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In silico identification and expression analysis of Rare Cold Inducible 2 (RCI2) gene family in cucumber

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Abstract

Rare Cold Inducible 2 (RCI2), also known as plasma membrane protein 3, is a group of low molecular weight proteins that play crucial roles in plant growth and development as well as environmental stress responses. In this work, we performed a comprehensive analysis of the RCI2 gene family and identified 4 RCI2 genes (CsaRCI2A–D) from cucumber (Cucumis sativus L.), which were distributed in four chromosomes of the cucumber genome. The amino acid identities among the 4 CsaRCI2 proteins varied from 46.55 to 76.00%. Phylogenetic analysis showed that RCI2 proteins from cucumber, Arabidopsis, Medicago truncatula, maize and rice could be classified into four distinct clades, and nearly all the RCI2 genes harbored two exons separated by an intron of variable size. Many development-, stress-, and hormone-related cis-elements were found in the promoter regions of the CsaRCI2 genes, and the CsaRCI2 genes seemed to have tissue-specific expression patterns. In addition, qRT-PCR analysis revealed that these four CsaRCI2 genes were all responsive to various abiotic stresses including cold, salt, and drought, as well as ABA treatment. Our findings lay a foundation for further elucidating the biological roles of the RCI2 gene family in cucumber.

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Abbreviations

RCI2:

Rare Cold Inducible 2

Pmp3:

Plasma membrane protein 3

Lti:

Low temperature induced

MW:

Molecular weight

CDS:

Coding sequence

gDNA:

Genomic DNA

qRT-PCR:

Quantitative real-time PCR

References

  • Anderson SL, Teakle GR, Martino-Catt SJ, Kay SA (1994) Circadian clock- and phytochrome-regulated transcription is conferred by a 78 bp cis-acting domain of the Arabidopsis CAB2 promoter. Plant J 6:457–470

    CAS  PubMed  Google Scholar 

  • Bai L, Liu Y, Mu Y, Anwar A, He C, Yan Y et al (2018) Heterotrimeric G-protein γ subunit CsGG3.2 positively regulates the expression of CBF genes and chilling tolerance in cucumber. Front Plant Sci 9:488

    PubMed  PubMed Central  Google Scholar 

  • Ben Romdhane W, Ben-Saad R, Meynard D, Verdeil JL, Azaza J, Zouari N et al (2017) Ectopic expression of Aeluropus littoralis plasma membrane protein gene AlTMP1 confers abiotic stress tolerance in transgenic tobacco by improving water status and cation homeostasis. Int J Mol Sci 18:692

    PubMed Central  Google Scholar 

  • Ben-Romdhane W, Ben-Saad R, Meynard D, Zouari N, Mahjoub A, Fki L et al (2018) Overexpression of AlTMP2 gene from the halophyte grass Aeluropus littoralis in transgenic tobacco enhances tolerance to different abiotic stresses by improving membrane stability and deregulating some stress-related genes. Protoplasma 255:1161–1177

    CAS  PubMed  Google Scholar 

  • Biłas R, Szafran K, Hnatuszko-Konka K, Kononowicz AK (2016) Cis-regulatory elements used to control gene expression in plants. Plant Cell Tissue Organ Cult 127:269–287

    Google Scholar 

  • Blumwald E (2000) Sodium transport and salt tolerance in plants. Curr Opin Cell Biol 12:431–434

    CAS  PubMed  Google Scholar 

  • Chidambaram R, Venkataraman G, Parida A (2015) Analysis of transcriptional regulation and tissue-specific expression of Avicennia marina Plasma Membrane Protein 3 suggests it contributes to Na+ transport and homoeostasis in A. marina. Plant Sci 236:89–102

    CAS  PubMed  Google Scholar 

  • Eddy SR (2011) Accelerated profile HMM searches. PLoS Comput Biol 7:e1002195

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fu J, Zhang DF, Liu YH, Ying S, Shi YS, Song YC et al (2012) Isolation and characterization of maize PMP3 genes involved in salt stress tolerance. PLoS ONE 7:e31101

    CAS  PubMed  PubMed Central  Google Scholar 

  • Goldsbrough AP, Albrecht H, Stratford R (1993) Salicylic acid-inducible binding of a tobacco nuclear protein to a 10 bp sequence which is highly conserved amongst stress-inducible genes. Plant J 3:563–571

    CAS  PubMed  Google Scholar 

  • Inada M, Ueda A, Shi W, Takabe T (2005) A stress-inducible plasma membrane protein 3 (AcPMP3) in a monocotyledonous halophyte, Aneurolepidium chinense, regulates cellular Na+ and K+ accumulation under salt stress. Planta 220:395–402

    CAS  PubMed  Google Scholar 

  • Kayum MA, Park JI, Nath UK, Biswas MK, Kim HT, Nou IS (2017) Genome-wide expression profiling of aquaporin genes confer responses to abiotic and biotic stresses in Brassica rapa. BMC Plant Biol 17:23

    PubMed  PubMed Central  Google Scholar 

  • Khurana N, Chauhan H, Khurana P (2015) Characterization of a chloroplast localized wheat membrane protein (TaRCI) and its role in heat, drought and salinity stress tolerance in Arabidopsis thaliana. Plant Gene 4:45–54

    CAS  Google Scholar 

  • Kim SH, Kim JY, Kim SJ, An KS, An G, Kim SR (2007) Isolation of cold stress-responsive genes in the reproductive organs, and characterization of the OsLti6b gene from rice (Oryza sativa L.). Plant Cell Rep 26:1097–1110

    CAS  PubMed  Google Scholar 

  • Kim HS, Lee JE, Jang HY, Kwak KJ, Ahn SJ (2016) CsRCI2A and CsRCI2E genes show opposite salt sensitivity reaction due to membrane potential control. Acta Physiol Plant 38:50

    Google Scholar 

  • Kong X, Lv W, Jiang S, Zhang D, Cai G, Pan J et al (2013) Genome-wide identification and expression analysis of calcium-dependent protein kinase in maize. BMC Genom 14:433

    CAS  Google Scholar 

  • Kumari K, Jegadeeson V, Suji S, Venkataraman G, Parida A (2017) T-homoeolog specific plasma membrane protein 3 [Nt(t)PMP3-2] in polyploid Nicotiana tabacum shows conserved alternative splicing, derived from extant Nicotiana tomentosiformis parent. Plant Physiol Biochem 119:338–345

    CAS  PubMed  Google Scholar 

  • Lescot M, Dehais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y et al (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30:325–327

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li Z, Zhang Z, Yan P, Huang S, Fei Z, Lin K (2011) RNA-Seq improves annotation of protein-coding genes in the cucumber genome. BMC Genom 12:540

    CAS  Google Scholar 

  • Li L, Li N, Song SF, Li YX, Xia XJ, Fu XQ et al (2014) Cloning and characterization of the drought-resistance OsRCI2-5 gene in rice (Oryza sativa L.). Genet Mol Res 13:4022–4035

    CAS  PubMed  Google Scholar 

  • Liu B, Feng D, Zhang B, Mu P, Zhang Y, He Y et al (2012) Musa paradisica RCI complements AtRCI and confers Na+ tolerance and K+ sensitivity in Arabidopsis. Plant Sci 184:102–111

    CAS  PubMed  Google Scholar 

  • Liu H, Wu M, Zhu D, Pan F, Wang Y, Xiang Y (2017) Genome-Wide analysis of the AAAP gene family in moso bamboo (Phyllostachys edulis). BMC Plant Biol 17:29

    PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Long R, Zhang F, Li Z, Li M, Cong L, Kang J et al (2015) Isolation and functional characterization of salt-stress induced RCI2-like genes from Medicago sativa and Medicago truncatula. J Plant Res 128:697–707

    CAS  PubMed  Google Scholar 

  • Medina J, Catala R, Salinas J (2001) Developmental and stress regulation of RCI2A and RCI2B, two cold-inducible genes of Arabidopsis encoding highly conserved hydrophobic proteins. Plant Physiol 125:1655–1666

    CAS  PubMed  PubMed Central  Google Scholar 

  • Medina J, Ballesteros ML, Salinas J (2007) Phylogenetic and functional analysis of Arabidopsis RCI2 genes. J Exp Bot 58:4333–4346

    CAS  PubMed  Google Scholar 

  • Mitsuya S, Taniguchi M, Miyake H, Takabe T (2005) Disruption of RCI2A leads to over-accumulation of Na+ and increased salt sensitivity in Arabidopsis thaliana plants. Planta 222:1001–1009

    CAS  PubMed  Google Scholar 

  • Mitsuya S, Taniguchi M, Miyake H, Takabe T (2006) Overexpression of RCI2A decreases Na+ uptake and mitigates salinity-induced damages in Arabidopsis thaliana plants. Physiol Plant 128:95–102

    CAS  Google Scholar 

  • Morsy MR, Almutairi AM, Gibbons J, Yun SJ, de los Reyes BG (2005) The OsLti6 genes encoding low-molecular-weight membrane proteins are differentially expressed in rice cultivars with contrasting sensitivity to low temperature. Gene 344:171–180

    CAS  PubMed  Google Scholar 

  • Narusaka Y, Nakashima K, Shinwari ZK, Sakuma Y, Furihata T, Abe H et al (2003) Interaction between two cis-acting elements, ABRE and DRE, in ABA-dependent expression of Arabidopsis rd29A gene in response to dehydration and high-salinity stresses. Plant J 34:137–148

    CAS  PubMed  Google Scholar 

  • Navarre C, Goffeau A (2000) Membrane hyperpolarization and salt sensitivity induced by deletion of PMP3, a highly conserved small protein of yeast plasma membrane. EMBO J 19:2515–2524

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nejad ES, Askari H, Soltani S (2012) Regulatory TGACG-motif may elicit the secondary metabolite production through inhibition of active cyclin-dependent kinase/cyclin complex. Plant Omics 5:553–558

    CAS  Google Scholar 

  • Nylander M, Heino P, Helenius E, Palva ET, Ronne H, Welin BV (2001) The low-temperature- and salt-induced RCI2A gene of Arabidopsis complements the sodium sensitivity caused by a deletion of the homologous yeast gene SNA1. Plant Mol Biol 45:341–352

    CAS  PubMed  Google Scholar 

  • Pokrzywa W, Guerriat B, Dodzian J, Morsomme P (2009) Dual Sorting of the Saccharomyces cerevisiae vacuolar protein Sna4p. Eukaryot Cell 8:278–286

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rocha PSCF (2016) Plant abiotic stress-related RCI2/PMP3s: multigenes for multiple roles. Planta 243:1–12

    CAS  PubMed  Google Scholar 

  • Shen Q, Ho TH (1995) Functional dissection of an abscisic acid (ABA)-inducible gene reveals two independent ABA-responsive complexes each containing a G-box and a novel cis-acting element. Plant Cell 7:295–307

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li W et al (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 7:539

    PubMed  PubMed Central  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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Vishwakarma K, Upadhyay N, Kumar N, Yadav G, Singh J, Mishra RK et al (2017) Abscisic acid signaling and abiotic stress tolerance in plants: a review on current knowledge and future prospects. Front Plant Sci 8:161

    PubMed  PubMed Central  Google Scholar 

  • Wang DH, Chen YQ, Wang Y, Wang ZZ (2013) Molecular cloning and expression of two plasma membrane protein 3 (SmPMP3) genes from Salvia miltiorrhiza. Russ J Plant Physiol 60:155–164

    CAS  Google Scholar 

  • Yeshvekar RK, Nitnavare RB, Chakradhar T, Bhatnagar-Mathur P, Reddy MK, Reddy PS (2017) Molecular characterization and expression analysis of pearl millet plasma membrane proteolipid 3 (Pmp3) genes in response to abiotic stress conditions. Plant Gene 10:37–44

    CAS  Google Scholar 

  • Zhang CQ, Nishiuchi S, Liu S, Takano T (2008) Characterization of two plasma membrane protein 3 genes (PutPMP3) from the alkali grass, Puccinellia tenuiflora, and functional comparison of the rice homologues, OsLti6a/b from rice. BMB Rep 41:448–454

    Google Scholar 

  • Zhao Y, Tong H, Cai R, Peng X, Li X, Gan D et al (2014) Identification and characterization of the RCI2 gene family in maize (Zea mays). J Genet 93:655–666

    CAS  PubMed  Google Scholar 

  • Zhou Y, Hu L, Jiang L, Liu S (2018a) Genome-wide identification and expression analysis of YTH domain-containing RNA-binding protein family in cucumber (Cucumis sativus). Genes Genom 40:579–589

    CAS  Google Scholar 

  • Zhou Y, Hu L, Ye S, Jiang L, Liu S (2018b) Genome-wide identification and characterization of cysteine-rich polycomb-like protein (CPP) family genes in cucumber (Cucumis sativus) and their roles in stress responses. Biologia 73:425–435

    CAS  Google Scholar 

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Acknowledgements

This work was funded by the Key Project of Youth Science Foundation of Jiangxi Province (20171ACB21025), and the National Natural Science Foundation of China (31460522 and 31660578).

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Authors and Affiliations

  1. College of Science, Jiangxi Agricultural University, Nanchang Economic and Technological Development District, Nanchang, 330045, Jiangxi, China

    Yong Zhou, Guanghua Li & Shiqiang Liu

  2. Key Laboratory of Crop Physiology, Ecology and Genetic Breeding, Ministry of Education, Jiangxi Agricultural University, Nanchang, 330045, China

    Yong Zhou

  3. College of Agronomy, Jiangxi Agricultural University, Nanchang, 330045, China

    Lingli Ge, Peng He & Yingui Yang

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  1. Yong Zhou
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  3. Guanghua Li
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Correspondence to Shiqiang Liu.

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Zhou, Y., Ge, L., Li, G. et al. In silico identification and expression analysis of Rare Cold Inducible 2 (RCI2) gene family in cucumber. J. Plant Biochem. Biotechnol. 29, 56–66 (2020). https://doi.org/10.1007/s13562-019-00510-6

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