Abstract
Main conclusion
HaNAC3 is a transcriptional activator located in the nucleus that may be involved in the response to high temperature, high salt and drought stresses as well as phytohormone IAA and ABA treatments. Our study demonstrated that HaNAC3 increased the tolerance of transgenic tobacco to abiotic stress and was involved in the regulation of a range of downstream genes and metabolic pathways. This also indicates the potential application of HaNAC3 as a plant tolerance gene.
Abstract
NAC transcription factors play a key role in plant growth and development and plant responses to biotic and abiotic stresses. However, the biological functions of NAC transcription factors in the desert plant Haloxylon ammodendron are still poorly understood. In this study, the NAC transcription factor HaNAC3 was isolated and cloned from a typical desert plant H. ammodendron, and its possible biological functions were investigated. Bioinformatics analysis showed that HaNAC3 has the unique N-terminal NAC structural domain of NAC transcription factor. Quantitative real-time fluorescence analysis showed that HaNAC3 was able to participate in the response to simulated drought, high temperature, high salt, and phytohormone IAA and ABA treatments, and was very sensitive to simulated high temperature and phytohormone ABA treatments. Subcellular localization analysis showed that the GFP-HaNAC3 fusion protein was localized in the nucleus of tobacco epidermal cells. The transcriptional self-activation assay showed that HaNAC3 had transcriptional self-activation activity, and the truncation assay confirmed that the transcriptional activation activity was located at the C-terminus. HaNAC3 gene was expressed exogenously in wild-type Nicotiana benthamiana, and the physiological function of HaNAC3 was verified by simulating drought and other abiotic stresses. The results indicated that transgenic tobacco had better resistance to abiotic stresses than wild-type B. fuminata. Further transcriptome analysis showed that HaNAC3 was involved in the regulation of a range of downstream resistance genes, wax biosynthesis and other metabolic pathways. These results suggest that HaNAC3 may have a stress resistance role in H. ammodendron and has potential applications in plant molecular breeding.
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The datasets generated or analyzed during this study are available from the corresponding author on reasonable request.
References
Aida M, Ishida T, Fukaki H et al (1997) Genes involved in organ separation in Arabidopsis: an analysis of the cup-shaped cotyledon mutant. Plant Cell 9(6):841–857. https://doi.org/10.1105/tpc.9.6.841
Bian Z, Gao H, Wang C (2020) NAC transcription factors as positive or negative regulators during ongoing battle between pathogens and our food crops. Int J Mol Sci 22(1):81. https://doi.org/10.3390/ijms22010081
Borisjuk N, Hrmova M, Lopato S (2014) Transcriptional regulation of cuticle biosynthesis. Biotechnol Adv 32(2):526–540. https://doi.org/10.1016/j.biotechadv.2014.01.005
Cao H, Wang Li, Nawaz MA et al (2017) Ectopic expression of pumpkin NAC transcription factor CmNAC1 improves multiple abiotic stress tolerance in Arabidopsis. Front Plant Sci 8:2052. https://doi.org/10.3389/fpls.2017.02052
Cenci A, Guignon V, Roux N et al (2014) Genomic analysis of NAC transcription factors in banana (Musa acuminata) and definition of NAC orthologous groups for monocots and dicots. Plant Mol Biol 85(1–2):63–80. https://doi.org/10.1007/s11103-013-0169-2
Cheng Z, Zhang X, Zhao K et al (2020) Ectopic expression of a poplar gene NAC13 confers enhanced tolerance to salinity stress in transgenic Nicotiana tabacum. J Plant Res 133(5):727–737. https://doi.org/10.1007/s10265-020-01213-z
Cui X, Yue P, Gong Y et al (2017) Impacts of water and nitrogen addition on nitrogen recovery in Haloxylon ammodendron dominated desert ecosystems. Sci Total Environ 2017(601–602):1280–1288. https://doi.org/10.1016/j.scitotenv.2017.05.202
de Dios Alché J (2019) A concise appraisal of lipid oxidation and lipoxidation in higher plants. Redox BIol 2019(23):101136. https://doi.org/10.1016/j.redox.2019.101136
Duan A-Q, Yang X-L, Feng K et al (2020) Genome-wide analysis of NAC transcription factors and their response to abiotic stress in celery (Apium graveolens L.). Comput Biol Chem 84(C). https://doi.org/10.1016/j.compbiolchem.2019.107186
eUpadhyaya HD et al (2012) Phenotyping chickpeas and pigeonpeas for adaptation to drought. Front Physiol 3. https://doi.org/10.3389/fphys.2012.00179
Fan L, Wang G, Wei Hu et al (2018) Transcriptomic view of survival during early seedling growth of the extremophyte Haloxylon ammodendron. Plant Physiol Biochem 132(2018):475–489. https://doi.org/10.1016/j.plaphy.2018.09.024
Francisca G, Karina OH, Claudia S, Michael H (2021) Abiotic stress in crop species: improving tolerance by applying plant metabolites. Plants 10(2). https://doi.org/10.3390/plants10020186
Gelvin SB (2003) Agrobacterium-mediated plant transformation: the biology behind the “gene-jockeying” tool. Microbiol Mol Biol Rev 67(1):16–37. https://doi.org/10.1128/MMBR.67.1.16-37.2003
Gong Y, Zack TI, Morris LGT et al (2014) Pan-cancer genetic analysis identifies PARK2 as a master regulator of G1/S cyclins. Nature Genet 46(6):588–594. https://doi.org/10.1038/ng.2981
Gong C, Wang J, Congxia Hu et al (2015) Interactive response of photosynthetic characteristics in Haloxylon ammodendron and Hedysarum scoparium exposed to soil water and air vapor pressure deficits. J Environ Sci 34(8):184–196. https://doi.org/10.1016/j.jes.2015.03.012
Gong L, Zhang H, Liu X et al (2020) Ectopic expression of HaNACl, an ATAF transcription factor from Haloxylon ammodendron, improves growth and drought tolerance in transgenic Arabidopsis. Plant Physiol Biochem 2020(151):535–544. https://doi.org/10.1016/j.plaphy.2020.04.008
Hao Y-J, Wei W, Song Q-X et al (2011) Soybean NAC transcription factors promote abiotic stress tolerance and lateral root formation in transgenic plants. Plant J 68(2):302–313. https://doi.org/10.1111/j.1365-313X.2011.04687.x
Hayat S, Hayat Q, Alyemeni MN et al (2012) Role of proline under changing environments: a review. Plant Signal Behav 7(11):1456–1466. https://doi.org/10.4161/psb.21949
He X-J, Rui-Ling Mu, Cao W-H et al (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(6):903–916. https://doi.org/10.1111/j.1365-313X.2005.02575.x
He A, Niu S, Yang Di et al (2021) Two PGPR strains from the rhizosphere of Haloxylon ammodendron promoted growth and enhanced drought tolerance of ryegrass. Plant Physiol Biochem 2021(161):74–85. https://doi.org/10.1016/j.plaphy.2021.02.003
Javed T, Shabbir R, Ali A et al (2020) Transcription factors in plant stress responses: challenges and potential for sugarcane improvement. Plants 9(4):491–491. https://doi.org/10.3390/plants9040491
Kavi Kishor PB, Sreenivasulu N (2014) Proline homeostasis. Plant Cell Environ 37:300–311. https://doi.org/10.1111/pce.12157
Kim Y-S, Kim S-G, Park J-E et al (2006) A membrane-bound NAC transcription factor regulates cell division in Arabidopsis. Plant Cell 18(11):3132–3144. https://doi.org/10.1105/tpc.106.043018
Kim Y-H, Khan AL, Waqas M et al (2017) Silicon regulates antioxidant activities of crop plants under abiotic-induced oxidative stress: a review. Front Plant Sci 2017(8):510. https://doi.org/10.3389/fpls.2017.00510
Krenek P, Samajova O, Luptovciak I et al (2015) Transient plant transformation mediated by Agrobacterium tumefaciens: Principles, methods and applications. Biotechnol Adv 33(6):1024–1042. https://doi.org/10.1016/j.biotechadv.2015.03.012
Le Hénanff G, Profizi C, Courteaux B et al (2013) Grapevine NAC1 transcription factor as a convergent node in developmental processes, abiotic stresses, and necrotrophic/biotrophic pathogen tolerance. J Exp Bot 64(16):4877–4893. https://doi.org/10.1093/jxb/ert277
Li Y, Ma X, Zhao J et al (2015) Developmental genetic mechanisms of C4 syndrome based on transcriptome analysis of C3 cotyledons and C4 assimilating shoots in Haloxylon ammodendron. PLoS ONE 10(2):e0117175. https://doi.org/10.1371/journal.pone.0117175
Liu Q-L, Ke-Dong Xu, Zhao L-J et al (2011) Overexpression of a novel chrysanthemum NAC transcription factor gene enhances salt tolerance in tobacco. Biotech Lett 33(10):2073–2082. https://doi.org/10.1007/s10529-011-0659-8
Lü X-P, Gao H-J, Zhang L et al (2019) Dynamic responses of Haloxylon ammodendron to various degrees of simulated drought stress. Plant Physiol Biochem 2019(139):121–131. https://doi.org/10.1016/j.plaphy.2019.03.019
Miller J, Stagljar I (2004) Using the yeast two-hybrid system to identify interacting proteins. Methods Mol Biol 2004(261):247–262. https://doi.org/10.1385/1-59259-762-9:247
Minoru K, Yoko S (2020) KEGG Mapper for inferring cellular functions from protein sequences. Protein Sci Publ Protein Soc 29(1). https://doi.org/10.1002/pro.3711
Negi S, Tak H, Ganapathi TR (2016) Functional characterization of secondary wall deposition regulating transcription factors MusaVND2 and MusaVND3 in transgenic banana plants. Protoplasma 253:431–446. https://doi.org/10.1007/s00709-015-0822-5
Nuruzzaman M, Sharoni AM, Kikuchi S (2013) Roles of NAC transcription factors in the regulation of biotic and abiotic stress responses in plants. Front Microbiol 2013(4):248. https://doi.org/10.3389/fmicb.2013.00248
Panda A, Rangani J, Parida AK (2021) Physiological and metabolic adjustments in the xero-halophyte Haloxylon salicornicum conferring drought tolerance. Physiol Plant 172(2):1189–1211. https://doi.org/10.1111/ppl.13351
Rausch T, Gromes R, Liedschulte V et al (2007) Novel insight into the regulation of GSH biosynthesis in higher plants. Plant Biol (Stuttg) 9(5):565–572. https://doi.org/10.1055/s-2007-965580
Rio DC, Ares Jr M, Hannon GJ et al (2010) Purification of RNA using TRIzol (TRI reagent). Cold Spring Harb Protoc. https://doi.org/10.1101/pdb.prot5439
Shao H, Wang H, Tang X (2015) NAC transcription factors in plant multiple abiotic stress responses: progress and prospects. Front Plant Sci 2015(6):902–902. https://doi.org/10.3389/fpls.2015.00902
Sheng Y, Zheng W, Pei K et al (2005) Genetic variation within and among populations of a dominant desert tree Haloxylon ammodendron (Amaranthaceae) in China. Ann Bot 96(2):245–252. https://doi.org/10.1093/aob/mci171
Singh S, Koyama H, Bhati KK et al (2021) Correction to: The biotechnological importance of the plant-specific NAC transcription factor family in crop improvement. J Plant Res 2021(134):475–495. https://doi.org/10.1007/s10265-021-01281-9
Souer E, van Houwelingen A, Kloos D et al (1996) The no apical meristem gene of petunia is required for pattern formation in embryos and flowers and is expressed at meristem and primordia boundaries. Cell 85(2):159–170. https://doi.org/10.1016/s0092-8674(00)81093-4
Todaka D, Nakashima K, Shinozaki K et al (2012) Toward understanding transcriptional regulatory networks in abiotic stress responses and tolerance in rice. Rice 5(1):6. https://doi.org/10.1186/1939-8433-5-6
Tran L-S, Nishiyama R, Yamaguchi-Shinozaki K et al (2010) Potential utilization of NAC transcription factors to enhance abiotic stress tolerance in plants by biotechnological approach. GM Crops 1(1):32–39. https://doi.org/10.4161/gmcr.1.1.10569
Trupkin SA, Astigueta FH, Baigorria AH et al (2019) Identification and expression analysis of NAC transcription factors potentially involved in leaf and petal senescence in Petunia hybrid. Plant Sci 2019(287):110195. https://doi.org/10.1016/j.plantsci.2019.110195
Wang D, Ni Y, Liao L et al (2021a) Poa pratensis ECERIFERUM1 (PpCER1) is involved in wax alkane biosynthesis and plant drought tolerance. Plant Physiol Biochem 2021(159):312–321. https://doi.org/10.1016/j.plaphy.2020.12.032
Wang Qi, Guo C, Li Z et al (2021b) Potato NAC transcription factor StNAC053 enhances salt and drought tolerance in transgenic Arabidopsis. Int J Mol Sci 22(5):2568–2568. https://doi.org/10.3390/ijms22052568
Xia X, Huo W, Wan R et al (2017) Identification of housekeeping genes as references for quantitative real-time RT-PCR analysis in Misgurnus anguillicaudatus. J Genet 96(6):895–904. https://doi.org/10.1007/s12041-017-0845-0
Yang X, He K, Chi X et al (2018) Miscanthus NAC transcription factor MlNAC12 positively mediates abiotic stress tolerance in transgenic Arabidopsis. Plant Sci 2018(277):229–241. https://doi.org/10.1016/j.plantsci.2018.09.013
Yang X, Kim MY, Ha J et al (2019) Overexpression of the soybean NAC gene gmnac109 increases lateral root formation and abiotic stress tolerance in transgenic Arabidopsis plants. Front Plant Sci 10(2019):1036. https://doi.org/10.3389/fpls.2019.01036
Zhang J, Li L, Huang L et al (2019) Maize NAC-domain retained splice variants act as dominant negatives to interfere with the full-length NAC counterparts. Plant Sci 2019(289):110256. https://doi.org/10.1016/j.plantsci.2019.110256
Zhao X, Yang X, Pei S et al (2016) The miscanthus NAC transcription factor MlNAC9 enhances abiotic stress tolerance in transgenic Arabidopsis. Gene 586(1):158–169. https://doi.org/10.1016/j.gene.2016.04.028
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Supported by: National Natural Science Foundation of China (31760214) and the Plant Biotechnology Laboratory of Xinjiang Agricultural University.
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Liu, X., Zong, X., Wu, X. et al. Ectopic expression of NAC transcription factor HaNAC3 from Haloxylon ammodendron increased abiotic stress resistance in tobacco. Planta 256, 105 (2022). https://doi.org/10.1007/s00425-022-04021-y
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DOI: https://doi.org/10.1007/s00425-022-04021-y