BrRH37, a Cabbage (Brassica rapa) DEAD-Box RNA Helicase, Confers Drought Tolerance and ABA Response in Transgenic Arabidopsis Plants

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 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 Dinh SN, Kang H (2017) An endoplasmic reticulum-localized Coffea arabica BURP domain-containing protein affects the response of transgenic Arabidopsis plants to diverse abiotic stresses. Plant Cell Rep 36:1829–1839 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 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 González-Guzmán M, Apostolova N, Bellés JM, Barrero JM, Piqueras P, Ponce MR, Micol JL, Serrano R, Rodríguez PL (2002) The short-chain alcohol dehydrogenase ABA2 catalyzes the conversion of xanthoxin into abscisic aldehyde. Plant Cell 14:1833–1846 Gu L, Xu T, Lee K, Lee KH, Kang H (2014) A chloroplast-localized DEAD-box RNAhelicase 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 Guan Q, Wu J, Zhang Y, Jiang C, Liu R, Chai C, Zhu J (2013) A DEAD box RNA helicase is critical for pre-mRNA splicing, cold-responsive gene regulation, and cold tolerance in Arabidopsis. Plant Cell 25:342–356 Hall 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 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 Huang CK, Shen YL, Huang LF, Wu SJ, Yeh CH, Lu CA (2016) The DEAD-box RNA helicase AtRH7/PRH75 participates in pre-rRNA processing, plant development and cold tolerance in Arabidopsis. Plant Cell Physiol 57:174–191 Jankowsky E (2011) RNA helicases at work: binding and rearranging. Trends Biochem Sci 36:11–29 Jarmoskaite I, Russell R (2011) DEAD-box proteins as RNA helicases and chaperones. WIREs RNA 2:135–152 Jarmoskaite I, Bhaskaran H, Seifert S, Russell R (2014) DEAD-box protein CYT-19 is activated by exposed helices in a group I intron RNA. Proc Natl Acad Sci USA 22:2928–2936 Kang H, Park SJ, Kwak KJ (2013) Plant RNA chaperones in stress response. Trends Plant Sci 18:100–106 Kant P, Kant S, Gordon M, Shaked R, Barak S (2007) Stress response suppressor1 and stress response suppressor2, two DEAD box RNA helicases that attenuate Arabidopsis responses to multiple abiotic stresses. Plant Physiol 145:814–830 Kim JS, Park SJ, Kwak KJ, Kim YO, Kim JY, Song J, Jang B, Jung CH, Kang H (2007) Cold shock domain proteins and glycine-rich RNA-binding protein from Arabidopsis thaliana can promote the cold adaptation process in Escherichia coli. Nucleic Acids Res 35:506–516 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 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 Cell 39:179–185 Lee K, Kang H (2020) Roles of organellar RNA-binding proteins in plant growth, development, and abiotic stress responses. Int J Mol Sci 21:4548 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 Lu C-A, Huang C-K, Huang W-S, Huang T-S, Liu H-Y, Chen Y-F (2020) DEAD-box RNA helicase 42 plays a critical role in pre-mRNA splicing under cold stress. Plant Physiol 182:255–271 Macovei A, Vaid N, Tula S, Tuteja N (2012) A new DEAD-box helicase ATP-binding protein (OsABP) from rice is responsive to abiotic stress. Plant Signal Behav 7:1138–1143 Maggio A, De PS, Ruggiero C, Barbieri G (2005) Physiological response of field-grown cabbage to salinity and drought stress. Eur J Agron 23:57–67 Mohr S, Stryker JM, Lambowitz AM (2002) 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 8:871 Nawaz G, Kang H (2019) Rice OsRH58, a chloroplast DEAD-box RNA helicase, improves salt or drought stress tolerance in Arabidopsis by affecting chloroplast translation. BMC Plant Biol 19:17 Nawaz G, Lee K, Park SJ, Kim YO, Kang H (2018a) A chloroplast-targeted cabbage DEAD-box RNA helicase BrRH22 confers abiotic stress tolerance to transgenic Arabidopsis plants by affecting translation of chloroplast transcripts. Plant Physiol Biochem 127:336–342 Nawaz G, Sai TZT, Lee K, Kim YO, Kang H (2018b) Rice DEAD-box RNA helicase OsRH53 has negative impact on Arabidopsis response to abiotic stresses. Plant Growth Regul 85:153–163 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 Park SJ, Lee HJ, Lee K, Kang H (2020) A La-related protein LaRP6a delays flowering of Arabidopsis thaliana by upregulating FLC transcript levels. J Plant Biol 63:369–378 Russell R, Jarmoskaite I, Lambowitz AM (2013) Toward a molecular understanding of RNA remodeling by DEAD-box proteins. RNA Biol 10:44–55 Semrad K (2011) Proteins with RNA chaperone activity: a world of diverse proteins with a common task-impediment of RNA misfolding. Biochem Res Int 2011:532908 Seok HY, Nguyen LV, Van Nguyen D, Lee SY, Moon YH (2020) Investigation of a novel salt stress-responsive pathway mediated by Arabidopsis DEAD-box RNA helicase gene AtRH17 using RNA-seq analysis. Int J Mol Sci 21:1595 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 Tripurani SK, Nakaminami K, Thompson KB, Crowell SV, Guy CL, Karlson DT (2011) Spatial and temporal expression of cold-responsive DEAD-box RNA helicases reveals their functional roles during embryogenesis in Arabidopsis thaliana. Plant Mol Biol Rep 29:761–768 Turk EM, Caprara MG (2010) Splicing of yeast aI5β group I intron requires SUV3 to recycle MRS1 via mitochondrial degradosome-promoted decay of excised intron ribonucleoprotein (RNP). J Biol Chem 285:8585–8594 Wang B, Chai H, Zhong Y, Shen Y, Yang W, Chen J, Xin Z, Shi H (2020) The DEAD-box RNA helicase SHI2 functions in repression of salt-inducible genes and regulation of cold-inducible gene splicing. J Exp Bot 71:1598–1613 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 Xiaomei W, Rongrong K, Ting Z, Yuanyuan G, Jianlong X, Zhongze P, Gangseob L, Dongzhi L, Yanjun D (2020) A DEAD-box RNA helicase TCD33 that confers chloroplast development in rice at seedling stage under cold stress. J Plant Physiol 248:153138 Xiong L, Ishitani M, Lee H, Zhu JK (2001) The Arabidopsis LOS5/ABA3 locus encodes a molybdenum cofactor sulfurase and modulates cold stress- and osmotic stress-responsive gene expression. Plant Cell 13:2063–2083 Xiong L, Lee H, Ishitani M, Zhu JK (2002) Regulation of osmotic stress-responsive gene expression by the LOS6/ABA1 locus in Arabidopsis. J Biol Chem 277:8588–8596 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 Zhu M, Chen G, Dong T, Wang L, Zhang J, Zhao Z, Hu Z (2015) SlDEAD31, a putative DEAD-box RNA helicase gene, regulates salt and drought tolerance and stress-related genes in tomato. PLoS ONE 10:e0133849