Abstract
DEAD-box RNA helicases (RHs) play key roles in the regulation of RNA metabolism at the posttranscriptional level. In this study, the expression patterns under abiotic stresses and the functions of a rice (Oryza sativa) RH, OsRH53, in stress response were determined using transgenic Arabidopsis plants. The level of OsRH53 decreased upon abiotic stress treatment, including, drought, salt, cold, and UV stress, and by abscisic acid (ABA). Although OsRH53 contains a putative chloroplast transit peptide at the N-terminal end, confocal analysis of OsRH53–GFP fusion proteins transiently expressed in tobacco leaves revealed that OsRH53 is localized to the nucleus. OsRH53-expressing transgenic Arabidopsis displayed retarded germination and reduced growth under high salinity or dehydration stress but not under cold stress. OsRH53 negatively affected the growth and cotyledon greening of seedlings upon ABA application by activating the genes related to ABA signaling such as ABI3 and ABI4. The ability of OsRH53 to recover growth-defect phenotype of Escherichia coli mutant, and both in vitro and in vivo base pair-breaking ability confirmed that OsRH53 harbors RNA chaperone activity. Collectively, these results suggest that OsRH53 negatively affects plant abiotic stress responses via modulating RNA metabolism through its RNA chaperone activity.
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References
Ambrosone A, Costa A, Leone A, Grillo S (2012) Beyond transcription: RNA-binding proteins as emerging regulators of plant response to environmental constraints. Plant Sci 182:12–18
Asakura Y, Galarneau E, Watkins KP, Barkan A, van Wijk KJ (2012) Chloroplast RH3 DEAD-box RNA helicases in Zea mays and Arabidopsis thaliana function in splicing of specific group II introns and affect chloroplast ribosome. Plant Physiol 159:961–974
Bechtold N, Pelletier G (1998) In planta Agrobacterium-mediated transformation of adult Arabidopsis thaliana plants by vacuum infiltration. Methods Mol Biol 82:259–266
Bickmore WA, Sutherland HG (2002) Addressing protein localization within the nucleus. EMBO J 21:1248–1254
Chung E, Cho CW, Yun BH, Choi HK, So HA, Lee SW, Lee JH (2009) Molecular cloning and characterization of the soybean DEAD-box RNA helicase gene induced by low temperature and high salinity stress. Gene 443:91–99
Cutler SR, Rodriguez PL, Finkelstein RR, Abrams SR (2010) Abscisic acid: Emergence of a core signaling network. Annu Rev Plant Biol 61:651–679
Fairman-Williams ME, Guenther UP, Jankowsky E (2010) SF1 and SF2 helicases: family matters. Curr Opin Struct Biol 20:313–324
Finkelstein RR (2013) Abscisic acid synthesis and response. Arabidopsis Book 11:e0166
Finkelstein RR, Lynch TJ (2000) The Arabidopsis abscisic acid response gene ABI5 encodes a basic leucine zipper transcription factor. Plant Cell 12:599–609
Gallardo K, Job C, Groot SP, Puype M, Demol H, Vandekerckhove J, Job D (2001) Proteomic analysis of Arabidopsis seed germination and priming. Plant Physiol 126:835–848
Gong Z, Dong CH, Lee H, Zhu J, Xiong L, Gong D, Stevenson B, Zhu JK (2005) A DEAD-box RNA helicase is essential for mRNA export and important for development and stress responses in Arabidopsis. Plant Cell 17:256–267
Grover A, Minhas D (2000) Towards the production of abiotic stress tolerant transgenic rice plants: Issues, progress and future research needs. Proc Indian Nat Sci Acad B 66:13–32
Gu L, Xu T, Lee K, Lee KH, Kang H (2014) A chloroplast-localized DEAD-box RNA helicase AtRH3 is essential for intron splicing and plays an important role in the growth and stress response in Arabidopsis thaliana. Plant Physiol Biochem 82:309–318
Halls C, Mohr S, del Campo M, Yang Q, Jankowsky E, Lambowitz AM (2007) Involvement of DEAD-box proteins in group I and group II intron splicing. Biochemical characterization of Mss116p, ATP hydrolysis-dependent and -independent mechanisms, and general RNA chaperone activity. J Mol Biol 365:835–855
He J, Duan Y, Hua D, Fan G, Wang L, Liu Y (2012) DEXH box RNA helicase-mediated mitochondrial reactive oxygen species production in Arabidopsis mediates crosstalk between abscisic acid and auxin signaling. Plant Cell 24:1815–1833
Hsu YF, Chen YC, Hsiao YC, Wang BJ, Lin SY, Cheng WH, Jauh GY, Harada JJ, Wang CS (2014) AtRH57, a DEAD-box RNA helicase, is involved in feedback inhibition of glucose-mediated abscisic acid accumulation during seedling development and additively affects pre-ribosomal RNA processing with high glucose. Plant J 77:119–135
Kang H, Park SJ, Kwak KJ (2013) Plant RNA chaperones in stress response. Trends Plant Sci 18:100–106
Kim JS, Kim KA, Oh TR, Park CM, Kang H (2008) Functional characterization of DEAD-box RNA helicases in Arabidopsis thaliana under abiotic stress conditions. Plant Cell Physiol 49:1563–1571
Kim J, Le T-NN, Kang H (2017) 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
Landick R, Stewart J, Lee DN (1990) Amino acid changes in conserved regions of the beta-subunit of Escherichia coli RNA polymerase alter transcription pausing and termination. Genes Dev 4:1623–1636
Lee K, Kang H (2016) Emerging roles of RNA-binding proteins in plant growth, development, and stress responses. Mol Cells 39:179–185
Lee DW, Jung C, Hwang I (2013) Cytosolic events involved in chloroplast protein targeting. Biochim Biophys Acta 1833:245–252
Liu Y, Tabata D, Imai R (2016) A cold-inducible DEAD-box RNA helicase from Arabidopsis thaliana regulates plant growth and development under low temperature. PLoS ONE 11:e0154040
Lorković ZJ (2009) Role of plant RNA-binding proteins in development, stress response and genome organization. Trends Plant Sci 14:229–236
Lotfi A, Pervaiz T, Jiu S, Faghihi F, Jahanbakhshian Z, Khorzoghi EG, Fang J, Seyedi SM (2017) Role of microRNAs and their target genes in salinity response in plants. Plant Growth Regul 82:377–390
Millar AH, Whelan J, Small I (2006) Recent surprises in protein targeting to mitochondria and plastids. Curr Opin Plant Biol 9:610–615
Mohr S, Stryker JM, Lambowitz AM (2002) A DEAD-box protein functions as an ATP-dependent RNA chaperone in group I intron splicing. Cell 109:769–779
Nawaz G, Kang H (2017) Chloroplast-or Mitochondria-targeted DEAD-box RNA helicases play essential roles in organellar RNA metabolism and abiotic stress responses. Front Plant Sci 8:e871
Park YR, Choi MJ, Park SJ, Kang H (2017) Three zinc-finger RNA-binding proteins in cabbage (Brassica rapa) play diverse roles in seed germination and plant growth under normal and abiotic stress conditions. Physiol Plant 159:93–106
Semrad K (2011) Proteins with RNA chaperone activity: a world of diverse proteins with a common task-impediment of RNA misfolding. Biochem Res Int 10:1155–1165
Silverman E, Edwalds-Gilbert G, Lin RJ (2003) DExD/H-box proteins and their partners: helping RNA helicases unwind. Gene 312:1–16
Tanz SK, Castleden I, Hooper CM, Small I, Millar AH (2014) Using the SUB cellular database for Arabidopsis proteins to localize the Deg protease family. Front Plant Sci 5:396
Tuteja N, Sahoo RK, Garg B, Tuteja R (2013) OsSUV3 dual helicase functions in salinity stress tolerance by maintaining photosynthesis and antioxidant machinery in rice (Oryza sativa L. cv. IR64). Plant J 76:115–127
Vashisht AA, Tuteja N (2006) Stress responsive DEAD-box helicases: a new pathway to engineer plant stress tolerance. J Photochem Photobiol 84:150–160
Wang D, Qin B, Li X, Tang D, Zhang Y, Cheng Z, Xue Y (2016) Nucleolar DEAD-box RNA helicase TOGR1 regulates thermotolerant growth as a pre-rRNA chaperone in rice. PLoS Genet 12:e1005844
Xia B, Ke H, Inouye M (2001) Acquirement of cold sensitivity by quadruple deletion of the cspA family and its suppression by PNPase S1 domain in Escherichia coli. Mol Microbiol 40:179–188
Xu T, Gu L, Choi MJ, Kim RJ, Suh MC, Kang H (2014) Comparative functional analysis of wheat (Triticum aestivum) zinc finger-containing glycine-rich RNA-binding proteins in response to abiotic stresses. PLoS ONE 9:1–8
Xu T, Lee HJ, Sy ND, Kang H (2015) Wheat (Triticum aestivum) zinc finger-containing glycine-rich RNA-binding protein TaRZ1 affects plant growth and defense response in Arabidopsis thaliana. Plant Growth Regul 76:243–250
Yamaguchi S, Smith MW, Brown RG, Kamiya Y, Sun T (1998) Phytochrome regulation and differential expression of gibberellin 3β-hydroxylase genes in germinating Arabidopsis seeds. Plant Cell 10:2115–2126
Zhu M, Chen G, Dong T, Wang L, Zhang J, Zhao Z (2015) SlDEAD31, a putative DEAD-box RNA helicase gene, regulates salt and drought tolerance and stress-related genes in tomato. PLoS ONE 10:1–20
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This work was supported by a grant from the Next-Generation BioGreen21 Program (PJ01103601; PJ01312201), Rural Development Administration, Republic of Korea.
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Nawaz, G., Sai, T.Z.T., Lee, K. et al. Rice DEAD-box RNA helicase OsRH53 has negative impact on Arabidopsis response to abiotic stresses. Plant Growth Regul 85, 153–163 (2018). https://doi.org/10.1007/s10725-018-0381-9
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DOI: https://doi.org/10.1007/s10725-018-0381-9