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Target of tae-miR408, a chemocyanin-like protein gene (TaCLP1), plays positive roles in wheat response to high-salinity, heavy cupric stress and stripe rust

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Abstract

microRNAs (miRNAs) are novel and significant regulators of gene expression at the post-transcriptional level, and they are essential for normal growth and development and adaptation to stress conditions. As miRNAs are a kind of RNAs that do not code proteins, they play roles by repressing gene translation or degrading the corresponding target mRNAs. Plantacyanin-like (basic blue) proteins have been predicted and verified as the target gene of miR408 in wheat and Arabidopsis, respectively. Besides some biochemical characteristics, their detailed biological function remains unknown. In this study, the target gene of a wheat miRNA (tae-miR408), designated TaCLP1, was identified using degradome sequencing and co-transformation technology in tobacco leaves. We isolated the full-length cDNA clone, and defined its product as a chemocyanin-like protein, a kind of plantacyanin. Transcript accumulation of TaCLP1 and tae-miR408 showed contrasting divergent expression patterns in wheat response to Puccinia striiformis f. sp. tritici (Pst) and high copper ion stress. Overexpression of TaCLP1 in yeast (Schizosaccharomyces pombe) significantly increased cell growth under high salinity and Cu2+ stresses. Silencing of individual cDNA clones in wheat challenged with Pst indicated that TaCLP1 positively regulates resistance to stripe rust. The results indicate that the target of tae-miR408, TaCLP1, play an important role in regulating resistance of host plants to abiotic stresses and stripe rust, and such interactions can be a valuable resource for investigating stress tolerance in wheat.

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Abbreviations

BCP:

Blue copper protein

CYR:

Chinese yellow rust

dsRNA:

Double-strand RNA

hpi/t:

Hours post inoculation/treatment

HR:

Hypersensitive reaction

miRNAs:

microRNAs

pri-miRNA:

Primary miRNA transcripts

Pst :

Puccinia striiformis f. sp. tritici

qRT-PCR:

Quantitative real time PCR

RT-PCR:

Reverse transcription PCR

References

  • Adam H, Marguerettaz M, Qadri R, Adroher B, Richaud F, Collin M, Thuillet AC, Vigouroux Y, Laufs P, Tregear JW, Jouannic S (2011) Divergent expression patterns of miR164 and CUP-SHAPED COTYLEDON genes in palms and other monocots: implication for the evolution of meristem function in angiosperms. Mol Biol Evol 28(4):1439–1454

    Article  PubMed  CAS  Google Scholar 

  • Aukerman MJ, Sakai H (2003) Regulation of flowering time and floral organ identity by a microRNA and its APETALA2-like target genes. Plant Cell 15(11):2730–2741

    Article  PubMed  CAS  Google Scholar 

  • Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116(2):281–297

    Article  PubMed  CAS  Google Scholar 

  • Canters GW, Gilardi G (1993) Engineering type 1 copper sites in proteins. FEBS Lett 325(1–2):39–48

    Article  PubMed  CAS  Google Scholar 

  • De Rienzo F, Gabdoulline RR, Menziani MC, Wade RC (2000) Blue copper proteins: a comparative analysis of their molecular interaction properties. Protein Sci 9(8):1439–1454

    Article  PubMed  Google Scholar 

  • Dong J, Kim ST, Lord EM (2005) Plantacyanin plays a role in reproduction in Arabidopsis. Plant Physiol 138(2):778–789

    Article  PubMed  CAS  Google Scholar 

  • Ezaki B, Sivaguru M, Ezaki Y, Matsumoto H, Gardner RC (1999) Acquisition of aluminum tolerance in Saccharomyces cerevisiae by expression of the BCB or NtGDI1 gene derived from plants. FEMS Microbiol Lett 171(2):81–87

    Article  PubMed  CAS  Google Scholar 

  • Ezaki B, Gardner RC, Ezaki Y, Matsumoto H (2000) Expression of aluminum-induced genes in transgenic Arabidopsis plants can ameliorate aluminum stress and/or oxidative stress. Plant Physiol 122(3):657–666

    Article  PubMed  CAS  Google Scholar 

  • Ezaki B, Katsuhara M, Kawamura M, Matsumoto H (2001) Different mechanisms of four aluminum (Al)-resistant transgenes for Al toxicity in Arabidopsis. Plant Physiol 127(3):918–927

    Article  PubMed  CAS  Google Scholar 

  • Ezaki B, Sasaki K, Matsumoto H, Nakashima S (2005) Functions of two genes in aluminium (Al) stress resistance: repression of oxidative damage by the AtBCB gene and promotion of efflux of Al ions by the NtGDI1gene. J Exp Bot 56(420):2661–2671

    Article  PubMed  CAS  Google Scholar 

  • Feng H, Wang X, Sun Y, 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(6):3857–3866

    Article  PubMed  CAS  Google Scholar 

  • Feng H, Huang X, Zhang Q, Wei G, Wang X, Kang Z (2012) Selection of suitable inner reference genes for relative quantification expression of microRNA in wheat. Plant Physiol Biochem 51:116–122

    Article  PubMed  CAS  Google Scholar 

  • Hampton CR, Bowen HC, Broadley MR, Hammond JP, Mead A, Payne KA, Pritchard J, White PJ (2004) Cesium toxicity in Arabidopsis. Plant Physiol 136(3):3824–3837

    Article  PubMed  CAS  Google Scholar 

  • Hegedus D, Yu M, Baldwin D, Gruber M, Sharpe A, Parkin I, Whitwill S, Lydiate D (2003) Molecular characterization of Brassica napus NAC domain transcriptional activators induced in response to biotic and abiotic stress. Plant Mol Biol 53(3):383–397

    Article  PubMed  CAS  Google Scholar 

  • Hibino T, Lee BH, Takabe T (1995) Expression and characterization of Met92Gln mutant plastocyanin from Silene pratensis. J Biochem 117(1):101–106

    PubMed  CAS  Google Scholar 

  • Holzberg S, Brosio P, Gross C, Pogue GP (2002) Barley stripe mosaic virus-induced gene silencing in a monocot plant. Plant J 30(3):315–327

    Article  PubMed  CAS  Google Scholar 

  • Houde M, Diallo AO (2008) Identification of genes and pathways associated with aluminum stress and tolerance using transcriptome profiling of wheat near-isogenic lines. BMC Genomics 9(400):1471–2164

    Google Scholar 

  • Ikeda O, Sakurai T (1994) Electron transfer reaction of stellacyanin at a bare glassy carbon electrode. Eur J Biochem 219(3):813–819

    Article  PubMed  CAS  Google Scholar 

  • Jagadeeswaran G, Saini A, Sunkar R (2009) Biotic and abiotic stress down-regulate miR398 expression in Arabidopsis. Planta 229(4):1009–1014

    Article  PubMed  CAS  Google Scholar 

  • Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6(13):3901–3907

    PubMed  CAS  Google Scholar 

  • Jin H (2008) Endogenous small RNAs and antibacterial immunity in plants. FEBS Lett 582(18):2679–2684

    Article  PubMed  CAS  Google Scholar 

  • Katiyar-Agarwal S, Jin H (2010) Role of small RNAs in host-microbe interactions. Annu Rev Phytopathol 48:225–246

    Article  PubMed  CAS  Google Scholar 

  • Kim S, Mollet JC, Dong J, Zhang K, Park SY, Lord EM (2003) Chemocyanin, a small basic protein from the lily stigma, induces pollen tube chemotropism. Proc Natl Acad Sci USA 100(26):16125–16130

    Article  PubMed  CAS  Google Scholar 

  • Lamb CJ, Lawton MA, Dron M, Dixon RA (1989) Signals and transduction mechanisms for activation of plant defenses against microbial attack. Cell 56(2):215–224

    Article  PubMed  CAS  Google Scholar 

  • Llave C, Kasschau KD, Rector MA, Carrington JC (2002) Endogenous and silencing-associated small RNAs in plants. Plant Cell 14(7):1605–1619

    Article  PubMed  CAS  Google Scholar 

  • Ma H, Zhao H, Liu Z, Zhao J (2011) The phytocyanin gene family in rice (Oryza sativa L.): genome-wide identification, classification and transcriptional analysis. PLoS ONE 6(10):e25184

    Article  PubMed  CAS  Google Scholar 

  • Maunoury N, Vaucheret H (2011) AGO1 and AGO2 act redundantly in miR408-mediated Plantacyanin regulation. PLoS ONE 6(12):e28729

    Article  PubMed  CAS  Google Scholar 

  • Mengiste T, Chen X, Salmeron J, Dietrich R (2003) The BOTRYTIS SUSCEPTIBLE1 gene encodes an R2R3 MYB transcription factor protein that is required for biotic and abiotic stress responses in Arabidopsis. Plant Cell 15(11):2551–2565

    Article  PubMed  CAS  Google Scholar 

  • Miller JD, Arteca RN, Pell EJ (1999) Senescence-associated gene expression during ozone-induced leaf senescence in Arabidopsis. Plant Physiol 120(4):1015–1024

    Article  PubMed  CAS  Google Scholar 

  • Navarro L, Dunoyer P, Jay F, Arnold B, Dharmasiri N, Estelle M, Voinnet O, Jones JDG (2006) A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science 312(5772):436–439

    Article  PubMed  CAS  Google Scholar 

  • Nersissian AM, Immoos C, Hill MG, Hart PJ, Williams G, Herrmann RG, Valentine JS (1998) Uclacyanins, stellacyanins, and plantacyanins are distinct subfamilies of phytocyanins: plant-specific mononuclear blue copper proteins. Protein Sci 7(9):1915–1929

    Article  PubMed  CAS  Google Scholar 

  • Nikovics K, Blein T, Peaucelle A, Ishida T, Morin H, Aida M, Laufs P (2006) The balance between the MIR164A and CUC2 genes controls leaf margin serration in Arabidopsis. Plant Cell 18(11):2929–2945

    Article  PubMed  CAS  Google Scholar 

  • Padmanabhan C, Zhang X, Jin H (2009) Host small RNAs are big contributors to plant innate immunity. Curr Opin Plant Biol 12(4):465–472

    Article  PubMed  CAS  Google Scholar 

  • Palatnik JF, Allen E, Wu X, Schommer C, Schwab R, Carrington JC, Weigel D (2003) Control of leaf morphogenesis by microRNAs. Nature 425(6955):257–263

    Article  PubMed  CAS  Google Scholar 

  • Qin L, Kostic NM (1993) Importance of protein rearrangement in the electron-transfer reaction between the physiological partners cytochrome f and plastocyanin. Biochemistry 32(23):6073–6080

    Article  PubMed  CAS  Google Scholar 

  • Richards KD, Schott EJ, Sharma YK, Davis KR, Gardner RC (1998) Aluminum induces oxidative stress genes in Arabidopsis thaliana. Plant Physiol 116(1):409–418

    Article  PubMed  CAS  Google Scholar 

  • Ruan XM, Luo F, Li DD, Zhang J, Liu ZH, Xu WL, Huang GQ, Li XB (2011) Cotton BCP genes encoding putative blue copper-binding proteins are functionally expressed in fiber development and involved in response to high-salinity and heavy metal stresses. Physiol Plant 141(1):71–83

    Article  PubMed  CAS  Google Scholar 

  • Rubio-Somoza I, Weigel D (2011) MicroRNA networks and developmental plasticity in plants. Trends Plant Sci 16(5):258–264

    Article  PubMed  CAS  Google Scholar 

  • Ryden LG, Hunt LT (1993) Evolution of protein complexity: the blue copper-containing oxidases and related proteins. J Mol Evol 36(1):41–66

    Article  PubMed  CAS  Google Scholar 

  • Sakurai T, Kataoka K (2007) Structure and function of type I copper in multicopper oxidases. Cell Mol Life Sci 64(19–20):2642–2656

    Article  PubMed  CAS  Google Scholar 

  • Sigfridsson K (1998) Plastocyanin, an electron-transfer protein. Photosynth Res 57(1):1–28

    Article  CAS  Google Scholar 

  • Sunkar R, Zhu J-K (2004) Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell 16(8):2001–2019

    Article  PubMed  CAS  Google Scholar 

  • Sunkar R, Kapoor A, Zhu JK (2006) Posttranscriptional induction of two Cu/Zn superoxide dismutase genes in Arabidopsis is mediated by downregulation of miR398 and important for oxidative stress tolerance. Plant Cell 18(8):2051–2065

    Article  PubMed  CAS  Google Scholar 

  • Ueda T, Nomoto N, Koga M, Ogasa H, Ogawa Y, Matsumoto M, Stampoulis P, Sode K, Terasawa H, Shimada I (2012) Structural basis of efficient electron transport between photosynthetic membrane proteins and plastocyanin in spinach revealed using nuclear magnetic resonance. Plant Cell 24(10):4173–4186

    Article  PubMed  CAS  Google Scholar 

  • Wang C-F, Huang L–L, Buchenauer H, Han Q-M, Zhang H-C, Kang Z-S (2007) Histochemical studies on the accumulation of reactive oxygen species (O2 and H2O2) in the incompatible and compatible interaction of wheat: puccinia striiformis f. sp. tritici. Physiol Mol Plant Pathol 71(4–6):230–239

    Article  CAS  Google Scholar 

  • Wang X, Wang X, Feng H, Tang C, Bai P, Wei G, Huang L, Kang Z (2012) TaMCA4, a novel wheat metacaspase gene functions in programmed cell death induced by the fungal pathogen Puccinia striiformis f. sp. tritici. Mol Plant Microbe Interact 25(6):755–764

    Article  PubMed  CAS  Google Scholar 

  • Yao Y, Guo G, Ni Z, Sunkar R, Du J, Zhu JK, Sun Q (2007) Cloning and characterization of microRNAs from wheat (Triticum aestivum L.). Genome Biol 8(6):R96

    Article  PubMed  Google Scholar 

  • Zhang W, Gao S, Zhou X, Chellappan P, Chen Z, Zhang X, Fromuth N, Coutino G, Coffey M, Jin H (2011a) Bacteria-responsive microRNAs regulate plant innate immunity by modulating plant hormone networks. Plant Mol Biol 75(1–2):93–105

    Article  PubMed  CAS  Google Scholar 

  • Zhang X, Zhao H, Gao S, Wang WC, Katiyar-Agarwal S, Huang HD, Raikhel N, Jin H (2011b) Arabidopsis Argonaute 2 regulates innate immunity via miRNA393*-mediated silencing of a Golgi-localized SNARE gene, MEMB12. Mol Cell 42(3):356–366

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This research was financially supported through grants from The National Basic Research Program (2013CB127700), the National Natural Science Foundation of China (No. 30930064 and No. 31071651) and the 111 Project from the Ministry of Education of China (B07049).

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Correspondence to Zhensheng Kang.

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Feng, H., Zhang, Q., Wang, Q. et al. Target of tae-miR408, a chemocyanin-like protein gene (TaCLP1), plays positive roles in wheat response to high-salinity, heavy cupric stress and stripe rust. Plant Mol Biol 83, 433–443 (2013). https://doi.org/10.1007/s11103-013-0101-9

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