Skip to main content
SpringerLink
Log in

Genome-wide analysis of the Chinese cabbage IQD gene family and the response of BrIQD5 in drought resistance

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Key message

Thirty-five IQD genes were identified and analysed in Chinese cabbage and BrIQD5 transgenic plants enhanced the drought resistance of plants.

Abstract

The IQD (IQ67-domain) family plays an important role in various abiotic stress responses in plant species. However, the roles of IQD genes in the Chinese cabbage response to abiotic stress remain unclear. Here, 35 IQD genes, from BrIQD1 to BrIQD35, were identified in Chinese cabbage (Brassica rapa ssp. pekinensis). Based on the phylogenetic analysis, these genes were clustered into three subfamilies (I-III), and members within the same subfamilies shared conserved exon–intron distribution and motif composition. The 35 BrIQD genes were unevenly distributed on 9 of the 10 chromosomes with 4 segmental duplication events. Ka/Ks ratios showed that the duplicated BrIQDs had mainly experienced strong purifying selection. Quantitative real-time polymerase chain reaction of 35 BrIQDs under PEG6000 indicated that BrIQD5 was significantly induced by PEG6000. To verify BrIQD5 function, BrIQD5 was heterologously overexpressed in tobacco and was silenced in Chinese cabbage. BrIQD5-overexpressed plants showed more tolerance to drought stress than wild-type plants, while BrIQD5-silenced plants in Chinese cabbage showed decreased drought tolerance. Additionally, six BrIQD5 potential interactive proteins were isolated by the yeast two-hybrid assay, including BrCaMa, BrCaMb and four other stress-related proteins. Motif IQ1 of BrIQD5 is important for the interaction with BrCaMa and BrCaMb, and the isoleucine in motif IQ1 is an essential amino acid for calmodulin binding to BrIQD5. The identification and cloning of the new Chinese cabbage drought tolerance genes will promote the drought-resistant breeding of Chinese cabbage and help to better understand the mechanism of IQD involved in the drought tolerance of plants.

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
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

References

  • Abel S, Savchenko T, Levy M (2005) Genome-wide comparative analysis of the IQD gene families in Arabidopsis thaliana and Oryza sativa. BMC Evol Biol 5:72–84

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bähler M, Rhoads A (2002) Calmodulin signaling via the IQ motif. FEBS Lett 513(1):107–113

    Article  PubMed  Google Scholar 

  • Bailey TL, Elkan C (1995) The value of prior knowledge in discovering motifs with MEME. Proc Int Conf Sys Mol Biol 3:21–29

    CAS  Google Scholar 

  • Bao F, Du DL, An Y, Yang WR, Wang J, Cheng TR, Zhang QX (2017) Overexpression of prunus mume dehydrin genes in tobacco enhances tolerance to cold and drought. Front Plant Sci 8:151

    PubMed  PubMed Central  Google Scholar 

  • Bhattacharya S, Bunick CG, Chazin WJ (2004) Target selectivity in EF-hand calcium binding proteins. BBA-Mol Cell Res 1742(1):69–79

    CAS  Google Scholar 

  • Blanc G, Wolfe KH (2004) Widespread paleopolyploidy in model plant species inferred from age distributions of duplicate genes. Plant Cell 16:1667–1678

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bouché N, Yellin A, Snedden WA, Fromm H (2005) Plant-specific calmodulin-binding proteins. Annu Rev Plant Biol 56:435–466

    Article  PubMed  CAS  Google Scholar 

  • Bürstenbinder K, Savchenko T, Müller J, Adamson AW, Stamm G, Kwong R, Zipp BJ, Dinesh DC, Abel S (2013) Arabidopsis calmodulin-binding protein IQ67-domain 1 localizes to microtubules and interacts with kinesin light chain-related protein-1. J Biol Chem 288:1871–1882

    Article  PubMed  CAS  Google Scholar 

  • Cai R, Zhang C, Zhao Y, Zhu K, Wang Y, Jiang H, Xiang Y, Cheng B (2016) Genome-wide analysis of the IQD gene family in maize. Mol Genet Genomic 291:543–558

    Article  CAS  Google Scholar 

  • Chen CN, Chu CC, Zentella R, Pan SM, Ho THD (2002) Athva22 gene family in Arabidopsis: phylogenetic relationship, ABA and stress regulation, and tissue-specific expression. Plant Mol Biol 49:631–642

    Article  Google Scholar 

  • Choi JY et al (2002) Identification of calmodulin isoform-specific binding peptides from a phage-displayed random 22-mer peptide library. J Biol Chem 277(24):21630–21638

    Article  CAS  PubMed  Google Scholar 

  • Clapperton JA, Martin SR, Smerdon SJ, Gamblin SJ, Bayley PM (2002) Structure of the complex of calmodulin with the target sequence of calmodulin-dependent protein kinase I: studies of the kinase activation mechanism. Biochemistry 41(50):14669–14679

    Article  CAS  PubMed  Google Scholar 

  • Day IS, Reddy VS, Ali GS, Reddy A (2002) Analysis of EF-hand-containing proteins in Arabidopsis. Genome Bio 3(10):RESEARCH0056

    Article  Google Scholar 

  • Dodd AN, Kudla J, Sanders D (2010) The language of calcium signaling. Annu Rev Plant Bio 61:593–620

    Article  CAS  Google Scholar 

  • Emanuelsson O, Nielsen H, Brunak S, Heijne GV (2000) Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J Mol Biol 300:1005–1016

    Article  CAS  PubMed  Google Scholar 

  • Filiz E, Tombuloglu H, Ozyi̇gi̇t II (2013) Genome-wide analysis of IQ67 domain (IQD) gene families in Brachypodium distachyon. Plant Omics 6:425–432

    CAS  Google Scholar 

  • Fischer C, Kugler A, Hoth S, Dietrich P (2013) An IQ domain mediates the interaction with calmodulin in a plant cyclic nucleotide-gated channel. Plant Cell Physiol 54:573–584

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gornall J, Betts R, Burke E, Clark R, Camp J, Willett K, Wiltshire A (2010) Implications of climate change for agricultural productivity in the early twenty-first century. PhilosT R Soc B 365:2973–2989

    Article  Google Scholar 

  • Hoeflich KP, Ikura M (2002) Calmodulin in action: diversity in target recognition and activation mechanisms. Cell 108:739–742

    Article  CAS  PubMed  Google Scholar 

  • Huang GB, Zhang XH, Yang SL, Li JY, Xu CH, Rong ZY, Yang LY, Gong M (2012) Involvement of osmotic regulation in enhancement of drought resistance in tobacco (Nicotiana tabacum L.) plants through circular drought-hardening. J Plant Physiol 48:465–471

    Google Scholar 

  • Huang ZJ, Houten JV, Gonzalez G, Xiao H, Knaap EV (2013) Genome-wide identification, phylogeny and expression analysis of SUN, OFP and YABBY gene family in tomato. Mol Genet Genomics 288:111–129

    Article  CAS  PubMed  Google Scholar 

  • Irigoyen JJ, Einerich DW, Sánchez-Díaz M (1992) Water stress induced changes in concentrations of proline and total soluble sugars in nodulated alfalfa (Medicago sativd) plants. Physiol Plantarum 84:55–60

    Article  CAS  Google Scholar 

  • Koch MA, Haubold B, Mitchell-Olds T (2000) Comparative evolutionary analysis of chalcone synthase and alcohol dehydrogenase loci in Arabidopsis, Arabis, and related genera (Brassicaceae). Mol Biol Evol 17:1483–1498

    Article  CAS  PubMed  Google Scholar 

  • Letunic I, Doerks T, Bork P (2012) SMART 7: recent updates to the protein domain annotation resource. Nucleic Acids Res 40:302–305

    Article  CAS  Google Scholar 

  • Levy M, Wang Q, Kaspi R, Parrella MP, Abel S (2005) Arabidopsis IQD1, a novel calmodulin-binding nuclear protein, stimulates glucosinolate accumulation and plant defense. Plant J 43:79–96

    Article  CAS  PubMed  Google Scholar 

  • Li Z, Jiang HY, Zhou LY, Deng L, Lin YX, Peng XJ, Yan HW, Cheng BJ (2014) Molecular evolution of the HD-ZIP I gene family in legume genomes. Gene 533:218–228

    Article  CAS  PubMed  Google Scholar 

  • Li KQ, Xing CH, Yao ZH, Huang XS (2017) PbrMYB21, a novel MYB protein of Pyrus betulaefolia, functions in drought tolerance and modulates polyamine levels by regulating arginine decarboxylase gene. Plant Biotechnol J 15:1186–1203

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lim YP, Plaha P, Choi SR, Uhm T, Hong CP, Bang J, Hur YK (2006) Toward unraveling the structure of Brassica rapa genome. Physiol Plantarum 126:585–591

    Article  CAS  Google Scholar 

  • Lin F, Zhu C, Hui M, Xue C, Yuan L, Wang YY, Yan X (2014) The IQD gene family in soybean: structure, phylogeny, evolution and expression. PLoS ONE 9:e110896

    Article  CAS  Google Scholar 

  • Liu X, Liu S, Wu JL, Zhang BY, Li XY, Yan YC, Li L (2013) Overexpression of Arachis hypogaea NAC3 in tobacco enhances dehydration and drought tolerance by increasing superoxide scavenging. Plant Physiol Biochem 70(1):354–359

    Article  CAS  PubMed  Google Scholar 

  • Liu DQ, Han Q, Shah T, Chen CY, Wang Q, Tang BF, Ge F (2018) A hybrid proline-rich cell-wall protein gene JsPRP1, from Juglans sigillata Dode confers both biotic and abiotic stresses in transgenic tobacco plants. Trees 32(5):1–11

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Ma H, Feng L, Chen Z, Chen X, Zhao HL, Xiang Y (2014) Genome-wide identification and expression analysis of the IQD gene family in Populus trichocarpa. Plant Sci 229:96–110

    Article  CAS  PubMed  Google Scholar 

  • Maere S, De Bodt S, Raes J, Casneuf T, Van Montagu M, Kuiper M, Van de Peer Y (2005) Modeling gene and genome duplications in eukaryotes. Proc Natl Acad Sci 102:5454–5459

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410

    Article  CAS  PubMed  Google Scholar 

  • Moons A, Valcke R, Van Montagu M (2010) Low-oxygen stress and water deficit induce cytosolic pyruvate orthophosphate dikinase (PPDK) expression in roots of rice, a C3 plant. Plant J 15(1):89–98

    Article  Google Scholar 

  • Park JS, Yu JG, Park YD (2017) Characterization of a drought tolerance-related gene of Brassica rapa in a transgenic tobacco plant. Hortic Environ Biot 58:48–55

    Article  CAS  Google Scholar 

  • Park JS, Yu JG, Lee GH, Park YD (2018) Drought tolerance induction in transgenic tobacco through RNA interference of BrDST71, a drought-responsive gene from Chinese cabbage. Hortic Environ Biote 59(5):749–757

    Article  CAS  Google Scholar 

  • Peng S, Huang ZC, Ou YLJ, Cheng J, Zeng FH (2011) Research progress of artificial promoter in plant genetic engineering. Plant Physiol J 47(2):141–146 (in chinese)

    CAS  Google Scholar 

  • Perochon A, Aldon D, Galaud JP, Ranty B (2011) Calmodulin and calmodulin-like proteins in plant calcium signaling. Biochimie 93:2048–2053

    Article  CAS  PubMed  Google Scholar 

  • Puhakainen T, Hess MW, Mäkelä P, Svensson J, Heino P, Palva ET (2004) Overexpression of multiple dehydrin genes enhances tolerance to freezing stress in Arabidopsis. Plant Mol Biol 54:743–753

    Article  CAS  PubMed  Google Scholar 

  • Rochfort SJ, Imsic M, Jones R, Trenerry VC, Tomkins B (2006) Characterization of flavonol conjugates in immature leaves of pakchoi [Brassica rapa L. ssp. chinensis L. (Hanelt.)] by HPLC-DAD and LC-MS / MS. J Agric Food Chem 54:4855–4860

    Article  CAS  PubMed  Google Scholar 

  • Saeed AI, Bhagabati NK, Braisted JC, Liang W, Sharov V, Howe EA, Li J, Thiagarajan M, White JA, Quackenbush J (2006) TM4 microarray software suite. Method Enzymol 411(2):134–193

    Article  CAS  Google Scholar 

  • Shen Q, Chen CN, Brands A, Pan SM, Ho TH (2001) The stress- and abscisic acid-induced barley gene hva22: developmental regulation and homologues in diverse organisms. Plant Mol Biol 45:327–340

    Article  CAS  PubMed  Google Scholar 

  • Snedden WA, Fromm H (1998) Calmodulin, calmodulin-related proteins and plant responses to the environment. Trends Plant Sci 3:299–304

    Article  Google Scholar 

  • Snedden WA, Fromm H (2001) Calmodulin as a versatile calcium signal transducer in plants. New Phytol 151:35–66

    Article  CAS  PubMed  Google Scholar 

  • Stagge JH, Kohn I, Tallaksen LM, Stahl K (2015) Modeling drought impact occurrence based on meteorological drought indices in Europe. J Hydrol 530:37–50

    Article  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tian CG, Zhou YP (2014) Research progress in plant IQ motif-containing calmodulin-binding proteins. Chin Bull Bot 48:447–460

    Article  CAS  Google Scholar 

  • Wang LQ, Guo K, Li Y, Tu YY, Hu HZ, Wang BR, Cui XC, Peng LC (2010) Expression profiling and integrative analysis of the CESA/CSL superfamily in rice. BMC Plant Biol 10(1):282–297

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang X, Wang H, Wang J (2011) The genome of the mesopolyploid crop species Brassica rapa. Nat Genet 43:1035–1039

    Article  CAS  PubMed  Google Scholar 

  • Wu M, Li Y, Chen D, Liu H, Zhu D, Xiang Y (2016) Genome-wide identification and expression analysis of the IQD gene family in moso bamboo (Phyllostachys edulis). Sci Rep 6:24520

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xia XJ, Gao CJ, Song LX, Zhou YH, Shi K, Yu JQ (2014) Role of H2O2 dynamics in brassinosteroid-induced stomatal closure and opening in Solanum lycopersicum. Plant Cell Environ 37:2036–2050

    Article  CAS  PubMed  Google Scholar 

  • Xiao BZ, Chen X, Xiang CB, Tang N, Zhang QF, Xiong LZ (2009) Evaluation of seven function known candidate genes for their effects on improving drought resistance of transgenic rice under field conditions. Mol Plant 2:73–83

    Article  CAS  PubMed  Google Scholar 

  • Xiong L, Schumaker KS, Zhu JK (2002) Cell signaling during cold, drought, and salt stress. Plant Cell 14:165–183

    Article  CAS  Google Scholar 

  • Yu J, Yang XD, Wang Q, Gao LW, Yang Y, Xiao D, Liu TK, Li Y, Hou XL, Zhang CW (2018) Efficient virus-induced gene silencing in Brassica rapa, using a turnip yellow mosaic virus vector. Biol Plantarum 62(4):826–834

    Article  CAS  Google Scholar 

  • Yue YS, Zhang MC, Zhang JC, Duan LS, Li ZH (2011) Arabidopsis LOS5/ABA3, overexpression in transgenic tobacco (Nicotiana tabacum, cv. Xanthi-nc) results in enhanced drought tolerance. Plant Sci 181(4):405–411

    Article  CAS  PubMed  Google Scholar 

  • Zentella R, Zhang ZL, Park M (2007) Global analysis of DELLA direct targets in early gibberellin signaling in Arabidopsis. Plant Cell 19:3037–3057

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Z, Li J, Zhao XQ, Wang J, Wong GK, Yu J (2006) KaKs calculating Ka and Ks through model selection and model averaging. Genom Proteom Bioinf 4:259–263

    Article  CAS  Google Scholar 

  • Zhang L, Tian LH, Zhao JF, Song Y, Zhang CJ, Guo Y (2009) Identification of an apoplastic protein involved in the initial phase of salt stress response in rice root by two-dimensional electrophoresis. Plant Physiol 149:916–928

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou YH, Lam HM, Zhang JH (2007) Inhibition of photosynthesis and energy dissipation induced by water and high light stresses in rice. J Exp Bot 58:1207–1217

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Natural Science Foundation of China (Nos. 31471886 and 31872106) and National Vegetable Industry Technology System (CARS-23-A-06), Jiangsu Modern Agriculture (vegetable) Industrial Technology System (SXGC [2017] 273), and a project funded by the Priority Academic Program Development of Jiangsu Higher Education Institutions.

Author information

Authors and Affiliations

  1. State Key Laboratory of Crop Genetics and Germplasm Enhancement, Key Laboratory of Biology and Germplasm Enhancement of Horticultural Crops in East China, Ministry of Agriculture, College of Horticulture, Nanjing Agricultural University, Nanjing, 210095, China

    Jingping Yuan, Tongkun Liu, Zhanghong Yu, Yan Li, Haibo Ren, Xilin Hou & Ying Li

Authors
  1. Jingping Yuan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tongkun Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Zhanghong Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yan Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Haibo Ren
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Xilin Hou
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Ying Li
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

YL (Ying Li) and XLH conceived and designed the experiments. JPY, TKL and ZHY performed the experiments. YL (Yan Li) and HBR performed the qRTPCR. JPY wrote the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Ying Li.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 4146 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yuan, J., Liu, T., Yu, Z. et al. Genome-wide analysis of the Chinese cabbage IQD gene family and the response of BrIQD5 in drought resistance. Plant Mol Biol 99, 603–620 (2019). https://doi.org/10.1007/s11103-019-00839-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-019-00839-5

Keywords

Search

Navigation