Skip to main content

Advertisement

Log in

Transcriptome wide identification, phylogenetic analysis, and expression profiling of zinc-finger transcription factors from Crocus sativus L.

  • Original Article
  • Published:
Molecular Genetics and Genomics Aims and scope Submit manuscript

Abstract

Crocus sativus belongs to Iridaceae family and is the only plant species which produces apocarotenoids like crocin, picrocrocin, and safranal in significant quantities. Besides their organoleptic properties, Crocus apocarotenoids have been found to possess remarkable pharmacological potential. Although apocarotenoid biosynthetic pathway has been worked out to a great degree, but the mechanism that regulates the tissue and developmental stage-specific production of Crocus apocarotenoids is not known. To identify the genes regulating apocarotenoid biosynthesis in Crocus, transcriptome wide identification of zinc-finger transcription factors was undertaken. 81 zinc-finger transcription factors were identified which grouped into eight subfamilies. C2H2, C3H, and AN20/AN1 were the major subfamilies with 29, 20, and 14 members, respectively. Expression profiling revealed CsSAP09 as a potential candidate for regulation of apocarotenoid biosynthesis. CsSAP09 was found to be highly expressed in stigma at anthesis stage corroborating with the accumulation pattern of apocarotenoids. CsSAP09 was nuclear localized and activated reporter gene transcription in yeast. It was highly induced in response to oxidative, salt and dehydration stresses, ABA and methyl jasmonate. Furthermore, upstream region of CsSAP09 was found to contain stress and light responsive elements. To our knowledge, this is the first report on the study of a gene family in C. sativus and may provide basic insights into the putative role of zinc finger genes. It may also serve as a valuable resource for functional characterization of these genes aimed towards unraveling their role in regulation of apocarotenoid biosynthesis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+
from $39.99 /Month
  • Starting from 10 chapters or articles per month
  • Access and download chapters and articles from more than 300k books and 2,500 journals
  • Cancel anytime
View plans

Buy Now

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
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

References

  • Agarwal P, Arora R, Ray S, Singh AK, Singh VP, Takatsuji H et al (2007) Genome-wide identification of C2H2 zinc-finger gene family in rice and their phylogeny and expression analysis. Plant Mol Biol 65:467–485

    Article  CAS  PubMed  Google Scholar 

  • Ahrazem O, Rubio-Moraga A, Nebauer SG, Molina RV, Gómez-Gómez L (2015) Saffron: its phytochemistry, developmental processes, and biotechnological prospects. J Agric Food Chem 63:8751–8764

    Article  CAS  PubMed  Google Scholar 

  • Ahrazem O, Rubio-Moraga A, Argandoña-Picazo J, Castillo R, Gómez-Gómez L (2016) Intron retention and rhythmic diel pattern regulation of carotenoid cleavage dioxygenase 2 during crocetin biosynthesis in saffron. Plant Mol Biol 91:355–374

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arnaud D, Dejardin A, Leple JC, Lesage Descauses M, Pilate G (2007) Genome-wide analysis of LIM gene family in Populus trichocarpa, Arabidopsis thaliana, and Oryza sativa. DNA Res 14:103–116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arora R, Agarwal P, Ray S, Singh AK, Singh VP, Tyagi AK et al (2007) MADS-box gene family in rice: genome-wide identification, organization and expression profiling during reproductive development and stress. BMC Genomics 8:242

    Article  PubMed  PubMed Central  Google Scholar 

  • Ashraf N, Jain D, Vishwakarma RA (2015) Identification, cloning and characterization of an ultrapetala transcription factor CsULT1 from Crocus: a novel regulator of apocarotenoid biosynthesis. BMC Plant Biol 15:25

    Article  PubMed  PubMed Central  Google Scholar 

  • Baba SA, Jain D, Abbas N, Ashraf N (2015a) Overexpression of Crocus carotenoid cleavage dioxygenase, CsCCD4b, in Arabidopsis imparts tolerance to dehydration, salt and oxidative stresses by modulating ROS machinery. J Plant Physiol 189:114–125

    Article  CAS  PubMed  Google Scholar 

  • Baba SA, Mohiuddin T, Basu S, Swarnkar MK, Malik AH, Wani ZA et al (2015b) Comprehensive transcriptome analysis of Crocus sativus for discovery and expression of genes involved in apocarotenoid biosynthesis. BMC Genomics 16:698

    Article  PubMed  PubMed Central  Google Scholar 

  • Brameier M, Krings A, MacCallum RM (2007) NucPred - Predicting nuclear localization of proteins. Bioinformatics 23:1159–1160

    Article  CAS  PubMed  Google Scholar 

  • Chezem WR, Clay NK (2016) Regulation of plant secondary metabolism and associated specialized cell development by MYBs and bHLHs. Phytochemistry 131:26–43

    Article  CAS  PubMed  Google Scholar 

  • Ciftci-Yilmaz S, Mittler R (2008) The zinc finger network of plants. CMLS 65;1150–1160.

    Article  CAS  PubMed  Google Scholar 

  • 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  CAS  PubMed  Google Scholar 

  • Dixit VM, Green S, Sarma V, Holzman LB, Wolf FW, O’Rourke K et al (1990) Tumor necrosis factor-alpha induction of novel gene products in human endothelial cells including a macrophage-specific chemotaxin. J Biol Chem 265:2973–2978

    CAS  PubMed  Google Scholar 

  • Fernández JA, Santana O, Guardiola JL, Molina RV, Heslop-Harrison P, Borbely G et al (2011) The World Saffron and Crocus collection: strategies for establishment, management, characterization and utilization. Genet Resour Crop E 58:125–137

    Article  Google Scholar 

  • Frusciante S, Diretto G, Bruno M, Ferrante P, Pietrella M, Prado-Cabrero A et al (2014) Novel carotenoid cleavage dioxygenase catalyzes the first dedicated step in saffron crocin biosynthesis. Proc Natl Acad Sci USA 111:12246–12251

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Giri J, Vij S, Dansana PK, Tyagi AK (2011) Rice A20/AN1 zinc-finger containing stress-associated proteins (SAP1/11) and a receptor-like cytoplasmic kinase (OsRLCK253) interact via A20 zinc-finger and confer abiotic stress tolerance in transgenic Arabidopsis plants. N Phytol 191:721–732

    Article  CAS  Google Scholar 

  • Giri J, Dansana PK, Kothari KS, Sharma G, Vij S, Tyagi AK (2013) SAPs as novel regulators of abiotic stress response in plants. Bioessays 35:639–648

    Article  CAS  PubMed  Google Scholar 

  • Gourcilleau D, Lenne C, Armenise C, Moulia B, Julien JL, Bronner G et al (2011) Phylogenetic study of plant Q-type C2H2 zinc finger proteins and expression analysis of poplar genes in response to osmotic, cold and mechanical stresses. DNA Res Int J Rapid Publ Rep Genes Genom 18:77–92

    CAS  Google Scholar 

  • Gu X (2004) Statistical framework for phylogenomic analysis of gene family expression profiles. Genetics 167:531–542

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gutheil WG, Reed G, Ray A, Anant S, Dhar A (2012) Crocetin: an agent derived from saffron for prevention and therapy for cancer. Curr Pharm Biotechnol 13:173–179

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hall TMT (2005) Multiple modes of RNA recognition by zinc finger proteins. Curr Opin Struct Biol 15:367–373

    Article  CAS  PubMed  Google Scholar 

  • Hishiya, Iemura S, Natsume T, Takayama S, Ikeda K, Watanabe K (2006) A novel ubiquitin-binding protein ZNF216 functioning in muscle atrophy. EMBO J 25:554–564

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Iuchi S (2001) Three classes of C2H2 zinc finger proteins. CMLS Cell Mol Life Sci 58:625–635

    Article  CAS  PubMed  Google Scholar 

  • Jain M, Srivastava PL, Verma M, Ghangal R, Garg R, Fernandez JA et al (2016) De novo transcriptome assembly and comprehensive expression profiling in Crocus sativus to gain insights into apocarotenoid biosynthesis. Sci Rep 6:22456

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaefer CM, Milner JA (2008) The role of herbs and spices in cancer prevention. J Nutr Biochem 19:347–361

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kanneganti V, Gupta AK (2008) Overexpression of OsiSAP8, a member of stress associated protein (SAP) gene family of rice confers tolerance to salt, drought and cold stress in transgenic tobacco and rice. Plant Mol Biol 66:445–462

    Article  CAS  PubMed  Google Scholar 

  • Kasuga M, Liu Q, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1999) Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor. Nat Biotechnol 17:287–291

    Article  CAS  PubMed  Google Scholar 

  • Kianbakht S, Mozaffari K (2009) Effects of saffron and its active constituents, crocin and safranal, on prevention of indomethacin induced gastric ulcers in diabetic and nondiabetic rats. J Med Plants 1:30–38

    Google Scholar 

  • Kim GD, Cho YH, Yoo SD (2015) Regulatory functions of evolutionarily conserved AN1/A20-like Zinc finger family proteins in Arabidopsis stress responses under high temperature. Biochem Biophys Res Commun 457:213–220

    Article  CAS  PubMed  Google Scholar 

  • Klug A, Schwabe JW (1995) Protein motifs 5. Zinc fingers. FASEB J 9:597–604

    CAS  PubMed  Google Scholar 

  • Kyriakoudi A, Ordoudi S, Roldán M, Medina MZ, Tsimidou (2015) Saffron, a functional spice. Austin J Nutri Food Sci 3:1059–1

  • Li WT, He M, Wang J, Wang YP (2013) Zinc finger protein (ZFP) in plants—a review. POJ 6:474–480

    CAS  Google Scholar 

  • Li MJ, Qiao Y, Li YQ, Shi ZL, Zhang N, Bi CL, Guo JK (2016) A R2R3-MYB transcription factor gene in common wheat (namely TaMYBsm1) involved in enhancement of drought tolerance in transgenic Arabidopsis. J Plant Res 129:1097–1107

    Article  CAS  PubMed  Google Scholar 

  • Liu J, Osbourn A, Ma P (2015) MYB transcription factors as regulators of phenylpropanoid metabolism in plants. Mol Plant. 8:689–708

    Article  CAS  PubMed  Google Scholar 

  • Lopresti AL, Drummond PD (2014) Saffron (Crocus sativus) for depression: a systematic review of clinical studies and examination of underlying antidepressant mechanisms of action. Hum Psychopharmacol Clin Exp 29:517–527

    Article  Google Scholar 

  • Luo M, Bilodeau P, Koltunow A, Dennis ES, Peacock WJ, Chaudhury AM (1999) Genes controlling fertilization-independent seed development in Arabidopsis thaliana. Proc Natl Acad Sci USA 96:296–301

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mir JI, Ahmed N, Wafai AH, Qadri RA (2012) Relative expression of CsZCD gene and apocarotenoid biosynthesis during stigma development in Crocus sativus L. Physiol Mol Biol Plants Int J Funct Plant Biol 18:371–375

    Article  CAS  Google Scholar 

  • Molnár G, Bancoş S, Nagy F, Szekeres M (2002) Characterisation of BRH1, a brassinosteroid-responsive RING-H2 gene from Arabidopsis thaliana. Planta 215:127–133

    Article  PubMed  Google Scholar 

  • Moshiri M, Vahabzadeh M, Hosseinzadeh H (2015) Clinical applications of saffron (Crocus sativus) and its constituents: a review. Drug Res 65:287–295.

    CAS  Google Scholar 

  • Mukhopadhyay A, Vij S, Tyagi AK (2004) Overexpression of a zinc-finger protein gene from rice confers tolerance to cold, dehydration, and salt stress in transgenic tobacco. Proc Natl Acad Sci USA 101:6309–6314

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nguyen BAN, Pogoutse A, Provart N, Moses AM (2009) NLStradamus: a simple Hidden Markov Model for nuclear localization signal prediction. BMC Bioinform 10:202

    Article  Google Scholar 

  • Paul A, Kumar S (2015) An A20/AN1-zinc-finger domain containing protein gene in tea is differentially expressed during winter dormancy and in response to abiotic stress and plant growth regulators. Plant Gene 1:1–7

    Article  CAS  Google Scholar 

  • Rakesh K, Virendra Singh V, Devi K, Sharma M, Singh MK, Ahuja PS (2009) State of art of saffron (Crocus sativus L.) agronomy: a comprehensive review. Food Rev Int 25:44–85

    Google Scholar 

  • Rubio-Moraga A, Trapero A, Ahrazem O, Gómez-Gómez L (2010) Crocin transport in Crocus sativus: the long road from a senescent stigma to a newborn corm. Phytochemistry 71:1506–1513

    Article  CAS  PubMed  Google Scholar 

  • Shirsat A, Wilford N, Croy R, Boulter D (1989) Sequences responsible for the tissue specific promoter activity of a pea legumin gene in tobacco. Mol Gen Genet 215:326–331

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.06. Mol Biol Evol 30:2725–2729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tian ZD, Zhang Y, Liu J, Xie CH (2010) Novel potato C2H2-type zinc finger protein gene, StZFP1, which responds to biotic and abiotic stress, plays a role in salt tolerance. Plant Biol (Stuttgart, Germany) 12:689–697

    Article  CAS  Google Scholar 

  • Tjaden G, Edwards JW, Coruzzi GM (1995) cis elements and trans-acting factors affecting regulation of a nonphotosynthetic light-regulated gene for chloroplast glutamine synthetase. Plant Physiol 108:1109–1117

  • Urao T, Yamaguchi-Shinozaki K, Urao S, Shinozaki K (1993) An Arabidopsis myb homolog is induced by dehydration stress and its gene product binds to the conserved MYB recognition sequence. Plant Cell 5:1529–1539

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vij S, Tyagi AK (2006) Genome-wide analysis of the stress associated protein (SAP) gene family containing A20/AN1 zinc-finger(s) in rice and their phylogenetic relationship with Arabidopsis. MGG 276;565–575

    Article  CAS  PubMed  Google Scholar 

  • Wang D, Guo Y, Wu C, Yang G, Li Y, Zheng C (2008) Genome-wide analysis of CCCH zinc finger family in Arabidopsis and rice. BMC Genom 9:44

    Article  Google Scholar 

  • Wani SH, Kumar V (2015) Plant Stress Tolerance: Engineering ABA: A Potent Phytohormone. Transcriptomics 3:113

  • Yang L, Liu Z, Lu F, Dong A, Huang H (2006) SERRATE is a novel nuclear regulator in primary microRNA processing in Arabidopsis. Plant J Cell Mol Biol 47:841–850

    Article  CAS  Google Scholar 

  • Yun JY, Weigel D, Lee I (2002) Ectopic expression of SUPERMAN suppresses development of petals and stamens. Plant Cell Physiol 43:52–57

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Jin JP, Tang L, Zhao Y, Gu XC, Gao G, Luo JC (2011) PlantTFDB 2.0: update and improvement of the comprehensive plant transcription factor database. Nucleic Acids Res 39:1114–1117

    Article  Google Scholar 

  • Zhang C, Zhang H, Zhao Y, Jiang H, Zhu S, Cheng B, Xiang Y (2013) Genome-wide analysis of the CCCH zinc finger gene family in Medicago truncatula. Plant Cell Rep 32:1543–1555

    Article  CAS  PubMed  Google Scholar 

  • Zheng S, Qian Z, Sheng L, Wen N (2006) Crocetin attenuates atherosclerosis in hyperlipidemic rabbits through inhibition of LDL oxidation. J Cardiovasc Pharmacol 47:70–76

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The work was supported by grant from SERB, Govt. of India. AHM acknowledges fellowship from CSIR India. We further acknowledge Dr. Nazia Abbas for careful reading of manuscript. The manuscript bears institutional manuscript Number IIIM/1994/2017.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Nasheeman Ashraf.

Ethics declarations

Conflict of interest

Authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies performed with animals by any of the authors.

Additional information

Communicated by S. Hohmann.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 26 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Malik, A.H., Ashraf, N. Transcriptome wide identification, phylogenetic analysis, and expression profiling of zinc-finger transcription factors from Crocus sativus L.. Mol Genet Genomics 292, 619–633 (2017). https://doi.org/10.1007/s00438-017-1295-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00438-017-1295-3

Keywords