Skip to main content
Log in

The transcription factor VaNAC17 from grapevine (Vitis amurensis) enhances drought tolerance by modulating jasmonic acid biosynthesis in transgenic Arabidopsis

  • Original Article
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

Key message

Expression of VaNAC17 improved drought tolerance in transgenic Arabidopsis by upregulating stress-responsive genes, modulating JA biosynthesis, and enhancing ROS scavenging.

Abstract

Water deficit severely affects the growth and development of plants such as grapevine (Vitis spp.). Members of the NAC (NAM, ATAF1/2, and CUC2) transcription factor (TF) family participate in drought-stress-induced signal transduction in plants, but little is known about the roles of NAC genes in drought tolerance in grapevine. Here, we explored the role of VaNAC17 in Vitis amurensis, a cold-hardy, drought-tolerant species of grapevine. VaNAC17 was strongly induced in grapevine by drought, exogenous abscisic acid (ABA), and methyl jasmonate (MeJA). A transient expression assay in yeast indicated that VaNAC17 functions as a transcriptional activator. Notably, heterologous expression of VaNAC17 in Arabidopsis thaliana enhanced drought tolerance. VaNAC17-expressing Arabidopsis plants showed decreased reactive oxygen species (ROS) accumulation compared to wild-type plants under drought conditions. RNA-seq analysis indicated that VaNAC17 expression increased the transcription of downstream stress-responsive genes after 5 days of drought treatment, especially genes involved in jasmonic acid (JA) biosynthesis (such as LOX3, AOC1 and OPR3) and signaling (such as MYC2, JAZ1, VSP1 and CORI3) pathways. Endogenous JA levels increased in VaNAC17-OE plants under drought stress. Taken together, these results indicate that VaNAC17 plays a positive role in drought tolerance by modulating endogenous JA biosynthesis and ROS scavenging.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Availability of data and material

The raw data of RNA-seq have been submitted to the Sequence Read Archive database (accession number from SRR6080007 to SRR6080014).

Abbreviations

ABA:

Abscisic acid

AOC:

Allene oxide cyclase

AOS:

Allene oxide synthase

CDS:

Coding sequence

DAB:

Diaminobenzidine

EL:

Electrolyte leakage

JA:

Jasmonic acid

JAZ:

Jasmonate-ZIM domain protein

LOX:

Lipoxygenase

NAC:

NAM, ATAF1/2, and CUC2

NBT:

Nitro blue tetrazolium

OPR:

Oxophytodienoate reductase

PS II:

Photosystem II

qRT-PCR:

Quantitative real-time PCR

ROS:

Reactive oxygen species

STEM:

Short time-series expression miner

TF:

Transcription factor

References

  • Abe H, Urao T, Ito T, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling. Plant Cell 15:63–78

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ahmad P, Rasool S, Gul A, Sheikh SA, Akram NA, Ashraf M et al (2016) Jasmonates: multifunctional roles in stress tolerance. Front Plant Sci 7:813

    PubMed  PubMed Central  Google Scholar 

  • Attaran E, Major IT, Cruz JA, Rosa BA, Koo AJ, Chen J et al (2014) Temporal dynamics of growth and photosynthesis suppression in response to jasmonate signaling. Plant Physiol 165:1302–1314

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bajji M, Kinet J-M, Lutts S (2002) The use of the electrolyte leakage method for assessing cell membrane stability as a water stress tolerance test in durum wheat. Plant Growth Regul 36:61–70

    CAS  Google Scholar 

  • Bies-Etheve N, Gaubier-Comella P, Debures A, Lasserre E, Jobet E, Raynal M et al (2008) Inventory, evolution and expression profiling diversity of the LEA (late embryogenesis abundant) protein gene family in Arabidopsis thaliana. Plant Mol Biol 67:107–124

    CAS  PubMed  Google Scholar 

  • Bu Q, Jiang H, Li CB, Zhai Q, Zhang J, Wu X et al (2008) Role of the Arabidopsis thaliana NAC transcription factors ANAC019 and ANAC055 in regulating jasmonic acid-signaled defense responses. Cell Res 18(7):756

    CAS  PubMed  Google Scholar 

  • Chen X, Wang Y, Lv B, Li J, Luo L, Lu S et al (2014) The NAC family transcription factor OsNAP confers abiotic stress response through the ABA pathway. Plant Cell Physiol 55:604–619

    CAS  PubMed  Google Scholar 

  • Chong J, Le Henanff G, Bertsch C, Walter B (2008) Identification, expression analysis and characterization of defense and signaling genes in Vitis vinifera. Plant Physiol Biochem 46:469–481

    CAS  PubMed  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    CAS  PubMed  Google Scholar 

  • Cruz de Carvalho MH (2008) Drought stress and reactive oxygen species: production, scavenging and signaling. Plant Signal Behav 3:156–165

    PubMed  PubMed Central  Google Scholar 

  • Dar TA, Uddin M, Khan MMA, Hakeem K, Jaleel H (2015) Jasmonates counter plant stress: a review. Environ Exp Bot 115:49–57

    CAS  Google Scholar 

  • Das K, Roychoudhury A (2014) Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants. Front Environ Sci 2:53

    Google Scholar 

  • de Ollas C, Dodd IC (2016) Physiological impacts of ABA–JA interactions under water-limitation. Plant Mol Biol 91:641–650

    PubMed  PubMed Central  Google Scholar 

  • Ernst J, Bar-Joseph Z (2006) STEM: a tool for the analysis of short time series gene expression data. BMC Bioinform 7(1):191

    Google Scholar 

  • Fang L, Su L, Sun X, Li X, Sun M, Karungo SK et al (2016) Expression of Vitis amurensis NAC26 in Arabidopsis enhances drought tolerance by modulating jasmonic acid synthesis. J Exp Bot 67:2829–2845

    CAS  PubMed  PubMed Central  Google Scholar 

  • Forcat S, Bennett MH, Mansfield JW, Grant MR (2008) A rapid and robust method for simultaneously measuring changes in the phytohormones ABA, JA and SA in plants following biotic and abiotic stress. Plant Methods 4:16

    PubMed  PubMed Central  Google Scholar 

  • Fujita M, Fujita Y, Maruyama K, Seki M, Hiratsu K, Ohme-Takagi M et al (2004) A dehydration-induced NAC protein, RD26, is involved in a novel ABA-dependent stress-signaling pathway. Plant J 39:863–876

    CAS  PubMed  Google Scholar 

  • Hao YJ, Wei W, Song QX, Chen HW, Zhang YQ, Wang F et al (2011) Soybean NAC transcription factors promote abiotic stress tolerance and lateral root formation in transgenic plants. Plant J 68:302–313

    CAS  PubMed  Google Scholar 

  • He XJ, Mu RL, Cao WH, Zhang ZG, Zhang JS, Chen SY (2005) AtNAC2, a transcription factor downstream of ethylene and auxin signaling pathways, is involved in salt stress response and lateral root development. Plant J 44:903–916

    CAS  PubMed  Google Scholar 

  • Hellemans J, Mortier G, De Paepe A, Speleman F, Vandesompele J (2007) qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biol 8:R19

    PubMed  PubMed Central  Google Scholar 

  • Hong Y, Zhang H, Huang L, Li D, Song F (2016) Overexpression of a stress-responsive NAC transcription factor gene ONAC022 improves drought and salt tolerance in rice. Front Plant Sci 7:4

    PubMed  PubMed Central  Google Scholar 

  • Huang L, Hong Y, Zhang H, Li D, Song F (2016) Rice NAC transcription factor ONAC095 plays opposite roles in drought and cold stress tolerance. BMC Plant Biol 16:203

    PubMed  PubMed Central  Google Scholar 

  • Ismail A, Seo M, Takebayashi Y, Kamiya Y, Nick P (2015) A balanced JA/ABA status may correlate with adaptation to osmotic stress in Vitis cells. J Plant Physiol 185:57–64

    CAS  PubMed  Google Scholar 

  • Jaleel CA, Manivannan P, Wahid A, Farooq M, Al-Juburi HJ, Somasundaram R et al (2009) Drought stress in plants: a review on morphological characteristics and pigments composition. Int J Agric Biol 11:100–105

    Google Scholar 

  • Jiang X, Zhang C, Lü P, Jiang G, Liu X, Dai F et al (2014) RhNAC3, a stress-associated NAC transcription factor, has a role in dehydration tolerance through regulating osmotic stress-related genes in rose petals. Plant Biotechnol J 12:38–48

    CAS  PubMed  Google Scholar 

  • Kazan K (2015) Diverse roles of jasmonates and ethylene in abiotic stress tolerance. Trends Plant Sci 20:219–229

    CAS  PubMed  Google Scholar 

  • Kikuchi K, Ueguchi-Tanaka M, Yoshida K, Nagato Y, Matsusoka M, Hirano H-Y (2000) Molecular analysis of the NAC gene family in rice. Mol Gen Genet 262:1047–1051

    CAS  PubMed  Google Scholar 

  • Kleinow T, Himbert S, Krenz B, Jeske H, Koncz C (2009) NAC domain transcription factor ATAF1 interacts with SNF1-related kinases and silencing of its subfamily causes severe developmental defects in Arabidopsis. Plant Sci 177:360–370

    CAS  Google Scholar 

  • Lovisolo C, Perrone I, Carra A, Ferrandino A, Flexas J, Medrano H et al (2010) Drought-induced changes in development and function of grapevine (Vitis spp.) organs and in their hydraulic and non-hydraulic interactions at the whole-plant level: a physiological and molecular update. Funct Plant Biol 37:98–116

    CAS  Google Scholar 

  • Mahmood K, Xu Z, El-Kereamy A, Casaretto JA, Rothstein SJ (2016) The Arabidopsis transcription factor ANAC032 represses anthocyanin biosynthesis in response to high sucrose and oxidative and abiotic stresses. Front Plant Sci 7:1548

    PubMed  PubMed Central  Google Scholar 

  • Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51:659–668

    CAS  PubMed  Google Scholar 

  • Munné-Bosch S, Müller M (2013) Hormonal cross-talk in plant development and stress responses. Front Plant Sci 4:529

    PubMed  PubMed Central  Google Scholar 

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

    CAS  Google Scholar 

  • Noir S, Bömer M, Takahashi N, Ishida T, Tsui T-L, Balbi V et al (2013) Jasmonate controls leaf growth by repressing cell proliferation and the onset of endoreduplication while maintaining a potential stand-by mode. Plant Physiol 161:1930–1951

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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. Sci Rep 6:23609

    CAS  PubMed  PubMed Central  Google Scholar 

  • Olsen AN, Ernst HA, Leggio LL, Skriver K (2005) NAC transcription factors: structurally distinct, functionally diverse. Trends Plant Sci 10:79–87

    CAS  PubMed  Google Scholar 

  • Pedranzani H, Sierra-de-Grado R, Vigliocco A, Miersch O, Abdala G (2007) Cold and water stresses produce changes in endogenous jasmonates in two populations of Pinus pinaster Ait. Plant Growth Regul 52:111–116

    CAS  Google Scholar 

  • Puranik S, Sahu PP, Srivastava PS, Prasad M (2012) NAC proteins: regulation and role in stress tolerance. Trends Plant Sci 17:369–381

    CAS  PubMed  Google Scholar 

  • Qiu Z, Guo J, Zhu A, Zhang L, Zhang M (2014) Exogenous jasmonic acid can enhance tolerance of wheat seedlings to salt stress. Ecotoxicol Environ Saf 104:202–208

    CAS  PubMed  Google Scholar 

  • Riemann M, Dhakarey R, Hazman M, Miro B, Kohli A, Nick P (2015) Exploring jasmonates in the hormonal network of drought and salinity responses. Front Plant Sci 6:1077

    PubMed  PubMed Central  Google Scholar 

  • Samarah NH (2016) Understanding how plants respond to drought stress at the molecular and whole plant levels. Drought stress tolerance in plants, vol 2. Springer, New York, pp 1–37

    Google Scholar 

  • Sasaki-Sekimoto Y, Taki N, Obayashi T, Aono M, Matsumoto F, Sakurai N et al (2005) Coordinated activation of metabolic pathways for antioxidants and defence compounds by jasmonates and their roles in stress tolerance in Arabidopsis. Plant J 44:653–668

    CAS  PubMed  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K (2007) Gene networks involved in drought stress response and tolerance. J Exp Bot 58:221–227

    CAS  PubMed  Google Scholar 

  • Simpson PJ, Tantitadapitak C, Reed AM, Mather OC, Bunce CM, White SA et al (2009) Characterization of two novel aldo–keto reductases from Arabidopsis: expression patterns, broad substrate specificity, and an open active-site structure suggest a role in toxicant metabolism following stress. J Mol Biol 392:465–480

    CAS  PubMed  Google Scholar 

  • Su L, Dai Z, Li S, Xin H (2015) A novel system for evaluating drought–cold tolerance of grapevines using chlorophyll fluorescence. BMC Plant Biol 15:82

    PubMed  PubMed Central  Google Scholar 

  • Tak H, Negi S, Ganapathi T (2016) Banana NAC transcription factor MusaNAC042 is positively associated with drought and salinity tolerance. Protoplasma 254:1–14

    Google Scholar 

  • Tattersall EA, Grimplet J, DeLuc L, Wheatley MD, Vincent D, Osborne C et al (2007) Transcript abundance profiles reveal larger and more complex responses of grapevine to chilling compared to osmotic and salinity stress. Funct Integr Genom 7:317–333

    CAS  Google Scholar 

  • Tran L-SP, Nakashima K, Sakuma Y, Simpson SD, Fujita Y, Maruyama K et al (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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Vishwakarma K, Upadhyay N, Kumar N, Yadav G, Singh J, Mishra RK et al (2017) Abscisic acid signaling and abiotic stress tolerance in plants: a review on current knowledge and future prospects. Front Plant Sci 8:161

    PubMed  PubMed Central  Google Scholar 

  • Wang N, Zheng Y, Xin H, Fang L, Li S (2013) Comprehensive analysis of NAC domain transcription factor gene family in Vitis vinifera. Plant Cell Rep 32:61–75

    PubMed  Google Scholar 

  • Wasternack C, Hause B (2013) Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in Annals of Botany. Ann Bot 111:1021–1058

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wellburn AR (1994) The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J Plant Physiol 144:307–313

    CAS  Google Scholar 

  • Wu H, Fu B, Sun P, Xiao C, Liu J-H (2016) A NAC transcription factor represses putrescine biosynthesis and affects drought tolerance. Plant Physiol 172:1532–1547

    CAS  PubMed  PubMed Central  Google Scholar 

  • Xiao H-M, Cai W-J, Ye T-T, Ding J, Feng Y-Q (2018) Spatio-temporal profiling of abscisic acid, indoleacetic acid and jasmonic acid in single rice seed during seed germination. Anal Chim Acta 1031:119–127

    CAS  PubMed  Google Scholar 

  • Ying L, Chen H, Cai W (2014) BnNAC485 is involved in abiotic stress responses and flowering time in Brassica napus. Plant Physiol Biochem 79:77–87

    CAS  PubMed  Google Scholar 

  • Yoshii M, Yamazaki M, Rakwal R, Kishi-Kaboshi M, Miyao A, Hirochika H (2010) The NAC transcription factor RIM1 of rice is a new regulator of jasmonate signaling. Plant J 61:804–815

    CAS  PubMed  Google Scholar 

  • Zhang C, Huang Z (2013) Effects of endogenous abscisic acid, jasmonic acid, polyamines, and polyamine oxidase activity in tomato seedlings under drought stress. Sci Hortic 159:172–177

    CAS  Google Scholar 

  • Zhang Y, Turner JG (2008) Wound-induced endogenous jasmonates stunt plant growth by inhibiting mitosis. PLoS ONE 3:e3699

    PubMed  PubMed Central  Google Scholar 

  • Zhong R, Demura T, Ye Z-H (2006) SND1, a NAC domain transcription factor, is a key regulator of secondary wall synthesis in fibers of Arabidopsis. Plant Cell 18:3158–3170

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu J-K (2016) Abiotic stress signaling and responses in plants. Cell 167:313–324

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Natural Science Foundation of China (NSFC Accession No.: 31672132), Youth Innovation Promotion Association of Chinese Academy of Sciences (2015281) and Grape Breeding Project of Ningxia (NXNYYZ201502).

Author information

Authors and Affiliations

Authors

Contributions

LS, LF and HX: conceived of the study, drafted manuscript; LS, LF, ZZ, LZ, XS and YW: conducted the experiments; QW and SL: corrected manuscript. All authors read and approved the final manuscript.

Corresponding authors

Correspondence to Shaohua Li or Haiping Xin.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by Prakash Lakshmanan.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (xlsx 334 kb)

Supplementary file2 (pdf 709 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Su, L., Fang, L., Zhu, Z. et al. The transcription factor VaNAC17 from grapevine (Vitis amurensis) enhances drought tolerance by modulating jasmonic acid biosynthesis in transgenic Arabidopsis. Plant Cell Rep 39, 621–634 (2020). https://doi.org/10.1007/s00299-020-02519-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-020-02519-x

Keywords

Navigation