Picea wilsonii NAC Transcription Factor PwNAC30 Negatively Regulates Abiotic Stress Tolerance in Transgenic Arabidopsis

Abstract

NAC (NAM, ATAF1/2, and CUC2) transcription factors play important roles in the process of abiotic stress response in plants. However, little is known about the functional roles of NACs in Picea (P.) wilsonii. In this study, we functionally characterized a novel P. wilsonii NAC transcription factor PwNAC30 by heterologous expression in Arabidopsis. The results showed that PwNAC30 is mainly localized in the nucleus by transient expression in Nicotiana benthamiana and can function as a nuclear localization transcription factor. β-Glucuronidase (GUS) staining in transgenic Arabidopsis (PwNAC30-promoter-GUS) confirmed the expression pattern of PwNAC30 throughout the plant development process, which is expressed in most of the plant tissues except stamens and petals. Overexpression of PwNAC30 in Arabidopsis significantly repressed the tolerance of seedlings and mature plants to both drought and salt stresses, while exerting no influence on growth and development of plants. The accumulation of reactive oxygen species (ROS) was significantly increased in transgenic plants, and the expression of some stress-responsive genes was obviously inhibited in PwNAC30 overexpression lines. Our study reveals that PwNAC30 functions as a negative regulator of plant tolerance to drought or salt stress, which provides new insights into abiotic tolerance mechanisms in woody plants.

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References

  1. An JP, Li R, Qu FJ, You CX, Wang XF, Hao YJ (2018) An apple NAC transcription factor negatively regulates cold tolerance via CBF-dependent pathway. J Plant Physiol 221:74–80. https://doi.org/10.1016/j.jplph.2017.12.009

    CAS  Article  PubMed  Google Scholar 

  2. An JP, Yao JF, Xu RR, You CX, Wang XF, Hao YJ (2019) An apple NAC transcription factor enhances salt stress tolerance by modulating the ethylene response. Physiol Plant 166:472–472. https://doi.org/10.1111/ppl.12695

    CAS  Article  Google Scholar 

  3. Baxter A, Mittler R, Suzuki N (2014) ROS as key players in plant stress signalling. J Exp Bot 65:1229–1240. https://doi.org/10.1093/jxb/ert375

    CAS  Article  PubMed  Google Scholar 

  4. Deng YW, Zhai K, Xie Z, Yang D, Zhu X, Liu J, Wang X, Qin P, Yang Y, Zhang G, Li Q, Zhang J, Wu S, Milazzo J, Mao B, Wang E, Xie H, Tharreau D, He Z (2017) Epigenetic regulation of antagonistic receptors confers rice blast resistance with yield balance. Science 355:962–965. https://doi.org/10.1126/science.aai8898

    CAS  Article  PubMed  Google Scholar 

  5. Ding AQ et al (2019) RhNAC31, a novel rose NAC transcription factor, enhances tolerance to multiple abiotic stresses in Arabidopsis. Acta Physiologiae Plantarum 41(6):75. https://doi.org/10.1007/s11738-019-2866-1

    CAS  Article  Google Scholar 

  6. Fang YJ, You J, Xie KB, Xie WB, Xiong LZ (2008) Systematic sequence analysis and identification of tissue-specific or stress-responsive genes of NAC transcription factor family in rice. Mol Gen Genomics 280:547–563. https://doi.org/10.1007/s00438-008-0386-6

    CAS  Article  Google Scholar 

  7. Fujita M, Fujita Y, Maruyama K, Seki M, Hiratsu K, Ohme-Takagi M, Tran LSP, Yamaguchi-Shinozaki K, Shinozaki K (2004) A dehydration-induced NAC protein, RD26, is involved in a novel ABA-dependent stress-signaling pathway. Plant J 39:863–876. https://doi.org/10.1111/j.1365-313X.2004.02171.x

    CAS  Article  PubMed  Google Scholar 

  8. Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930. https://doi.org/10.1016/j.plaphy.2010.08.016

    CAS  Article  Google Scholar 

  9. Guilfoyle TJ (1997) The structure of plant gene promoters. Genet Eng 19. https://doi.org/10.1007/978-1-4615-5925-2_2

  10. Guo P, Li Z, Huang P, Li B, Fang S, Chu J, Guo H (2017) A tripartite amplification loop involving the transcription factor WRKY75, salicylic acid, and reactive oxygen species accelerates leaf senescence. Plant Cell 29:2854–2870. https://doi.org/10.1105/tpc.17.00438

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  11. Han DG, Hou YJ, Wang YF, Ni BX, Li ZT, Yang GH (2019) Overexpression of a Malus baccata WRKY transcription factor gene (MbWRKY5) increases drought and salt tolerance in transgenic tobacco. Can J Plant Sci 99:173–183. https://doi.org/10.1139/cjps-2018-0053

    CAS  Article  Google Scholar 

  12. Hao YJ, Song QX, Chen HW, Zou HF, Wei W, Kang XS, Ma B, Zhang WK, Zhang JS, Chen SY (2010) Plant NAC-type transcription factor proteins contain a NARD domain for repression of transcriptional activation. Planta 232:1033–1043. https://doi.org/10.1007/s00425-010-1238-2

    CAS  Article  PubMed  Google Scholar 

  13. Hao YJ, Wei W, Song QX, Chen HW, Zhang YQ, Wang F, Zou HF, Lei G, Tian AG, Zhang WK, Ma B, Zhang JS, Chen SY (2011) Soybean NAC transcription factors promote abiotic stress tolerance and lateral root formation in transgenic plants. Plant Journal for Cell & Molecular Biology 68:302–313. https://doi.org/10.1111/j.1365-313x.2011.04687.x

    CAS  Article  Google Scholar 

  14. He K, Zhao X, Chi X, Wang Y, Jia C, Zhang H, Zhou G, Hu R (2019) A novel Miscanthus NAC transcription factor MlNAC10 enhances drought and salinity tolerance in transgenic Arabidopsis. J Plant Physiol 233:84–93. https://doi.org/10.1016/j.jplph.2019.01.001

    CAS  Article  PubMed  Google Scholar 

  15. Hellens RP, Allan AC, Friel EN, Bolitho K, Grafton K, Templeton MD, Karunairetnam S, Gleave AP, Laing WA (2005) Transient expression vectors for functional genomics, quantification of promoter activity and RNA silencing in plants. Plant Methods 1:13–13. https://doi.org/10.1186/1746-4811-1-13

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  16. Hu P, Zhang KM, Yang CP (2019) BpNAC012 positively regulates abiotic stress responses and secondary wall biosynthesis. Plant Physiol 179:700–717. https://doi.org/10.1104/pp.18.01167

    CAS  Article  PubMed  Google Scholar 

  17. Huang L, Hong YB, Zhang HJ, Li DY, Song FM (2016) Rice NAC transcription factor ONAC095 plays opposite roles in drought and cold stress tolerance. Bmc Plant Biology 16:203. https://doi.org/10.1186/s12870-016-0897-y

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  18. Jensen MK, Hagedorn PH, de Torres-Zabala M, Grant MR, Rung JH, Collinge DB, Lyngkjaer MF (2008) Transcriptional regulation by an NAC (NAM-ATAF1,2-CUC2) transcription factor attenuates ABA signalling for efficient basal defence towards Blumeria graminis f. sp hordei in Arabidopsis. Plant J 56:867–880. https://doi.org/10.1111/j.1365-313X.2008.03646.x

    CAS  Article  PubMed  Google Scholar 

  19. Jin C et al (2017) A novel NAC transcription factor, PbeNAC1, of Pyrus betulifolia confers cold and drought tolerance via interacting with PbeDREBs and activating the expression of stress-responsive genes. Frontiers Plant Sci 8:1049. https://doi.org/10.3389/fpls.2017.01049

    Article  Google Scholar 

  20. Katiyar-Agarwal S, Zhu J, Kim K, Agarwal M, Fu X, Huang A, Zhu JK (2006) The plasma membrane Na+/H+ antiporter SOS1 interacts with RCD1 and functions in oxidative stress tolerance in Arabidopsis. Proc Natl Acad Sci U S A 103:18816–18821. https://doi.org/10.1073/pnas.0604711103

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  21. Kehao L, Yongjiang S, Yihang Y, Lingyun Z (2019) Cloning and analysis of a transcription factor PwNAC30 and the promoter sequence in Picea wilsonii. Acta Botanica Boreali-Occidentalia Sinica 39:17–28 CNKI:SUN:DNYX.0.2019-01-002

    Google Scholar 

  22. Kurepin LV, Dahal K, Savitch L, Singh J, Bode R, Ivanov A, Hurry V, Hüner N (2013) Role of CBFs as integrators of chloroplast redox, phytochrome and plant hormone signaling during cold acclimation. Int J Mol Sci 14:12729–12763. https://doi.org/10.3390/ijms140612729

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  23. Lee DK, Chung PJ, Jeong JS, Jang G, Bang SW, Jung H, Kim YS, Ha SH, Choi YD, Kim JK (2017) The rice OsNAC6 transcription factor orchestrates multiple molecular mechanisms involving root structural adaptions and nicotianamine biosynthesis for drought tolerance. Plant Biotechnol J 15:754–764. https://doi.org/10.1111/pbi.12673

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  24. Li S, Wang N, Ji D, Zhang W, Wang Y, Yu Y, Zhao S, Lyu M, You J, Zhang Y, Wang L, Wang X, Liu Z, Tong J, Xiao L, Bai MY, Xiang F (2019) A GmSIN1/GmNCED3s/GmRbohBs feed-forward loop acts as a signal amplifier that regulates root growth in soybean exposed to salt stress. Plant Cell 31:9–2130. https://doi.org/10.1105/tpc.18.00662

    CAS  Article  Google Scholar 

  25. Liu B et al (2014a) Tomato NAC transcription factor SlSRN1 positively regulates defense response against biotic stress but negatively regulates abiotic stress response. Plos One 9:7. ARTN e102067. https://doi.org/10.1371/journal.pone.0102067

  26. Liu J, Xu X, Xu Q, Wang SH, Xu JC (2014b) Transgenic tobacco plants expressing PicW gene from Picea wilsonii exhibit enhanced freezing tolerance. Plant Cell Tiss Org 118:391–400. https://doi.org/10.1007/s11240-014-0491-7

    CAS  Article  Google Scholar 

  27. Liu C, Wang BM, Li ZX, Peng ZH, Zhang JR (2018a) TsNAC1 is a key transcription factor in abiotic stress resistance and growth. Plant Physiol 176:742–756. https://doi.org/10.1104/pp.17.01089

    CAS  Article  PubMed  Google Scholar 

  28. Liu Q, Yan S, Huang W, Yang J, Dong J, Zhang S, Zhao J, Yang T, Mao X, Zhu X, Liu B (2018b) NAC transcription factor ONAC066 positively regulates disease resistance by suppressing the ABA signaling pathway in rice. Plant Mol Biol 98:289–302. https://doi.org/10.1007/s11103-018-0768-z

    CAS  Article  PubMed  Google Scholar 

  29. Liu Y, Wei H, Ma M, Li Q, Kong D, Sun J, Ma X, Wang B, Chen C, Xie Y, Wang H (2019) Arabidopsis FHY3 and FAR1 proteins regulate the balance between growth and defense responses under shade conditions. Plant Cell 31:2089–2106. https://doi.org/10.1105/tpc.18.00991

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  30. Lu PL, Chen NZ, An R, Su Z, Qi BS, Ren F, Chen J, Wang XC (2007) A novel drought-inducible gene, ATAF1, encodes a NAC family protein that negatively regulates the expression of stress-responsive genes in Arabidopsis. Plant Mol Biol 63:289–305. https://doi.org/10.1007/s11103-006-9089-8

    CAS  Article  PubMed  Google Scholar 

  31. Meng XX, Li L, de Clercq I, Narsai R, Xu Y, Hartmann A, Claros DL, Custovic E, Lewsey MG, Whelan J, Berkowitz O (2019) ANAC017 coordinates organellar functions and stress responses by reprogramming retrograde signaling. Plant Physiol 180:634–653. https://doi.org/10.1104/pp.18.01603

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  32. Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell and Environment 33:453–467. https://doi.org/10.1111/j.1365-3040.2009.02041.x

    CAS  Article  Google Scholar 

  33. Moore K, Roberts LJ (1998) Measurement of lipid peroxidation. Free Radical Research Communications 28:659–671. https://doi.org/10.3109/10715769809065821

    CAS  Article  Google Scholar 

  34. Nakashima A, Chen L, Thao NP, Fujiwara M, Wong HL, Kuwano M, Umemura K, Shirasu K, Kawasaki T, Shimamoto K (2008) RACK1 functions in rice innate immunity by interacting with the rac1 immune complex. Plant Cell 20:2265–2279. https://doi.org/10.1105/tpc.107.054395

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  35. Nguyen KH, Mostofa MG, Li W, van Ha C, Watanabe Y, le DT, Thao NP, Tran LSP (2018) The soybean transcription factor GmNAC085 enhances drought tolerance in Arabidopsis. Environ Exp Bot 151:12–20. https://doi.org/10.1016/j.envexpbot.2018.03.017

    CAS  Article  Google Scholar 

  36. Nguyen KH, Mostofa MG, Watanabe Y, Tran CD, Rahman MM, Tran LSP (2019) Overexpression of GmNAC085 enhances drought tolerance in Arabidopsis by regulating glutathione biosynthesis, redox balance and glutathione-dependent detoxification of reactive oxygen species and methylglyoxal. Environ Exp Bot 161:242–254. https://doi.org/10.1016/j.envexpbot.2018.12.021

    CAS  Article  Google Scholar 

  37. Oda-Yamamizo C, Mitsuda N, Sakamoto S, Ogawa D, Ohme-Takagi M, Ohmiya A (2016) The NAC transcription factor ANAC046 is a positive regulator of chlorophyll degradation and senescence in Arabidopsis leaves. Scientific Reports 6:23609. https://doi.org/10.1038/srep23609

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  38. Sakuma Y, Maruyama K, Osakabe Y, Qin F, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2006) Functional analysis of an Arabidopsis transcription factor, DREB2A, involved in drought-responsive gene expression. Plant Cell 18:1292–1309. https://doi.org/10.1105/tpc.105.035881

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  39. Seo JJ et al (2010) Root-specific expression of OsNAC10 improves drought tolerance and grain yield in rice under field drought conditions. Plant Physiol 153:185–197. https://doi.org/10.1104/pp.110.154773

    CAS  Article  Google Scholar 

  40. Seok H-Y, Woo DH, Nguyen LV, Tran HT, Tarte VN, Mehdi SMM, Lee SY, Moon YH (2016) Arabidopsis AtNAP functions as a negative regulator via repression of AREB1 in salt stress response. Planta 245:329–341. https://doi.org/10.1007/s00425-016-2609-0

    CAS  Article  PubMed  Google Scholar 

  41. Shapiguzov A et al (2019) Arabidopsis RCD1 coordinates chloroplast and mitochondrial functions through interaction with ANAC transcription factors. Elife 8:e43284. https://doi.org/10.7554/eLife.43284

    Article  PubMed  PubMed Central  Google Scholar 

  42. Shen H, Yin YB, Chen F, Xu Y, Dixon RA (2009) A bioinformatic analysis of NAC genes for plant cell wall development in relation to lignocellulosic bioenergy production. Bioenergy Research 2:217–232. https://doi.org/10.1007/s12155-009-9047-9

    Article  Google Scholar 

  43. Shen J, Lv B, Luo L, He J, Mao C, Xi D, Ming F (2017) The NAC-type transcription factor OsNAC2 regulates ABA-dependent genes and abiotic stress tolerance in rice. Sci Rep 7:40641. https://doi.org/10.1038/srep40641

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  44. Sukiran N, Ma J, Ma H, Su Z (2019) ANAC019 is required for recovery of reproductive development under drought stress in Arabidopsis. Plant Mol Biol 99:161–174. https://doi.org/10.1007/s11103-018-0810-1

    CAS  Article  PubMed  Google Scholar 

  45. Tiancong Q et al (2015) Regulation of jasmonate-induced leaf senescence by antagonism between bHLH subgroup IIIe and IIId factors in Arabidopsis. Plant Cell 27:1634–1649. https://doi.org/10.1105/tpc.15.00110

    CAS  Article  Google Scholar 

  46. Tran L-SP, Nakashima K, Sakuma Y, Simpson SD, Fujita Y, Maruyama K, Fujita M, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2004) Isolation and functional analysis of Arabidopsis stress-inducible NAC transcription factors that bind to a drought-responsive cis-element in the early responsive to dehydration stress 1 promoter. Plant Cell 16:2481–2498. https://doi.org/10.1105/tpc.104.022699

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  47. Tsai SJ, Yin MC (2008) Antioxidative and anti-inflammatory protection of oleanolic acid and ursolic acid in PC12 cells. J Food Sci 73:H174–H178. https://doi.org/10.1111/j.1750-3841.2008.00864.x

    CAS  Article  PubMed  Google Scholar 

  48. Wang LQ, Li Z, Lu MZ, Wang YC (2017) ThNAC13, a NAC transcription factor from Tamarix hispida, confers salt and osmotic stress tolerance to transgenic Tamarix and Arabidopsis. Frontiers in Plant Science 8:635. https://doi.org/10.3389/fpls.2017.00635

    Article  PubMed  PubMed Central  Google Scholar 

  49. Wang JF et al (2018) Overexpression of BoNAC019, a NAC transcription factor from Brassica oleracea, negatively regulates the dehydration response and anthocyanin biosynthesis in Arabidopsis. Sci Rep-Uk 8:13349. https://doi.org/10.1038/s41598-018-31690-1

    CAS  Article  Google Scholar 

  50. Wei QH et al (2017) A wheat R2R3-type MYB transcription factor TaODORANT1 positively regulates drought and salt stress responses in transgenic tobacco plants. Frontiers in Plant Science 8:1374. https://doi.org/10.3389/fpls.2017.01374

    Article  PubMed  PubMed Central  Google Scholar 

  51. Wu R, Duan LN, Pruneda-Paz JL, Oh DH, Pound M, Kay S, Dinneny JR (2018) The 6xABRE synthetic promoter enables the spatiotemporal analysis of ABA-mediated transcriptional regulation. Plant Physiol 177:1650–1665. https://doi.org/10.1104/pp.18.00401

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  52. Wu JD, Jiang YL, Liang YN, Chen L, Chen WJ, Cheng BJ (2019) Expression of the maize MYB transcription factor ZmMYB3R enhances drought and salt stress tolerance in transgenic plants. Plant Physiol Biochem 137:179–188. https://doi.org/10.1016/j.plaphy.2019.02.010

    CAS  Article  PubMed  Google Scholar 

  53. Xiong HY, Yu J, Miao J, Li J, Zhang H, Wang X, Liu P, Zhao Y, Jiang C, Yin Z, Li Y, Guo Y, Fu B, Wang W, Li Z, Ali J, Li Z (2018) Natural variation in OsLG3 increases drought tolerance in rice by inducing ROS scavenging. Plant Physiol 178:451–467. https://doi.org/10.1104/pp.17.01492

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  54. Xu GY et al (2017) uORF-mediated translation allows engineered plant disease resistance without fitness costs. Nature 545:491. https://doi.org/10.1038/nature22372

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  55. Xu XY, Yao XZ, Lu LT, Zhao DG (2018) Overexpression of the transcription factor NtNAC2 confers drought tolerance in tobacco. Plant Mol Biol Report 36:543–552. https://doi.org/10.1007/s11105-018-1096-9

    CAS  Article  Google Scholar 

  56. Yang SD, Seo PJ, Yoon HK, Park CM (2011) The Arabidopsis NAC transcription factor VNI2 integrates abscisic acid signals into leaf senescence via the COR/RD genes. Plant Cell 23:2155–2168. https://doi.org/10.1105/tpc.111.084913

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  57. Yang X, Wang X, Ji L, Yi Z, Fu C, Ran J, Hu R, Zhou G (2015) Overexpression of a Miscanthus lutarioriparius NAC gene MlNAC5 confers enhanced drought and cold tolerance in Arabidopsis. Plant Cell Rep 34:943–958. https://doi.org/10.1007/s00299-015-1756-2

    CAS  Article  PubMed  Google Scholar 

  58. Yang XW, He K, Chi X, Chai G, Wang Y, Jia C, Zhang H, Zhou G, Hu R (2018) Miscanthus NAC transcription factor MlNAC12 positively mediates abiotic stress tolerance in transgenic Arabidopsis. Plant Sci 277:229–241. https://doi.org/10.1016/j.plantsci.2018.09.013

    CAS  Article  PubMed  Google Scholar 

  59. Yong Y, Zhang Y, Lyu Y (2019) A stress-responsive NAC transcription factor from tiger lily (LlNAC2) interacts with LlDREB1 and LlZHFD4 and enhances various abiotic stress tolerance in Arabidopsis. Int J Mol Sci 20:3225. https://doi.org/10.3390/ijms20133225

    CAS  Article  PubMed Central  Google Scholar 

  60. Yu YL, Li Y, Huang G, Meng Z, Zhang D, Wei J, Yan K, Zheng C, Zhang L (2011) PwHAP5, a CCAAT-binding transcription factor, interacts with PwFKBP12 and plays a role in pollen tube growth orientation in Picea wilsonii. J Exp Bot 62:4805–4817. https://doi.org/10.1093/jxb/err120

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  61. Yuan X, Wang H, Cai JT, Bi Y, Li DY, Song FM (2019) Rice NAC transcription factor ONAC066 functions as a positive regulator of drought and oxidative stress response. Bmc Plant Biology 19(1):278. https://doi.org/10.1186/s12870-019-1883-y

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  62. Zhang T, Zhang D, Liu Y, Luo C, Zhou Y, Zhang L (2015) Overexpression of a NF-YB3 transcription factor from Picea wilsonii confers tolerance to salinity and drought stress in transformed Arabidopsis thaliana. Plant Physiology & Biochemistry 94:153–164. https://doi.org/10.1016/j.plaphy.2015.05.001

    CAS  Article  Google Scholar 

  63. Zhang S, Li C, Wang R, Chen Y, Shu S, Huang R, Zhang D, Li J, Xiao S, Yao N, Yang C (2017) The Arabidopsis mitochondrial protease FtSH4 is involved in leaf senescence via regulation of WRKY-dependent salicylic acid accumulation and signaling. Plant Physiol 173:2294–2307. https://doi.org/10.1104/pp.16.00008

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  64. Zhang B, Guo GX, Lu F, Song Y, Liu Y, Xu JC, Gao W (2018a) PicW2 from Picea wilsonii: preparation, purification, crystallization and X-ray diffraction analysis. Acta Crystallogr F 74:363–366. https://doi.org/10.1107/S2053230x18007537

    CAS  Article  Google Scholar 

  65. Zhang HH, Cui XY, Guo YX, Luo CB, Zhang LY (2018b) Picea wilsonii transcription factor NAC2 enhanced plant tolerance to abiotic stress and participated in RFCP1-regulated flowering time. Plant Mol Biol 98:471–493. https://doi.org/10.1007/s11103-018-0792-z

    CAS  Article  PubMed  Google Scholar 

  66. Zhang XW, Chen LT, Wang JR, Wang MH, Yang SL, Zhao CM (2018c) Photosynthetic acclimation to long-term high temperature and soil drought stress in two spruce species (Picea crassifolia and P-wilsonii) used for afforestation. J For Res 29:363–372. https://doi.org/10.1007/s11676-017-0468-6

    CAS  Article  Google Scholar 

  67. Zhang XM, Cheng ZH, Zhao K, Yao WJ, Sun XM, Jiang TB, Zhou BR (2019) Functional characterization of poplar NAC13 gene in salt tolerance. Plant Sci 281:1–8. https://doi.org/10.1016/j.plantsci.2019.01.003

    CAS  Article  PubMed  Google Scholar 

  68. Zhu B, Huo DA, Hong XX, Guo J, Peng T, Liu J, Huang XL, Yan HQ, Weng QB, Zhang XC, du XY (2019a) The Salvia miltiorrhiza NAC transcription factor SmNAC1 enhances zinc content in transgenic Arabidopsis. Gene 688:54–61. https://doi.org/10.1016/j.gene.2018.11.076

    CAS  Article  PubMed  Google Scholar 

  69. Zhu Z, Li G, Yan C, Liu L, Zhang Q, Han Z, Li B (2019b) DRL1, encoding a NAC transcription factor, is involved in leaf senescence in grapevine. Int J Mol Sci 20:11. https://doi.org/10.3390/ijms20112678

    CAS  Article  Google Scholar 

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Acknowledgments

We thank Professor Dapeng Zhang (College of Life Sciences, Tsinghua University) for providing the pCAMBIA1205 vector and pBI121 vector.

Funding

This research was funded by a grant from the Agricultural Ministry of China, grant number 2016ZX08009-003.

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LZ and KL conceived the project and designed the experiments; LZ collected the samples; KL, YY, YM, and AW performed the experiments; KL conducted the data analysis and drafted the manuscript; LZ revised the manuscript. All authors read and approved the final manuscript.

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Correspondence to Ling-yun Zhang.

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Key Message

The function of PwNAC30, which is identified from Picea wilsonii, is characterized by heterologous expression in Arabidopsis. Our results demonstrated that PwNAC30, as a nuclear localization transcription factor, plays a negative role in drought and salt stress response in plants; moreover, the inhibition mechanism of tolerance to abiotic stress in transgenic plants is achieved by the accumulation of reactive oxygen species (ROS) and the downregulation of stress-related genes.

Electronic Supplementary Material

Table S1

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Fig. S1

Detection of PwNAC30 in transcription Arabidopsis. (a) Validation of PwNAC30 by RT-PCR. (b) The relative expression level of PwNAC30 in transgenic plants. WT, wild-type; NC, plant lines transformed with empty vectors; OE-2 and OE-4, transgenic lines of PwNAC30 overexpression. For qRT-PCR, AtActin was used as reference gene. Each value is the mean value ± SE of three independent determinations, and different letters indicate significant differences at P < 0.05 by Duncan’s multiple range test (PNG 1640 kb)

Fig. S2

Growth characteristics of PwNAC30 overexpression lines. (a, e) Plant heights of OE lines, WT and NC plants under normal growth condition. (b) Detached rosette leaves of OE lines, WT and NC plants under normal growth condition. (c) Flower organs of OE lines, WT and NC plants under normal growth condition. (d, f) Maturing siliques of OE lines, WT and NC plants. (g) Flowering times of OE lines, WT and NC plants under normal growth condition (WT, wild-type; NC, plant lines transformed with empty vectors; OE-2 and OE-4, transgenic lines of PwNAC30 overexpression). Each value is the mean value ± standard error of three independent determinations, and different letters indicate significant differences at P < 0.05 by Duncan’s multiple range test (PNG 6033 kb)

Fig. S3

Effects of exogenous ABA on the activity of the promoter. (a) GUS activity driven by the promoter of PwNAC30 under different concentrations of exogenous ABA. (b) Analysis of the PwNAC30 promoter under different ABA treatments through dual-luciferase reporter assay (PC, 35S-GUS, empty pBI121 vector transformed into N. benthamiana leaves; NC, N. benthamiana injected with buffer solution). Each value is the mean value ± standard error of three independent determinations, and different letters indicate significant differences at P < 0.05 by Duncan’s multiple range test (PNG 4144 kb)

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Liang, Kh., Wang, Ab., Yuan, Yh. et al. Picea wilsonii NAC Transcription Factor PwNAC30 Negatively Regulates Abiotic Stress Tolerance in Transgenic Arabidopsis. Plant Mol Biol Rep 38, 554–571 (2020). https://doi.org/10.1007/s11105-020-01216-z

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Keywords

  • Picea wilsonii
  • Transcription factor
  • PwNAC30
  • Abiotic stress