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Ectopic expression of nucleolar DEAD-Box RNA helicase OsTOGR1 confers improved heat stress tolerance in transgenic Chinese cabbage

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The DEAD-Box RNA helicase OsTOGR1 positively regulates heat stress tolerance in Chinese cabbage.

Abstract

Non-heading Chinese cabbage (Brassica rapa L. ssp. chinensis) is primarily cultivated vegetable crop in Asian countries. Heat stress is one of the major threats for its growth and yield. Numerous regulatory genes in various crops have shown to contribute thermotolerance. Among them, Thermotolerant growth required 1 (TOGR1) is an important DEAD-box RNA helicase. To examine whether its role is conserved in other crops, we constructed pCAMBIA1300-pHSP:OsTOGR1 expression vector driven by the rice small heat shock protein promoter (pHSP17.9) and successfully produced transgenic non-heading Chinese cabbage plants expressing OsTOGR1 gene via Agrobacterium-mediated vacuum infiltration transformation. In total, we generated three independent transgenic cabbage lines expressing TOGR1 gene. Expression and integration of TOGR1 was confirmed by PCR, RT-PCR and qPCR in T1 and T2 generations. The relative leaf electrical conductivity of transgenic seedlings was reduced subjected to high temperature (38 °C) compared to heat shock treatment (46 °C). In addition, hypocotyl length of transgenic seedlings increased compared to wild-type plants under high temperature and heat shock treatment. Furthermore, the transgenic plants exhibited higher chlorophyll content than wild-type plants under high temperature and heat shock treatment. The transgenic seeds displayed better germination under heat shock treatment. Tested heat stress-responsive genes were also up-regulated in the transgenic plants subjected to high temperature or heat shock treatment. To the best of our knowledge, this is the first report on describing the role of DAED-Box RNA helicases in improving heat stress tolerance of transgenic plants.

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References

  • Ali S, Rizwan M, Arif MS, Ahmad R, Hasanuzzaman M, Ali B, Hussain A (2019) Approaches in enhancing thermotolerance in plants: an updated review. J Plant Growth Regul 12:1–25

    Google Scholar 

  • Angadi SV, Cutforth HW, Miller PR, McConkey B, Entz MH, Volkmar K, Brandt S (2000) Response of three Brassica species to high temperature injury during reproductive growth. Can J Plant Sci 80:693–701

    Google Scholar 

  • Augustine SM, Narayan JA, Syamaladevi DP, Appunu C, Chakarvarthi M, Ravichandran V, Tuteja N, Subramonian N (2015) Introduction of pea DNA helicase 45 into sugarcane (Saccharum spp. Hybrid) enhances cell membrane thermostability and upregulation of stress-responsive genes leads to abiotic stress tolerance. MolBiotechnol 57:475–488

    CAS  Google Scholar 

  • Barnabás B, Jäger K, Fehér A (2008) The effect of drought and heat stress on reproductive processes in cereals. Plant Cell Environ 31:11–38

    Google Scholar 

  • Baruah I, Debbarma J, Boruah HPD, Keshavaiah C (2017) The DEAD-box RNA helicases and multiple abiotic stresses in plants: a systematic review of recent advantages and challenges. Plant Omics J 10:252–262

    CAS  Google Scholar 

  • Bisbis MB, Gruda NS, Blanke MM (2019) Securing horticulture in a changing climate—a mini review. Horticulturae 5:56

    Google Scholar 

  • Bita CE, Gerats T (2013) Plant tolerance to high temperature in a changing environment: scientific fundamentals and production of heat stress-tolerant crops. Front Plant Sci 4:273

    Google Scholar 

  • Bouchez D, Camilleri C, Caboche M (1993) A binary vector based on Basta resistance for in situ transformation of Arabidopsis thaliana. CR AcadSci Paris Life Sci 316:1188–1193

    CAS  Google Scholar 

  • Chen S, Qiu G (2020) Overexpression of seagrass nucleotide exchange factor gene ZjFes1 enhances heat tolerance in transgenic Arabidopsis. Plant Signal Behav 15:2

    CAS  Google Scholar 

  • Driedonks N, Rieu I, Vriezen WH (2016) Breeding for plant heat tolerance at vegetative and reproductive stages. Plant Reprod 29(1–2):67–79

    CAS  Google Scholar 

  • Fahad S, Bajwa AA, Nazir U, Anjum SA, Farooq A, Zohaib A, Sadia S, Nasim W, Adkins S, Saud S, Ihsan MZ, Alharby H, Wu C, Wang D, Huang J (2017) Crop production under drought and heat stress: plant responses and management options. Front Plant Sci 8:1147

    Google Scholar 

  • Feldmann KA, Marks MD (1987) Agrobacterium-mediated transformation of germinating seeds of Arabidopsis thaliana: a nontissue culture approach. Mol Gen Genet 208:1–9

    CAS  Google Scholar 

  • Fragkostefanakis S, Roeth S, Schlei E, Scharf K (2015) Prospects of engineering thermotolerance in crops through modulation of heat stress transcription factor and heat shock protein networks. Plant Cell Environ 38:1881–1895

    CAS  Google Scholar 

  • Gangadhar BH, Sajeesh K, Venkatesh J, Baskar V, Abhinandan K, Yu JW, Prasad R, Mishra RK (2016) Enhanced tolerance of transgenic potato plants over-expressing non-specific lipid transfer protein-1 (StnsLTP1) against multiple abiotic stresses. Front Plant Sci 7:1228

    Google Scholar 

  • Grover A, Mittal D, Negi M, Lavania D (2013) Generating high temperature tolerant transgenic plants: achievements and challenges. Plant Sci 205–206:38–47

    Google Scholar 

  • Guan JC, Jinn TL, YehCH FSP, Chen YM, Lin CY (2004) Characterization of the genomic structures and selective expression profiles of nine class I small heat shockprotein genes clustered on two chromosomes in rice (Oryza sativa L.). Plant MolBiol 56:795–809

    CAS  Google Scholar 

  • Hasanuzzaman M, Nahar K, Alam MM, RoychowdhuryR FM (2013) Physiological, biochemical, and molecular mechanisms of heat stress tolerance in plants. Int J MolSci 14(5):9643–9684

    Google Scholar 

  • Hu D, Bent AF, Hou X, Li Y (2019) Agrobacterium-mediated vacuum infiltration and floral dip transformation of rapid-cycling Brassica rapa. BMC Plant Biol 19:246

    Google Scholar 

  • 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(1):174–191

    CAS  Google Scholar 

  • Huo L, Sun X, Guo Z, Jia X, Che R, Sun Y, Zhu Y, Wang P, Gong X, Ma F (2020) MdATG18a overexpression improves basal thermotolerance in transgenic apple by decreasing damage to chloroplasts. Hortic Res 7:21

    CAS  Google Scholar 

  • Jankowsky E (2011) RNA helicases at work: binding and rearranging. Trends BiochemSci 36(1):19–29

    CAS  Google Scholar 

  • Jiang J, Bai J, Li S, Li X, Yang L, He Y (2018) HTT2 promotes plant thermotolerance in Brassica rapa. BMC Plant Biol 18:127

    Google Scholar 

  • Kaushal N, Bhandari K, Siddique KHM, Nayyar H (2016) Food crops face rising temperatures: an overview of responses, adaptive mechanisms, and approaches to improve heat tolerance. Cogent Food Agric 2(1):1134380

    Google Scholar 

  • Lamaoui M, Jemo M, Datla R, Bekkaoui F (2018) Heat and drought stresses in crops and approaches for their mitigation. Front Chem 6:26

    Google Scholar 

  • Lavania D, Dhingra A, Siddiqui MH, Al-Whaibi MH, Grover A (2015) Current status of the production of high temperature tolerant transgenic crops for cultivation in warmer climates. Plant PhysiolBiochem 86:100–108

    CAS  Google Scholar 

  • Lesk C, Rowhani P, Ramankutty N (2016) Influence of extreme weather disasters on global crop production. Nature 529(7584):84–87

    CAS  Google Scholar 

  • Li XM, Chao DY, Wu Y, Huang X, Chen K, Cui LG, Su L, Ye WW, Chen H, Chen HC, Dong NQ, Guo T, Shi M, Feng Q, Zhang P, Han B, Shan JX, Gao JP, Lin HX (2015) Natural alleles of a proteasome α2 subunit gene contribute to thermotolerance and adaptation of African rice. Nat Genet 47:827–833

    CAS  Google Scholar 

  • Lin JS, Kuo CC, Yang IC, Tsai WA, Shen YH, Lin CC, Liang YC, Li YC, Kuo YW, King YC, Lai HM, Jeng ST (2018) MicroRNA160 modulates plant development and heat shock protein gene expression to mediate heat tolerance in Arabidopsis. Front Plant Sci 9:68

    Google Scholar 

  • Liu Y, Imai R (2018) Function of plant DExD/H-box RNA helicases associated with ribosomal RNA biogenesis. Front Plant Sci 9:125

    Google Scholar 

  • Liu H, Li H, Zhang H, Li J, Xie B, Xu J (2016) The expansin gene PttEXPA8frompoplar (Populustomentosa) confers heat resistance in transgenic tobacco. Plant Cell Tiss Organ Cult 126:353–359

    CAS  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays of tobacco tissue cultures. Physiol Plant 15:473–497

    CAS  Google Scholar 

  • Narasimhulu SB, Chopra VL (1988) Species specific shoot regeneration response of cotyledonary explants of Brassicas. Plant Cell Rep 7:104–106

    CAS  Google Scholar 

  • Nguyen LV, Seok HY, Woo DH, Lee SY, Moon YH (2018) Overexpression of the DEAD-box RNA helicase gene AtRH17 confers tolerance to salt stress in Arabidopsis. Int J MolSci 19(12):3777

    Google Scholar 

  • Nidumukkala S, Tayi L, Chittela RK, Vudem DR, Khareedu VR (2019) DEAD box helicases as promising molecular tools for engineering abiotic stress tolerance in plants. Crit Rev Biotech 39(3):395–407

    CAS  Google Scholar 

  • Qing CM, Fan L, Lei Y, Bouchez D, Tourneur C, Yan L, Robaglia C (2000) Transformation of Pakchoi (Brassica rapa L. ssp. chinensis) by Agrobacterium infiltration. Mol Breed 6:67–72

    CAS  Google Scholar 

  • Sanan-Mishra N, Pham XH, Sopory SK, Tuteja N (2005) Pea DNA helicase 45 overexpression in tobacco confers high salinity tolerance without affecting yield. ProcNatlAcadSci USA 102:509–514

    CAS  Google Scholar 

  • Scheelbeek PFD, Bird FA, Tuomisto HL, Green R, Harris FB, Joy EJM, Chalabi Z, Allen E, Haines A, Dangour AD (2018) Effect of environmental changes on vegetable and legume yields and nutritional quality. ProcNatlAcadSci USA 115(26):6804–6809

    CAS  Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Silva-Correia J, Freitas S, Tavares RM, Lino-Neto T, Azevedo H (2014) Phenotypic analysis of the Arabidopsis heat stress response during germination and early seedling development. Plant Methods 10(1):7

    Google Scholar 

  • Singh B, Salaria N, Thakur K, Kukreja S, Gautam S, Gautam U (2019) Functional genomicapproaches to improve crop plant heat stress tolerance. F1000Research 8:1721

    CAS  Google Scholar 

  • Singha DL, Tuteja N, Boro D, Hazarika GN, Singh S (2017a) Heterologous expression of PDH47 confers drought tolerance in indica rice. Plant Cell Tiss Org Cult 130(3):577–589

    CAS  Google Scholar 

  • Singha DL, Tuteja N, Boro D, Hazarika GN, Singh S (2017b) Heterologous expression of PDH47 confers drought tolerance in indica rice. Plant Cell Tiss Organ Cult 130:577–589

    CAS  Google Scholar 

  • Song XM, Li Y, Liu TK, Duan WK, Huang ZN, Wang L, Tan H, Hou X (2014) Genes associated with agronomic trats in non-heading Chinese cabbage identified by expression profiling. BMC Plant Biol 14:71

    Google Scholar 

  • Suzuki N, Katano K (2018) Coordination between ROS regulatory systems and other pathways under heat stress and pathogen attack. Front Plant Sci 9:490

    Google Scholar 

  • Tubiello FN, Soussana JF, Howden SM (2007) Crop and pasture response to climate change. ProcNatlAcadSci USA 104:19686–19690

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • Wang D, Qin B, Li X, Tang D, Zhnag Y, Cheng Z, Xue YB (2016) Nucleolar DEAD-box RNA helicase TOGR1 regulates thermotolerant growth as a pre-rRNA chaperone in rice. Plos Genet 12:e1005844

    Google Scholar 

  • Wang A, Hu J, Huang X, Li X, Zhou G, Yan Z (2016b) Comparative transcriptome analysis reveals heat-responsive genes in Chinese cabbage (Brassica rapa ssp. chinensis). Front Plant Sci 7:939

    Google Scholar 

  • Wang G, Cai G, Xu N, Zhang L, Sun X, Guan J, Meng Q (2019) Novel DnaJ protein facilitates thermotolerance of transgenic tomatoes. Int J MolSci 20(2):367

    Google Scholar 

  • Xu H, Wang X, Zhao H, Liu F (2008) An intensive understanding of vacuum infiltrationtransformation of pakchoi (Brassica rapasspchinensis). Plant Cell Rep 27:1369–1376

    CAS  Google Scholar 

  • Xu Y, Ramanathan V, Victor DG (2018) Global warming will happen faster than we think. Nature 564:30–32

    CAS  Google Scholar 

  • Yu X, Wang H, Lu YZ, Ruiter MD, Caraso M, Prins M, Van Tunen A, He Y (2012) Identification of conserved and novel microRNAs that are responsive to heat stress in Brassica rapa. J Exp Bot 63:1025–1038

    CAS  Google Scholar 

  • Zhang FL, Takahata Y, Watanabe M (2000) Agrobacterium-mediated transformation of cotyledonary explants of Chinese cabbage (Brassica campestris L. ssp. pekinensis). Plant Cell Rep 19:569–575

    Google Scholar 

  • Zhang J, Liu F, Yao L, Luo C, Zhao Q, Huang Y (2011) Vacuum infiltration transformation of non-heading Chinese cabbage (Brassica rapa L sspchinensis) with the pinII gene and bioassay for diamondback moth resistance. Plant Biotechnol Rep 5:217

    CAS  Google Scholar 

  • Zhang J, Chen H, Wang H, Li B, Yi Y, Kong F, Liu J, Zhang H (2016) Constitutiveexpression of a tomato small heat shock protein gene LeHSP21 improves tolerance tohigh-temperature stress by enhancing antioxidation capacity in tobacco. Plant MolBiol Rep 34:399–409

    CAS  Google Scholar 

  • Zhang J, Li XM, Lin HX, Chong K (2019) Crop improvement through temperature resilience. Ann Rev Plant Bio 70(1):753–780

    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

    Google Scholar 

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Acknowledgements

We thank Dr. Liu Fan, Beijing Vegetable Research Centre, Beijing, China for generous help in providing the seeds used in this study. Authors also thank Dr. Yue Zhang, Dr. Huashan Tang, Dr. Liu Zheng and Mr. Pengfei Wang for their help throughout this research.

Funding

This work has been financially supported by the Chinese Academy of Sciences, Beijing, China in the form of postdoctoral fellowship (Grant No. 2017PB0039) granted to RY.

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YX and RY conceived and designed the study. RY performed the experiments and analyzed the data. YX and RY drafted the manuscript. All authors read and approved the final manuscript.

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Correspondence to Yongbiao Xue.

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Communicated by Günther Hahne.

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Yarra, R., Xue, Y. Ectopic expression of nucleolar DEAD-Box RNA helicase OsTOGR1 confers improved heat stress tolerance in transgenic Chinese cabbage. Plant Cell Rep 39, 1803–1814 (2020). https://doi.org/10.1007/s00299-020-02608-x

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