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Identification, expression analysis, and function evaluation of 42 tomato DEAD-box RNA helicase genes in growth development and stress response

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Abstract

DEAD-box RNA helicases play pivotal roles in almost all processes in RNA metabolisms, associated with various cellular functions including plant development and the response to abiotic stress. Previously, although DEAD-box genes were identified in tomato genome, specific molecular characterizations regarding development- and/or stress-related tomato DEAD-box genes are still rudimentary. In this study, a systematic expression analysis and function evaluation of 42 DEAD-box RNA helicase genes was conducted in the growth development and stress response of tomato using qRT-PCR. The results revealed that these SlDEAD genes showed discrepant tissue-/organ-specific (such as leaf, flower and fruit) expression levels, indicating that they might play important and different roles in tomato development. Variant expression profiles of many SlDEAD genes were observed when treated with different hormones including ABA, ACC, GA3, IAA, and SA. Moreover, the transcription of multiple tomato SlDEAD genes was also upregulated by multiple abiotic stresses, such as salinity, dehydration, and heat and cold stresses. Cumulatively, the data will be valuable to comprehensive functional characterization of SlDEAD genes, and to support the thesis that DEAD-box RNA helicases may represent one of the main components that mediate hormone signaling and stress responses in tomato.

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References

  • Asakura Y, Galarneau E, Watkins KP, Barkan A, van Wijk KJ (2012) Chloroplast RH3 DEAD box RNA helicases in maize and Arabidopsis function in splicing of specific group II introns and affect chloroplast ribosome biogenesis. Plant Physiol 159(3):961–974

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bari R, Jones JD (2009) Role of plant hormones in plant defence responses. Plant Mol Biol 69(4):473–488

    Article  CAS  PubMed  Google Scholar 

  • Beaudoin N, Serizet C, Gosti F, Giraudat J (2000) Interactions between abscisic acid and ethylene signaling cascades. Plant Cell 12(7):1103–1115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen J, Wan S, Liu H, Fan S, Zhang Y, Wang W, Xia M, Yuan R, Deng F, Shen F (2016) Overexpression of an Apocynum venetum DEAD-box helicase gene (AvDH1) in cotton confers salinity tolerance and increases yield in a saline field. Front Plant Sci 6:1227

    PubMed  PubMed Central  Google Scholar 

  • Expósito-Rodríguez M, Borges AA, Borges-Pérez A, Pérez JA (2008) Selection of internal control genes for quantitative real-time RT-PCR studies during tomato development process. BMC Plant Biol 8(1):131

    Article  PubMed  PubMed Central  Google Scholar 

  • Foolad MR (2007) Current status of breeding tomatoes for salt and drought tolerance. In: Advances in molecular breeding toward drought and salt tolerant crops. Springer p 669–700

  • Gong Z, Lee H, Xiong L, Jagendorf A, Stevenson B, Zhu J-K (2002) RNA helicase-like protein as an early regulator of transcription factors for plant chilling and freezing tolerance. Proc Nat Acad Sci USA 99(17): 11507–11512

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gong Z, Dong C-H, Lee H, Zhu J, Xiong L, Gong D, Stevenson B, Zhu J-K (2005) A DEAD box RNA helicase is essential for mRNA export and important for development and stress responses in Arabidopsis. Plant Cell 17(1):256–267

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gorbalenya AE, Koonin EV (1993) Helicases: amino acid sequence comparisons and structure-function relationships. Curr Opin Struct Biol 3(3):419–429

    Article  CAS  Google Scholar 

  • Gorbalenya AE, Koonin EV, Donchenko AP, Blinov VM (1988) A conserved NTP-motif in putative helicases. Nature 333(6168):22

    Article  CAS  PubMed  Google Scholar 

  • Gu L, Xu T, Lee K, Lee KH, Kang H (2014) A chloroplast-localized DEAD-box RNA helicaseAtRH3 is essential for intron splicing and plays an important role in the growth and stress response in Arabidopsis thaliana. Plant Physiol Biochem 82(3):309–318

    Article  CAS  PubMed  Google Scholar 

  • 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(1):342–356

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • He J, Duan Y, Hua D, Fan G, Wang L, Liu Y, Chen Z, Han L, Qu L-J, Gong Z (2012) DEXH box RNA helicase-mediated mitochondrial reactive oxygen species production in Arabidopsis mediates crosstalk between abscisic acid and auxin signaling. Plant Cell 24(5):1815–1833

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hedden P, Thomas SG (2012) Gibberellin biosynthesis and its regulation. Biochem J 444(1):11–25

    Article  CAS  PubMed  Google Scholar 

  • Huang C-K, Huang L-F, Huang J-J, Wu S-J, Yeh C-H, Lu C-A (2010) A DEAD-box protein, AtRH36, is essential for female gametophyte development and is involved in rRNA biogenesis in Arabidopsis. Plant Cell Physiol 51(5):694–706

    Article  CAS  PubMed  Google Scholar 

  • Jacobsen SE, Running MP, Meyerowitz EM (1999) Disruption of an RNA helicase/RNAse III gene in Arabidopsis causes unregulated cell division in floral meristems. Development 126(23):5231–5243

    CAS  PubMed  Google Scholar 

  • Kanai M, Hayashi M, Kondo M, Nishimura M (2013) The Plastidic DEAD-box RNA helicase 22, HS3, is essential for plastid functions both in seed development and in seedling growth. Plant Cell Physiol 54(9):1431–1440

    Article  CAS  PubMed  Google Scholar 

  • 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(3):814–830

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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(10):1563–1571

    Article  CAS  PubMed  Google Scholar 

  • Kobayashi K, Otegui MS, Krishnakumar S, Mindrinos M, Zambryski P (2007) INCREASED SIZE EXCLUSION LIMIT2 encodes a putative DEVH box RNA helicase involved in plasmodesmata function during Arabidopsis embryogenesis. Plant Cell 19(6):1885–1897

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kou X, Wang S, Wu M, Guo R, Xue Z, Meng N, Tao X, Chen M, Zhang Y (2014) Molecular characterization and expression analysis of NAC family transcription factors in tomato. Plant Mol Biol Rep 32(2):501–516

    Article  CAS  Google Scholar 

  • Le DT, Nishiyama R, Watanabe Y, Mochida K, Yamaguchi-Shinozaki K, Shinozaki K, Tran L-SP (2011) Genome-wide survey and expression analysis of the plant-specific NAC transcription factor family in soybean during development and dehydration stress. DNA Res 18(4):263–276

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee KH, Park J, Williams DS, Xiong Y, Hwang I, Kang BH (2013) Defective chloroplast development inhibits maintenance of normal levels of abscisic acid in a mutant of the Arabidopsis RH3 DEAD-box protein during early post-germination growth. Plant J 73(5):720–732

    Article  CAS  PubMed  Google Scholar 

  • Li D, Liu H, Zhang H, Wang X, Song F (2008) OsBIRH1, a DEAD-box RNA helicase with functions in modulating defence responses against pathogen infection and oxidative stress. J Exp Bot 59(8):2133–2146

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Linder P (2006) DEAD-box proteins: a family affair—active and passive players in RNP-remodeling. Nucleic Acids Res 34(15):4168–4180

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Linder P, Owttrim GW (2009) Plant RNA helicases: linking aberrant and silencing RNA. Trends Plant Sci 14(6):344–352

    Article  CAS  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2–∆∆CT Method. Methods 25(4):402–408

    Article  CAS  PubMed  Google Scholar 

  • Ljung K (2013) Auxin metabolism and homeostasis during plant development. Development 140(5):943–950

    Article  CAS  PubMed  Google Scholar 

  • Løvdal T, Lillo C (2009) Reference gene selection for quantitative real-time PCR normalization in tomato subjected to nitrogen, cold, and light stress. Anal Biochem 387(2):238–242

    Article  PubMed  Google Scholar 

  • Macovei A, Tuteja N (2012) microRNAs targeting DEAD-box helicases are involved in salinity stress response in rice (Oryza sativa L.). BMC Plant Biol 12(1):183

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nawaz G, Kang H (2017) Chloroplast- or mitochondria-targeted dead-Box RNA helicases play essential roles in organellar RNA metabolism and abiotic stress responses. Frontiers in Plant Science 8

  • Nicot N, Hausman J-F, Hoffmann L, Evers D (2005) Housekeeping gene selection for real-time RT-PCR normalization in potato during biotic and abiotic stress. J Exp Bot 56(421):2907–2914

    Article  CAS  PubMed  Google Scholar 

  • Nouri MZ, Moumeni A, Komatsu S (2015) Abiotic stresses: insight into gene regulation and protein expression in photosynthetic pathways of plants. Int J Mol Sci 16(9):20392–20416

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pan Y, Seymour GB, Lu C, Hu Z, Chen X, Chen G (2012) An ethylene response factor (ERF5) promoting adaptation to drought and salt tolerance in tomato. Plant Cell Rep 31(2):349–360

    Article  CAS  PubMed  Google Scholar 

  • Pastori GM, Foyer CH (2002) Common components, networks, and pathways of cross-tolerance to stress. The central role of “redox” and abscisic acid-mediated controls. Plant Physiol 129(2):460–468

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rivassan Vicente M, Plasencia J (2011) Salicylic acid beyond defence: its role in plant growth and development. J Exp Bot 62(10):3321–3338

    Article  CAS  Google Scholar 

  • Rocak S, Linder P (2004) DEAD-box proteins: the driving forces behind RNA metabolism. Nat Rev Mol Cell Biol 5(3):232–241

    Article  CAS  PubMed  Google Scholar 

  • Santner A, Calderonvillalobos LI, Estelle M (2009) Plant hormones are versatile chemical regulators of plant growth. Nat Chem Biol 5(5):301–307

    Article  CAS  PubMed  Google Scholar 

  • Shivakumara TN, Sreevathsa R, Dash PK, Sheshshayee MS, Papolu PK, Rao U, Tuteja N, Udayakumar M (2017) Overexpression of Pea DNA Helicase 45 (PDH45) imparts tolerance to multiple abiotic stresses in chili (Capsicum annuum L.). Sci Rep 7 7(1):2760

    Article  Google Scholar 

  • Stonebloom S, Burch-Smith T, Kim I, Meinke D, Mindrinos M, Zambryski P (2009) Loss of the plant DEAD-box protein ISE1 leads to defective mitochondria and increased cell-to-cell transport via plasmodesmata. Proc Natl Acad Sci 106(40): 17229–17234

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30(12):2725–2729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tang Y, Liu M, Gao S, Zhang Z, Zhao X, Zhao C, Zhang F, Chen X (2012) Molecular characterization of novel TaNAC genes in wheat and overexpression of TaNAC2a confers drought tolerance in tobacco. Physiol Plant 144(3):210–224

    Article  CAS  PubMed  Google Scholar 

  • 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(4):761–768

    Article  CAS  Google Scholar 

  • Tuteja N (2003) Plant DNA helicases: the long unwinding road. J Exp Bot 54(391):2201–2214

    Article  CAS  PubMed  Google Scholar 

  • Tuteja N, Ahmad P, Panda BB, Tuteja R (2009) Genotoxic stress in plants: shedding light on DNA damage, repair and DNA repair helicases. Mutat Res 681(2):134–149

    Article  CAS  PubMed  Google Scholar 

  • 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(1):115–127

    CAS  PubMed  Google Scholar 

  • Tuteja N, Banu MS, Huda KM, Gill SS, Jain P, Pham XH, Tuteja R (2014) Pea p68, a DEAD-box helicase, provides salinity stress tolerance in transgenic tobacco by reducing oxidative stress and improving photosynthesis machinery. PloS ONE 9(5):585–590

    Article  Google Scholar 

  • Umate P, Tuteja R, Tuteja N (2010) Genome-wide analysis of helicase gene family from rice and Arabidopsis: a comparison with yeast and human. Plant Mol Biol 73(4–5):449–465

    Article  CAS  PubMed  Google Scholar 

  • Vashisht AA, Tuteja N (2006) Stress responsive DEAD-box helicases: a new pathway to engineer plant stress tolerance. J Photochem Photobiol B 84(2):150–160

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Duby G, Purnelle B, Boutry M (2000) Tobacco VDL gene encodes a plastid DEAD box RNA helicase and is involved in chloroplast differentiation and plant morphogenesis. Plant Cell 12(11):2129–2142

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Western TL, Cheng Y, Liu J, Chen X (2002) HUA ENHANCER2, a putative DExH-box RNA helicase, maintains homeotic B and C gene expression in Arabidopsis. Development 129(7):1569–1581

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wolters H, Jürgens G (2009) Survival of the flexible: hormonal growth control and adaptation in plant development. Nat Rev Genet 10(5):305

    Article  CAS  PubMed  Google Scholar 

  • Woodward AW, Bartel B (2005) Auxin: regulation, action, and interaction. Ann Bot 95(5):707–735

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu R, Zhang S, Lu L, Cao H, Zheng C (2012) A genome-wide analysis of the RNA helicase gene family in Solanum lycopersicum. Gene 513(1):128–140

    Article  PubMed  Google Scholar 

  • Xu R, Zhang S, Huang J, Zheng C (2013) Genome-wide comparative in silico analysis of the RNA helicase gene family in zea mays and glycine max: a comparison with arabidopsis and Oryza sativa. PloS ONE 8(11):e78982

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoine M, Nishii T, Nakamura K (2006) Arabidopsis UPF1 RNA helicase for nonsense-mediated mRNA decay is involved in seed size control and is essential for growth. Plant Cell Physiol 47(5):572–580

    Article  CAS  PubMed  Google Scholar 

  • Zhang M, Yuan B, Leng P (2009) The role of ABA in triggering ethylene biosynthesis and ripening of tomato fruit. J Exp Bot 60(6):1579–1588

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu JK (2016) Abiotic stress signaling and responses in plants. Cell 167(2):313–324

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu J, Dong C-H, Zhu J-K (2007) Interplay between cold-responsive gene regulation, metabolism and RNA processing during plant cold acclimation. Curr Opin Plant Biol 10(3):290–295

    Article  CAS  PubMed  Google Scholar 

  • Zhu M, Chen G, Zhou S, Tu Y, Wang Y, Dong T, Hu Z (2014a) A new tomato NAC (NAM/ATAF1/2/CUC2) transcription factor, SlNAC4, functions as a positive regulator of fruit ripening and carotenoid accumulation. Plant Cell Physiol 55(1):119–135

    Article  CAS  PubMed  Google Scholar 

  • Zhu M, Hu Z, Zhou S, Wang L, Dong T, Pan Y, Chen G (2014b) Molecular characterization of six tissue-specific or stress-inducible genes of NAC transcription factor family in tomato (Solanum lycopersicum). J Plant Growth Regul 33(4):730–744

    Article  CAS  Google Scholar 

  • 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(8):e0133849

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhu DZ, Zhao XF, Liu CZ, Ma FF, Wang F, Gao XQ, Zhang XS (2016) Interaction between RNA helicase ROOT INITIATION DEFECTIVE 1 and GAMETOPHYTIC FACTOR 1 is involved in female gametophyte development in Arabidopsis. J Exp Bot 67(19):5757–5768

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This work was supported by the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD), National Natural Science Foundation of China (31700226), Natural Science Foundation of Jiangsu Province of China (BK20160215, BK20150229), Natural science fund for colleges and universities in Jiangsu Province (16KJB210004, 15KJB210001).

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Correspondence to Yonghua Han or Mingku Zhu.

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Communicated by Y. Wang.

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Cai, J., Meng, X., Li, G. et al. Identification, expression analysis, and function evaluation of 42 tomato DEAD-box RNA helicase genes in growth development and stress response. Acta Physiol Plant 40, 94 (2018). https://doi.org/10.1007/s11738-018-2665-0

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