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Artificial targeting of a nucleus-encoded RNA-binding protein AtRZ1a to chloroplasts affects flowering and ABA response of Arabidopsis thaliana

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Abstract

Despite the fact that many nucleus-encoded RNA-binding proteins (RBPs) are targeted to chloroplasts and play essential roles in RNA metabolism in chloroplasts, the question of whether artificial targeting of a nucleus-encoded RBP to chloroplasts affects chloroplast function and plant growth has never been addressed. In this study, a nuclear zinc finger-containing Arabidopsis RBP, designated AtRZ1a, which was previously shown to play a role in stress response, was artificially targeted to chloroplasts, and the growth and stress response of the transgenic plants were evaluated. Confocal analysis of the cellular localization of the cTP_AtRZ1a protein containing the N-terminal chloroplast transit peptide (cTP) from rubisco small subunit revealed that the cTP_AtRZ1a fusion protein is successfully targeted to chloroplasts. When grown under normal conditions, flowering of the transgenic plants was delayed, and the FLC expression was significantly upregulated in the transgenic plants. Artificial targeting of AtRZ1a to chloroplasts severely inhibited seedling growth of the plants in the presence of ABA by upregulating expression of ABA signaling-related genes ABI3 and ABI4. Taken together, these results suggest that artificial targeting of a nucleus-encoded AtRZ1a to chloroplasts affects the growth and development of Arabidopsis under normal or ABA treated conditions.

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References

  • Albertos P, Romero-Puertas MC, Tatematsu K, Mateos I, Sánchez-Vicente I, Nambara E, Lorenzo O (2015) See comment in PubMed Commons belowS-nitrosylation triggers ABI5 degradation to promote seed germination and seedling growth. Nat Commun 6:8669

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bae H, Lee DS, Hwang I (2006) Dual targeting of xylanase to chloroplasts and peroxisomes as a means to increase protein accumulation in plant cells. J Exp Bot 57:161–169

    Google Scholar 

  • Bechtold N, Pelletier G (1998) In planta Agrobacterium-mediated transformation of adult Arabidopsis thaliana plants by vacuum infiltration. Methods Mol Biol 82:259–266

    CAS  PubMed  Google Scholar 

  • Bryant N, Lloyd J, Sweeney C, Myouga F, Meinke D (2011) Identification of nuclear genes encoding chloroplast-localized proteins required for embryo development in Arabidopsis. Plant Physiol 155:1678–1689

    Article  CAS  PubMed  Google Scholar 

  • Burd CG, Dreyfuss G (1994) Conserved structures and diversity of functions of RNA-binding proteins. Science 265:615–621

    Article  CAS  PubMed  Google Scholar 

  • del Campo EM (2009) Post-transcriptional control of chloroplast gene expression. Gene Regul Syst Biol 3:31–47

    Google Scholar 

  • Chakraborty J, Sen S, Ghosh P, Sengupta A, Basu D, Das S (2016) Homologous promoter derived constitutive and chloroplast targeted expression of synthetic cry1Ac in transgenic chickpea confers resistance against Helicoverpa armigera. Plant Cell Tiss Organ Cult 125:521–535

    Article  CAS  Google Scholar 

  • Corbin DR, Grebenok RJ, Ohnmeiss TE, Greenplate JT, Purcell JP (2001) Expression and chloroplast targeting of cholesterol oxidase in transgenic tobacco plants. Plant Physiol 126:1116–1128

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cutler SR, Rodriguez PL, Finkelstein RR, Abrams SR (2010) Abscisic acid: Emergence of a core signaling network. Annu Rev Plant Biol 61:651–679

    Article  CAS  PubMed  Google Scholar 

  • Feng CZ, Chen Y, Wang C, Kong YH, Wu WH, Chen YF (2014) Arabidopsis RAV1 transcription factor, phosphorylated by SnRK2 kinases, regulates the expression of ABI3, ABI4, and ABI5 during seed germination and early seedling development. Plant J 80:654–668

    Article  CAS  PubMed  Google Scholar 

  • Finkelstein RR, Wang ML, Lynch TJ, Rao S, Goodman HM (1998) The Arabidopsis abscisic acid response locus ABI4 encodes an APETALA 2 domain protein. Plant Cell 10:1043–1054

    CAS  PubMed  PubMed Central  Google Scholar 

  • Finkelstein RR, Lynch TJ (2000) The Arabidopsis abscisic acid response gene ABI5 encodes a basic leucine zipper transcription factor. Plant Cell 12:599–609

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gu L, Jung HJ, Kim BM, Xu T, Lee K, Kim YO, Kang H (2015) A chloroplast-localized S1 domain-containing protein SRRP1 plays a role in Arabidopsis seedling growth in the presence of ABA. J Plant Physiol 189:34–41

    Article  CAS  PubMed  Google Scholar 

  • Jacobs J, Kück U (2011) Function of chloroplast RNA-binding proteins. Cell Mol Life Sci 68:735–748

    Article  CAS  PubMed  Google Scholar 

  • Jang IC, Lee KH, Nahm BH, Kim JK (2002) Chloroplast targeting signal of a rice rbcS gene enhances transgene expression. Mol Breed 9:81–91

    Article  CAS  Google Scholar 

  • Jarvis P (2008) Targeting of nucleus-encoded proteins to chloroplasts in plants. New Phytol 179:257–285

    Article  CAS  PubMed  Google Scholar 

  • Kakizaki T, Matsumura H, Nakayama K, Che FS, Terauchi R, Inaba T (2009) Coordination of plastid protein import and nuclear gene expression by plastid-to-nucleus retrograde signaling. Plant Physiol 151:1339–1353

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim WY, Kim JY, Jung HJ, Oh SH, Han YS, Kang H (2010) Comparative analysis of Arabidopsis zinc finger-containing glycine-rich RNA-binding proteins during cold adaptation. Plant Physiol Biochem 48:866–872

    Article  CAS  PubMed  Google Scholar 

  • Kim YO, Pan SO, Jung H, Kang H (2007) A zinc finger-containing glycine-rich RNA-binding protein, atRZ-1a, has a negative impact on seed germination and seedling growth of Arabidopsis thaliana under salt or drought stress conditions. Plant Cell Physiol 48:1170–1181

    Article  CAS  PubMed  Google Scholar 

  • Kim YO, Kim JS, Kang H (2005) Cold-inducible zinc finger-containing glycine-rich RNA-binding protein contributes to the enhancement of freezing tolerance in Arabidopsis thaliana. Plant J 42:890–900

    Article  CAS  PubMed  Google Scholar 

  • Kim EH, Suh SC, Park BS, Shin KS, Kweon SJ, Han EJ, Park SH, Kim YS, Kim JK (2009) Chloroplast-targeted expression of synthetic cry1Ac in transgenic rice as an alternative strategy for increased pest protection. Planta 230:397–405

    Article  CAS  PubMed  Google Scholar 

  • Kwak KJ, Kim YO, Kang H (2005) Characterization of transgenic Arabidopsis plants overexpressing GR-RBP4 under high salinity, dehydration, or cold stress. J Exp Bot 56:3007–3016

    Article  CAS  PubMed  Google Scholar 

  • Larkum AW, Lockhart PJ, Howe CJ (2007) Shopping for plastids. Trends Plant Sci 12:189–195

    Article  CAS  PubMed  Google Scholar 

  • Larkin RM, Alonso JM, Ecker JR, Chory J (2003) GUN4, a regulator of chlorophyll synthesis and intracellular signaling. Science 299:902–906

    Article  CAS  PubMed  Google Scholar 

  • Lee K, Kang H (2016) Emerging roles of RNA-binding proteins in plant growth, development, and stress responses. Mol Cells 39:79–185

    Google Scholar 

  • Lee DW, Kim JK, Lee S, Choi S, Kim S, Hwang I (2008) Arabidopsis nuclear-encoded plastid transit peptides contain multiple sequence subgroups with distinctive chloroplast-targeting sequence motifs. Plant Cell 20:1603–1622

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leister D (2003) Chloroplast research in the genomic age. Trends Genet 19:47–56

    Article  CAS  PubMed  Google Scholar 

  • Lorkovic ZJ, Barta A (2002) Genome analysis: RNA recognition motif (RRM) and K homology (KH) domain RNA-binding proteins from the flowering plant Arabidopsis thaliana. Nucleic Acids Res 30:623–635

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martin W, Rujan T, Richly E, Hansen A, Cornelsen S, Lins T, Leister D, Stoebe B, Hasegawa M, Penny D (2002) Evolutionary analysis of Arabidopsis, cyanobacterial, and chloroplast genomes reveals plastid phylogeny and thousands of cyanobacterial genes in the nucleus. Proc Natl Acad Sci USA 99:12246–12251

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mochizuki N, Brusslan JA, Larkin R, Nagatani A, Chory J (2001) Arabidopsis genomes uncoupled 5 (GUN5) mutant reveals the involvement of Mg-chelatase H subunit in plastid-to-nucleus signal transduction. Proc Natl Acad Sci 98:2053–2058

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nickelsen J (2003) Chloroplast RNA-binding proteins. Curr Genet 43:392–399

    Article  CAS  PubMed  Google Scholar 

  • Nott A, Jung HS, Koussevitzky S, Chory J (2006) Plastid-to-nucleus retrograde signaling. Annu Rev Plant Bio l57:739–759

    Article  Google Scholar 

  • Pesaresi P, Schneider A, Kleine T, Leister D (2007) Interorganellar communication. Curr Opin Plant Biol 10:600–606

    Article  CAS  PubMed  Google Scholar 

  • Picault N, Cazalé AC, Beyly A, Cuiné S, Carrier P, Luu DT, Forestier C, Peltier G (2006) Chloroplast targeting of phytochelatin synthase in Arabidopsis: effects on heavy metal tolerance and accumulation. Biochimie 88:1743–1750

    Article  CAS  PubMed  Google Scholar 

  • Reyes-Prieto A, Weber AP, Bhattacharya D (2007) The origin and establishment of the plastid in algae and plants. Annu Rev Genet 41:147–168

    Article  CAS  PubMed  Google Scholar 

  • Stern DB, Goldschmidt-Clermont M, Hanson MR (2010) Chloroplast RNA metabolism. Annu Rev Plant Biol 61:125–155

    Article  CAS  PubMed  Google Scholar 

  • Sun Q, Zybailov B, Majeran W, Friso G, Olinares PD, van Wijk KJ (2009) PPDB, the plant proteomics database at Cornell. Nucleic Acids Res. 37(Database issue):D969–D974

    Article  CAS  PubMed  Google Scholar 

  • Surpin M, Larkin RM, Chory J (2002) Signal transduction between the chloroplast and the nucleus. Plant Cell 14:S327–S338

    CAS  PubMed  PubMed Central  Google Scholar 

  • Terry MJ, Smith AG (2013) A model for tetrapyrrole synthesis as the primary mechanism for plastid-to-nucleus signaling during chloroplast biogenesis. Front Plant Sci 4:14

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Timmis JN, Ayliffe MA, Huang CY, Martin W (2004) Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nat Rev Genet 5:123–135

    Article  CAS  PubMed  Google Scholar 

  • Woodson JD, Perez-Ruiz JM, Schmitz RJ, Ecker JR, Chory J (2013) Sigma factor-mediated plastid retrograde signals control nuclear gene expression. Plant J 73:1–13

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Plant Biotechnology, College of Agriculture and Life Sciences, Chonnam National University, Gwangju, 61186, Korea

    Jiseong Kim, Tieu-Ngoc Le Nguyen & Hunseung Kang

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  1. Jiseong Kim
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  2. Tieu-Ngoc Le Nguyen
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  3. Hunseung Kang
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Correspondence to Hunseung Kang.

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Kim, J., Le Nguyen, TN. & Kang, H. Artificial targeting of a nucleus-encoded RNA-binding protein AtRZ1a to chloroplasts affects flowering and ABA response of Arabidopsis thaliana . J. Plant Biol. 60, 278–284 (2017). https://doi.org/10.1007/s12374-017-0044-9

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  • DOI: https://doi.org/10.1007/s12374-017-0044-9

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