Abstract
RNA helicase catalyzes the denaturation of DNA or the unwinding of double-stranded RNA. It is vital to RNA splicing, transport, editing, degradation and the initiation of protein translation. However, the function of RNA helicase in Medicago truncatula has rarely been reported. In this study, 170 putative RNA helicase genes were identified in the M. truncatula genome, and classified into three subfamilies based on the presence of either a DEAD-box (52 genes), DEAH-box (38 genes), or DExD/H-box (80 genes) in their coding regions. Additionally, conserved helicase_C domains and other functional domains (e.g., the HA2, DUF, and ZnF domains) were also present in these genes. Chromosomal mapping and synteny analyses showed that there were tandem and segment duplications of RNA helicase genes. Furthermore, transcriptome and real-time PCR analysis showed that the expression of 35 RNA helicase genes was affected by abiotic stress. To be specific, 17, 12 and 19 genes were regulated by salt, drought and cold stress, respectively. It is worth noting that MtDEAD8, MtDEAH3, MtDExD/H18 and MtDExD/H23 responded to all three types of stress. These results provide valuable information for understanding the RNA helicase genes in M. truncatula and their abiotic stress-related functions.
Similar content being viewed by others
References
Anja J, Ulf-Peter G, Eckhard J (2011) The RNA helicase database. Nucleic Acids Res 39:D338
Bateman A, Coggill P, Finn RD (2010) DUFs: families in search of function. Acta Crystallogr, Sect f: Struct Biol Cryst Commun 66:1148–1152
Chen C, Chen H, Zhang Y, Thomas HR, Frank MH, He Y, Xia R (2020) TBtools: an Integrative toolkit developed for interactive analyses of big biological data. Mol Plant 13:1194–1202
Chen J, Zhang Y, Liu J, Xia M, Wang W, Shen F (2014) Genome-wide analysis of the RNA helicase gene family in Gossypium raimondii. Int J Mol Sci 15:4635–4656
Dolferus R, Jacobs M, Peacock WJ, Dennis ES (1994) Differential interactions of promoter elements in stress responses of the arabidopsis adh gene. Plant Physiol 105:1075–1087
Fairman-Williams ME, Guenther UP, Jankowsky E (2010) SF1 and SF2 helicases: family matters. Curr Opin Struct Biol 20:313–324
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 82:309–318
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
He J, Benedito VA, Wang M, Murray JD, Zhao PX, Tang Y, Udvardi MK (2009) The medicago truncatula gene expression atlas web server. BMC Bioinformatics 10:441
Jankowsky E (2011) RNA helicases at work: binding and rearranging. Trends Biochem Sci 36:19–29
Khan A, Garbelli A, Grossi S, Florentin A, Batelli G, Acuna T, Zolla G, Kaye Y, Paul LK, Zhu JK (2014) The a rabidopsis STRESS RESPONSE SUPPRESSOR DEAD-box RNA helicases are nucleolar-and chromocenter-localized proteins that undergo stress-mediated relocalization and are involved in epigenetic gene silencing. Plant J 79:28–43
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 SJ, Ryu MY, Kim WT (2012) Suppression of arabidopsis RING-DUF1117 E3 ubiquitin ligases, AtRDUF1 and AtRDUF2, reduces tolerance to ABA-mediated drought stress. Biochem Biophys Res Commun 420:141–147
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 59:2133–2146
Liu C, Huang X (2015) Transcriptome-wide analysis of DEAD-box RNA helicase gene family in an Antarctic psychrophilic alga Chlamydomonas sp. ICE-l Extremophiles 19:921–931
Liu Y, Imai R (2018) Function of plant DExD/H-Box RNA helicases associated with ribosomal RNA biogenesis. Front Plant Sci 9:125
Lu CA, Huang CK, Huang WS, Huang TS, Liu HY, Chen YF (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
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
Nguyen L, Seok H-Y, Woo D-H, Lee S-Y, Moon Y-H (2018) Overexpression of the DEAD-Box RNA helicase gene AtRH17 confers tolerance to salt stress in arabidopsis. Int J Mol Sci 19:3777
Pandey S, Prasad A, Sharma N, Prasad M (2020) Linking the plant stress responses with RNA helicases. Plant Sci 299:110607
Patrick L, Owttrim GW (2009) Plant RNA helicases: linking aberrant and silencing RNA. Trends Plant Sci 14:344–352
Patterson C (2002) A new gun in town: the U box is a ubiquitin ligase domain. Sci Signaling 2002:pe4–pe4
Song J-J, Liu J, Tolia NH, Schneiderman J, Smith SK, Martienssen RA, Hannon GJ, Joshua-Tor L (2003) The crystal structure of the Argonaute2 PAZ domain reveals an RNA binding motif in RNAi effector complexes. Nat Struct Mol Biol 10:1026
Song J, Mo X, Yang H, Yue L, Song J, Mo B (2017) The U-box family genes in Medicago truncatula: key elements in response to salt, cold, and drought stresses. PLOS ONE 12:e0182402
Song JB, Wang YX, Li HB, Li BW, Zhou ZS, Gao S, Yang ZM (2015) The F-box family genes as key elements in response to salt, heavy mental, and drought stresses in Medicago truncatula. Funct Integr Genomics 15:495–507
Song L, Jiang L, Chen Y, Shu Y, Bai Y, Guo C (2016) Deep-sequencing transcriptome analysis of field-grown Medicago sativa L. crown buds acclimated to freezing stress. Funct Integr Genomics 16:495–511
Trapnell C, Pachter L, Salzberg SL (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25:1105–1111
Tuteja N, Banu MSA, Huda KMK, 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:e98287
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 73:449–465
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
Xing L, Zhao X, Niu M, Kleiman L (2014) Helicase associated 2 domain is essential for helicase activity of RNA helicase A. Biochimica et Biophys Acta (BBA)-Proteins Proteomics 1844:1757–1764
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:e78982
Xu R, Zhang S, Lu L, Cao H, Zheng C (2013b) A genome-wide analysis of the RNA helicase gene family in Solanum lycopersicum. Gene 513:128–140
Yang Q, Niu X, Tian X, Zhang X, Cong J, Wang R, Zhang G, Li G (2020) Comprehensive genomic analysis of the DUF4228 gene family in land plants and expression profiling of ATDUF4228 under abiotic stresses. BMC Genomics 21:12
Zhang XD, Sun JY, You YY, Song JB, Yang ZM (2018) Identification of Cd-responsive RNA helicase genes and expression of a putative BnRH 24 mediated by miR158 in canola (Brassica napus). Ecotoxicol Environ Saf 157:159–168
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
Acknowledgements
This study was financed by the National Natural Science Foundation of China (32060069), and Natural Science Foundation of Jiangxi Province (20202BABL205023).
Author information
Authors and Affiliations
Contributions
JC, SZ and KY carried out data collection and bioinformatics analysis. JC, SZ and RC performed the biological experiment. HY, LZ and HL prepared the plant sample. YW and JS designed the experiments and wrote the manuscript. All authors read and approved the final manuscript.
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
12298_2021_1087_MOESM1_ESM.docx
Supplemental Fig. 1. Evolutionary relationship analysis of RNA Helicases in Medicago truncatula, Arabidopsis thaliana, and Oryza sativa. (DOCX 542 KB)
12298_2021_1087_MOESM3_ESM.docx
Supplemental Table 2. Basic data of the DEAD-box, DEAH-box and DExD/H-box RNA helicase genes in the M. truncatula genome. (DOCX 62 KB)
Rights and permissions
About this article
Cite this article
Cheng, J., Zhou, S., Yang, K. et al. Identification of RNA helicases in Medicago truncatula and their expression patterns under abiotic stress. Physiol Mol Biol Plants 27, 2283–2296 (2021). https://doi.org/10.1007/s12298-021-01087-y
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12298-021-01087-y