Skip to main content

Genome-wide characterization and expression profiling of TIFY gene family in pigeonpea (Cajanus cajan (L.) Millsp.) under copper stress

Abstract

Copper is a vital micronutrient for plant growth and development, but in high concentration it leads to the oxidative damage thereby initiating biosynthesis of jasmonic acid (JA). The JA signalling is mediated by various transcription factors (TFs) such as JAZ and MYC2. JAZ TFs are the negative regulators of JA signalling which are degraded in presence of JA. JAZ proteins belong to TIFY family and regulate various biological processes such as plant development, response to phytohormones, biotic and abiotic stresses. In the present study, we identified 18 TIFY family proteins in pigeonpea, which are further classified into TIFY, JAZ and ZML subfamilies. Gene expression of 12 CcTIFY genes in pigeonpea was studied under methyl jasmonate (Me-JA), JA in presence and absence of copper (Cu). Our results showed that the transcript levels of CcTIFY3, CcTIFY4, CcTIFY5, CcTIFY9 and CcTIFY16 were upregulated under Cu stress, indicating their involvement in Cu stress signalling. The presence of defense and stress responsive cis-regulatory elements in the promoter regions of these genes further confirms their involvement in response to Cu stress. Apart from feedback regulation of JAZ proteins, the expression of CcTIFY3 and CcTIFY9 was observed to be upregulated in Me-JA and JA treatment, respectively, which suggest involvement of alternative JA and Me-JA signalling.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3

Abbreviations

JA:

Jasmonic Acid

Me-JA:

Methyl jasmonate

qRT-PCR:

Quantitative real-time polymerase chain reaction

References

  • Acosta IF, Farmer EE (2010) Jasmonates. In The Arabidopsis Book: the American Society of Plant Biologists http://www.bioone.org/doi/full/10.1199/tab.0129. Accessed 10 August 2014

  • Aparicio-fabre R, Guillen G, Loredo M, Arellano J, Valdes-lopez O, Ramirez M, Iniguez LP, Panzeri D, et al. (2013) Common bean (Phaseolus vulgaris L.) PvTIFY orchestrates global changes in transcript profile response to jasmonate and phosphorus deficiency. BMC Plant Biol 13:1–22

    Article  Google Scholar 

  • Bai Y, Meng Y, Huang D, Qi Y, Chen M (2011) Genomics origin and evolutionary analysis of the plant-specific TIFY transcription factor family. Genomics 98:128–136

    CAS  Article  PubMed  Google Scholar 

  • Chahal V, Chand P, Nagpal A, Katnoria JA, Pakade YB (2014) Evaluation of heavy metal contamination and its genotoxicity in agricultural soil of Amritsar, Punjab India. Int J Chem Environ 4:20–28

    Google Scholar 

  • Cheng Z, Sun L, Qi T, Zhang B, Peng W, Liu Y, Xie D (2011) The bHLH transcription factor MYC3 interacts with the jasmonate ZIM-domain proteins to mediate jasmonate response in Arabidopsis. Mol Plant 4:279–288

    CAS  Article  PubMed  Google Scholar 

  • Chini A, Fonseca S, Fernandez G, Adie B, Chico JM, Lorenzo O, Garcia-Casado G, Lopez-Vidriero I, et al. (2007) The JAZ family of repressors is the missing link in jasmonate signalling. Nature 448:666–671

    CAS  Article  PubMed  Google Scholar 

  • Chini A, Fonseca S, Chico JM, Fernandez-Calvo P, Solano R (2009) The ZIM domain mediates homo- and heteromeric interactions between Arabidopsis JAZ proteins. Plant J 59:77–87

    CAS  Article  PubMed  Google Scholar 

  • Chung HS, Howe GA (2009) A critical role for the TIFY motif in repression of jasmonate signaling by a stabilized splice variant of the JASMONATE ZIM- domain protein JAZ10 in Arabidopsis. Plant Cell 21:131–145

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Jiang YQ, Deyholos MK (2006) Comprehensive transcriptional profiling of NaCl-stressed Arabidopsis roots reveals novel classes of responsive genes. BMC Plant Biol 6:25

    Article  PubMed  PubMed Central  Google Scholar 

  • Maksymiec W, Krupa Z (2002) The in vivo and in vitro influence of methyl jasmonate on oxidative processes in Arabidopsis thaliana leaves. Acta Physiol Plant 24:351–357

    CAS  Article  Google Scholar 

  • Maksymiec W, Wianowska D, Dawidowicz AL, Mardarowicz M, Krupa Z (2005) The level of jasmonic acid in Arabidopsis thaliana and Phaseolus coccineus plants under heavy metal stress. J Plant Physiol 162:1338–1346

    CAS  Article  PubMed  Google Scholar 

  • Nishii A, Takemura M, Fujita H, Shikata M, Yokota A, Kohchi T (2000) Characterization of a novel gene encoding a putative single zinc finger protein, ZIM, expressed during the reproductive phase in Arabidopsis thaliana. Biosci Biotechnol Biochem 64:1402–1409

    CAS  Article  PubMed  Google Scholar 

  • Poonam S, Kaur H, Geetika S (2013) Effect of jasmonic acid on photosynthetic pigments and stress markers in Cajanus cajan (L.) millsp. Seedlings under copper stress. Amer J Plant Sci 4:817–823

    Article  Google Scholar 

  • Ritter A, Goulitquer S, Salaün JP, Tonon T, Correa JA, Potin P (2008) Copper stress induces biosynthesis of octadecanoid and eicosanoid oxygenated derivatives in the brown algal kelp Laminaria digitata. New Phytol 180:809–821

    CAS  Article  PubMed  Google Scholar 

  • Roy BK, Prasad R, Gunjan (2010) Heavy metal accumulation and changes in metabolic parameters in Cajanus cajan grown in mine spoil. J Environ Biol 31:567–573

    CAS  PubMed  Google Scholar 

  • Shikata M, Matsuda Y, Ando K, Nishii A, Takemura M, Yokota A, Kohchi T (2004) Characterization of Arabidopsis ZIM, a member of a novel plant-specific GATA factor gene family. J Exp Bot 55:631–639

    CAS  Article  PubMed  Google Scholar 

  • Singh AK, Sharma V, Pal AK, Acharya V, Ahuja PS (2013) Genome-wide organization and expression profiling of the NAC transcription factor family in potato (Solanum tuberosum L.). DNA Res 20:403–423

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Singh NK, Gupta DK, Jayaswal PK, Mahato AK, Dutta S, Singh S, Bhutani S, Dogra V, et al. (2012) The first draft of the pigeonpea genome sequence. J Plant Biochem Biotechnol 21:98–112

    Article  PubMed  Google Scholar 

  • Staswick PE (2008) JAZing up jasmonate signaling. Trends Plant Sci 13:66–71

    CAS  Article  PubMed  Google Scholar 

  • Strayer C, Oyama T, Schultz TF, Raman R, Somers DE, Mas P, Panda S, Kreps JA, et al. (2000) Cloning of the Arabidopsis clock gene TOC1, an autoregulatory response egulator homolog. Science 289:768–771

    CAS  Article  PubMed  Google Scholar 

  • Sun J, Xu Y, Ye S, Jiang H, Chen Q, Liu F, Zhou W, Chen R, et al. (2009) Arabidopsis ASA1 is important for jasmonate-mediated regulation of auxin biosynthesis and transport during lateral root formation. Plant Cell 218:1495–1511

    Article  Google Scholar 

  • Theis T, Freyre RH, Kennard WC (1957) Pellicularia filamentosa on Tephrosia vogelii and Cajanus indicus in Puerto Rico. FAO Plant Protection Bulletin 5:159–160

    Google Scholar 

  • Thines B, Katsir L, Melotto M, Niu Y, Mandaokar A, Liu G, Nomura K, He SY, et al. (2007) JAZ repressor proteins are targets of the SCFCOI1 complex during jasmonate signalling. Nature 448:661–665

    CAS  Article  PubMed  Google Scholar 

  • Vanholme B, Grunewald W, Bateman A, Kohchi T, Gheysen G (2007) The tify family previously known as ZIM. Trends Plant Sci 12:239–244

    CAS  Article  PubMed  Google Scholar 

  • Varshney RK, Chen W, Li Y, Bharti AK, Saxena RK, Schlueter JA, Donoghue MTA, Azam S, et al. (2012) Draft genome sequence of pigeonpea (Cajanus cajan), an orphan legume crop of resource-poor farmers. Nat Biotechnol 30:83–89

    CAS  Article  Google Scholar 

  • Wasternack C (2007) Jasmonates : an update on biosynthesis, signal transduction and action in plant stress response, growth and development. Ann Bot 100:681–697

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Ye H, Du H, Tang N, Li X, Xiong L (2009) Identification and expression profiling analysis of TIFY family genes involved in stress and phytohormone responses in rice. Plant Mol Biol 71:291–305

    CAS  Article  PubMed  Google Scholar 

  • Zhang Y, Gao M, Singer SD, Fei Z, Wang H, Wang X (2012) Genome-wide identification and analysis of the TIFY gene family in grape. PLoS One 7:1–13

    CAS  Google Scholar 

  • Zhang Z, Li X, Yu R, Han M, Wu Z (2015) Isolation, structural analysis, and expression characteristics of the maize TIFY gene family. Mol Gen Genomics. doi:10.1007/s00438-015-1042-6

    Google Scholar 

  • Zhu D, Bai X, Luo X, Chen Q, Cai H, Ji W, Zhu Y (2013) Identification of wild soybean (Glycine soja) TIFY family genes and their expression profiling analysis under bicarbonate stress. Plant Cell Rep 32:263–272

    CAS  Article  PubMed  Google Scholar 

Download references

Acknowledgments

GS acknowledges financial support from the Science and Engineering Research Board, Department of Science and Technology (DST), Government of India. Research in the laboratory of AKS and VA is supported by the grants of Council of Scientific and Industrial Research (CSIR). PS thanks the DST for financial support in the form of WOS-A project. PG thanks CSIR for providing fellowship. PA and GK thank University Grants Commission for providing fellowship. This manuscript represents CSIR-IHBT communication number 3854.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Anil Kumar Singh.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Electronic supplementary material

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Sirhindi, G., Sharma, P., Arya, P. et al. Genome-wide characterization and expression profiling of TIFY gene family in pigeonpea (Cajanus cajan (L.) Millsp.) under copper stress. J. Plant Biochem. Biotechnol. 25, 301–310 (2016). https://doi.org/10.1007/s13562-015-0342-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13562-015-0342-6

Keywords

  • CcTIFY
  • Cu stress
  • Jasmonate
  • JAZ
  • Pigeonpea
  • qRT-PCR