56. Quirino BF, Noh YS, Himelblau E, Amasino RM (2000) Molecular aspects of leaf senescence. Trends Plant Sci 5:278–282

    Article  PubMed  CAS  Google Scholar 

  57. Jiang H, Song W, Li A, Yang X, Sun D (2011) Identification of genes differentially expressed in cauliflower associated with resistance to Xanthomonas campestris pv. Campestris. Mol Biol Rep 38:621–629

    Article  PubMed  CAS  Google Scholar 

  58. Kufryk G, Hernandez-Prieto MA, Kieselbach T, Miranda H, Vermaas W, Funk C (2008) Association of small CAB-like proteins (SCPs) of Synechocystis sp. PCC 6803 with Photosystem II. Photosynth Res 95:135–145

    Article  PubMed  CAS  Google Scholar 

  59. Hecht V, Knowles CL, Schoor JKV, Liew LC, Jones SE, Lambert MJM, Weller JL (2007) Pea LATE BLOOMER1 is a GIGANTEA ortholog with roles in photoperiodic flowering, deetiolation, and transcriptional regulation of circadian clock gene homologs. Plant Physiol 144:648–661

    Article  PubMed  CAS  Google Scholar 

  60. Mahalingam R, Gomez-Buitrago A, Eckardt N, Shah N, Guevara-Garcia A, Day P, Raina R, Fedoroff NV (2003) Characterizing the stress/defense transcriptome of Arabidopsis. Genome Biol 4:R20

    Article  PubMed  Google Scholar 

  61. Jantasuriyarat C, Gowda M, Haller K, Hatfield J, Lu G, Stahlberg E, Zhou B, Li H, Kim H, Yu Y, Dean RA, Wing RA, Soderlund C, Wang GL (2005) Large-scale identification of expressed sequence tags involved in rice and rice blast fungus interaction. Plant Physiol 138:105–115

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the research grant provided by Department of Biotechnology, Government of India and National Institute of Plant Genome Research, New Delhi. Authors acknowledge Dr. Birendra Singh (Indian Agricultural Research Institute) and Mr. Ashok Kumar (National Institute of Plant Genome Research) for technical help.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Praveen Kumar Verma.

Additional information

Jyothi Reddy Cheruku, Kamal Kumar, Saurabh Yadav and Archana Singh have equally contributed in this work.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Table S1 List of primer sequences used for quantitative real time PCR (DOC 134 kb)

11033_2011_1255_MOESM2_ESM.doc

Table S2 Functional annotation of the unigenes from SSH library. The cDNA sequences of all unigenes obtained in 24 h and 3 h SSH libraries were submitted to the GenBank database and the assigned Accession no. was mentioned. BlastX searches were conducted to determine homologous genes and the putative function. BlastN was performed for cDNAs which did not show any significant homology in BlastX. GenBank Accession no. marked with (*) are cDNAs that showed significant homology in BlastN (e-value cutoff ≥ 1e-10) instead of BlastX (e-value cutoff ≥ 1e-5) (DOC 265 kb)

Table S3 Macroarray analysis of genes differentially expressed during Ascochyta infection (DOC 126 kb)

Table S4 Expression ratios of selected genes estimated by quantitative real-time PCR (DOC 247 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Jaiswal, P., Cheruku, J.R., Kumar, K. et al. Differential transcript accumulation in chickpea during early phases of compatible interaction with a necrotrophic fungus Ascochyta rabiei . Mol Biol Rep 39, 4635–4646 (2012). https://doi.org/10.1007/s11033-011-1255-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11033-011-1255-7

Keywords

Navigation