Abstract
Key message
Ectopic expression of Glycine max two-component system member GmHP08 in Arabidopsis enhanced drought tolerance of transgenic plants, possibly via ABA-dependent pathways.
Abstract
Phosphorelay by two-component system (TCS) is a signal transduction mechanism which has been evolutionarily conserved in both prokaryotic and eukaryotic organisms. Previous studies have provided lines of evidence on the involvement of TCS genes in plant perception and responses to environmental stimuli. In this research, drought-associated functions of GmHP08, a TCS member from soybean (Glycine max L.), were investigated via its ectopic expression in Arabidopsis system. Results from the drought survival assay showed that GmHP08-transgenic plants exhibited higher survival rates compared with their wild-type (WT) counterparts, indicating better drought resistance of the former group. Analyses revealed that the transgenic plants outperformed the WT in various regards, i.e. capability of water retention, prevention of hydrogen peroxide accumulation and enhancement of antioxidant enzymatic activities under water-deficit conditions. Additionally, the expression of stress-marker genes, especially antioxidant enzyme-encoding genes, in the transgenic plants were found greater than that of the WT plants. In contrary, the expression of SAG13 gene, one of the senescence-associated genes, and of several abscisic acid (ABA)-related genes was repressed. Data from this study also revealed that the ectopic expression lines at germination and early seedling development stages were hypersensitive to exogenous ABA treatment. Taken together, our results demonstrated that GmHP08 could play an important role in mediating plant response to drought, possibly via an ABA-dependent manner.
Similar content being viewed by others
References
Ahmad B, Azeem F, Ali MA et al (2020) Genome-wide identification and expression analysis of two component system genes in Cicer arietinum. Genomics 112:1371–1383
Ajithkumar IP, Panneerselvam R (2014) ROS scavenging system, osmotic maintenance, pigment and growth status of Panicum sumatrense Roth under drought stress. Cell Biochem Biophys 68:587–595
Binder BM, Kim HJ, Mathews DE et al (2018) A role for two-component signaling elements in the Arabidopsis growth recovery response to ethylene. Plant Direct 2:e00058
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Bowler C, van Camp W, van Montagu M, Inzé D (1994) Superoxide dismutase in plants. Crit Rev Plant Sci 13:199–218
Caser M, Chitarra W, D’Angiolillo F et al (2019) Drought stress adaptation modulates plant secondary metabolite production in Salvia dolomitica Codd. Ind Crops Prod 129:85–96
Chen Y, Jiang J, Song A et al (2013) Ambient temperature enhanced freezing tolerance of Chrysanthemum dichrum CdICE1 Arabidopsis via miR398. BMC Biol 11:121
Cho YH, Yoo SD (2007) Ethylene response 1 histidine kinase activity of Arabidopsis promotes plant growth. Plant Physiol 143:612–616
Choudhury FK, Rivero RM, Blumwald E, Mittler R (2017) Reactive oxygen species, abiotic stress and stress combination. Plant J 90:856–867
Chu ZX, Ma Q, Lin YX et al (2011) Genome-wide identification, classification, and analysis of two-component signal system genes in maize. Genet Mol Res 10:3316–3330
Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743
Considine MJ, María Sandalio L, Helen Foyer C (2015) Unravelling how plants benefit from ROS and NO reactions, while resisting oxidative stress. Ann Bot 116:469–473
Cortleven A, Nitschke S, Klaumünzer M et al (2014) A novel protective function for cytokinin in the light stress response is mediated by the Arabidopsis histidine kinase2 and Arabidopsis histidine kinase3 receptors. Plant Physiol 164:1470–1483
Cruz De Carvalho MH (2008) Drought stress and reactive oxygen species: production, scavenging and signaling. Plant Signal Behav 3:156–165
de Ollas C, Segarra-Medina C, González-Guzmán M et al (2019) A customizable method to characterize Arabidopsis thaliana transpiration under drought conditions. Plant Methods 15:89
Deng Y, Dong H, Mu J et al (2010) Arabidopsis histidine kinase CKI1 acts upstream of histidine phosphotransfer proteins to regulate female gametophyte development and vegetative growth. Plant Cell 22:1232–1248
Desikan R, Horák J, Chaban C et al (2008) The histidine kinase AHK5 integrates endogenous and environmental signals in Arabidopsis guard cells. PLoS ONE 3:e2491
Ding S, Cai Z, Du H, Wang H (2019) Genome-wide analysis of TCP family genes in Zea mays l. Identified a role for ZmTCP42 in drought tolerance. Int J Mol Sci 20:2762
Ding Z, Li S, An X et al (2009) Transgenic expression of MYB15 confers enhanced sensitivity to abscisic acid and improved drought tolerance in Arabidopsis thaliana. J Genet Genomics 36:17–29
Dittrich M, Mueller HM, Bauer H et al (2019) The role of Arabidopsis ABA receptors from the PYR/PYL/RCAR family in stomatal acclimation and closure signal integration. Nat Plants 5:1002–1011
Du YY, Wang PC, Chen J, Song CP (2008) Comprehensive functional analysis of the catalase gene family in Arabidopsis thaliana. J Integrat Plant Biol 50:1318–1326
Endo A, Sawada Y, Takahashi H et al (2008) Drought induction of Arabidopsis 9-cis-epoxycarotenoid dioxygenase occurs in vascular parenchyma cells. Plant Physiol 147:1984–1993
Farber M, Attia Z, Weiss D (2016) Cytokinin activity increases stomatal density and transpiration rate in tomato. J Exp Bot 67:6351–6362
Garapati P, Xue GP, Munné-Bosch S, Balazadeh S (2015) Transcription factor ATAF1 in Arabidopsis promotes senescence by direct regulation of key chloroplast maintenance and senescence transcriptional cascades. Plant Physiol 168:1122–1139
Giannopolitis CN, Ries SK (1977) Superoxide dismutases: I. Occurrence in higher plants. Plant Physiol 59:309–314
Gonzalez-Guzman M, Pizzio GA, Antoni R et al (2012) Arabidopsis PYR/PYL/RCAR receptors play a major role in quantitative regulation of stomatal aperture and transcriptional response to abscisic acid. Plant Cell 24:2483–2496
Grefen C, Städele K, Růžička K et al (2008) Subcellular localization and in vivo interactions of the Arabidopsis thaliana ethylene receptor family members. Mol Plant 1:308–320
Hamayun M, Khan SA, Khan AL et al (2010) Effect of salt stress on growth attributes and endogenous growth hormones of soybean cultivar Hwangkeumkong. Pak J Bot 42:3103–3112
Hao Z, Singh VP, Xia Y (2018) Seasonal drought prediction: Advances, challenges, and future prospects. Rev Geophys 56:108–141
Harb A, Awad D, Samarah N (2015) Gene expression and activity of antioxidant enzymes in barley (Hordeum vulgare l.) under controlled severe drought. J Plant Interact 10:109–116
Hass C, Lohrmann J, Albrecht V et al (2004) The response regulator 2 mediates ethylene signalling and hormone signal integration in Arabidopsis. EMBO J 23:3290–3302
He Y, Liu X, Ye L et al (2016a) Genome-wide identification and expression analysis of two-component system genes in tomato. Int J Mol Sci 17:1204
He Y, Liu X, Zou T et al (2016b) Genome-wide identification of two-component system genes in cucurbitaceae crops and expression profiling analyses in cucumber. Front Plant Sci 7:899
Héricourt F, Larcher M, Chefdor F et al (2019) New insight into HPts as hubs in poplar cytokinin and osmosensing multistep phosphorelays: Cytokinin pathway uses specific hpts. Plants 8:591
Hoang XLT, Nguyen NC, Nguyen YNH et al (2020) The soybean GmNAC019 transcription factor mediates drought tolerance in Arabidopsis in an abscisic acid-dependent manner. Int J Mol Sci 21:286
Hossain MA, Bhattacharjee S, Armin SM et al (2015) Hydrogen peroxide priming modulates abiotic oxidative stress tolerance: Insights from ROS detoxification and scavenging. Front Plant Sci 6:420
Hsieh TH, Lee JT, Charng YY, Chan MT (2002) Tomato plants ectopically expressing Arabidopsis CBF1 show enhanced resistance to water deficit stress. Plant Physiol 130:618–626
Hua J, Sakai H, Nourizadeh S et al (1998) EIN4 and ERS2 are members of the putative ethylene receptor gene family in Arabidopsis. Plant Cell 10:1321–1332
Huang CH, Kuo WY, Weiss C, Jinn TL (2012) Copper chaperone-dependent and -independent activation of three copper-zinc superoxide dismutase homologs localized in different cellular compartments in Arabidopsis. Plant Physiol 158:737–746
Huang HJ, Yang ZQ, Zhang MY et al (2018a) Effects of water stress on growth, photosynthesis, root activity and endogenous hormones of Cucumis sativus. Int J Agric Biol 20:2579–2589
Huang Q, Wang Y, Li B et al (2015) TaNAC29, a NAC transcription factor from wheat, enhances salt and drought tolerance in transgenic Arabidopsis. BMC Plant Biol 15:268
Huang X, Hou L, Meng J et al (2018b) The antagonistic action of abscisic acid and cytokinin signaling mediates drought stress response in Arabidopsis. Mol Plant 11:970–982
Huang Y, Sun MM, Ye Q et al (2017) Abscisic acid modulates seed germination via ABA insensitive5-mediated phosphate. Plant Physiol 175:1661–1668
Hutchison CE, Li J, Argueso C et al (2006) The Arabidopsis histidine phosphotransfer proteins are redundant positive regulators of cytokinin signaling. Plant Cell 18:3073–3087
Hwang I, Chen HC, Sheen J (2002) Two-component signal transduction pathways in Arabidopsis. Plant Physiol 129:500–515
Ighodaro OM, Akinloye OA (2018) First line defence antioxidants-superoxide dismutase (SOD), catalase (CAT) and glutathione peroxidase (GPX): their fundamental role in the entire antioxidant defence grid. Alexandria J Med 54:287–293
Impa SM, Nadaradjan S (2012) Drought stress induced reactive oxygen species and anti-oxidants in plants. In: Ahmad P, Prasad M (eds) Abiotic stress responses in plants: metabolism, productivity and sustainability. Springer, New York, pp 131–147
Ishida K, Niwa Y, Yamashino T, Mizuno T (2009) A genome-wide compilation of the two-component systems in Lotus japonicus. DNA Res 16:237–247
Ishida K, Yamashino T, Mizuno T (2008) Expression of the cytokinin-induced type-A response regulator gene ARR9 is regulated by the circadian clock in Arabidopsis thaliana. Biosci Biotechnol Biochem 72:3025–3029
Iuchi S, Kobayashi M, Taji T et al (2001) Regulation of drought tolerance by gene manipulation of 9-cis-epoxycarotenoid dioxygenase, a key enzyme in abscisic acid biosynthesis in Arabidopsis. Plant J 27:325–333
Jeon J, Kim J (2013) Arabidopsis response regulator1 and Arabidopsis histidine phosphotransfer protein2 (AHP2), AHP3, and AHP5 function in cold signaling. Plant Physiol 161:408–424
Jeon J, Kim NY, Kim S et al (2010) A subset of cytokinin two-component signaling system plays a role in cold temperature stress response in Arabidopsis. J Biol Chem 285:23371–23386
Jiang Y, Liang G, Yu D (2012) Activated expression of WRKY57 confers drought tolerance in Arabidopsis. Mol Plant 5:1375–1388
Jin C, Li KQ, Xu XY 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. Front Plant Sci 8:1049
Kang NY, Cho C, Kim J (2013) Inducible expression of Arabidopsis response regulator 22 (ARR22), a Type-C ARR, in transgenic Arabidopsis enhances drought and freezing tolerance. PLoS ONE 8:e79248
Kasuga M, Miura S, Shinozaki K, Yamaguchi-Shinozaki K (2004) A combination of the Arabidopsis DREB1A gene and stress-inducible rd29A promoter improved drought- and low-temperature stress tolerance in tobacco by gene transfer. Plant Cell Physiol 45:346–350
Kerchev P, Waszczak C, Lewandowska A et al (2016) Lack of Glycolate oxidase1, but not Glycolate oxidase2, attenuates the photorespiratory phenotype of catalase2-deficient Arabidopsis. Plant Physiol 171:1704–1719
Kong X, Zhou S, Yin S et al (2016) Stress-inducible expression of an F-box gene TaFBA1 from wheat enhanced the drought tolerance in transgenic tobacco plants without impacting growth and development. Front Plant Sci 7:1295
Kooyers NJ (2015) The evolution of drought escape and avoidance in natural herbaceous populations. Plant Sci 234:155–162
Kumar MN, Jane WN, Verslues PE (2013) Role of the putative osmosensor Arabidopsis in dehydration avoidance and low-water-potential response . Plant Physiol 161:942–953
Le DT, Nishiyama R, Watanabe Y et al (2011) Genome-wide expression profiling of soybean two-component system genes in soybean root and shoot tissues under dehydration stress. DNA Res 18:17–29
Leng G, Hall J (2019) Crop yield sensitivity of global major agricultural countries to droughts and the projected changes in the future. Sci Total Environ 654:811–821
Li Y, Cai H, Liu P et al (2017) Arabidopsis MAPKKK18 positively regulates drought stress resistance via downstream MAPKK3. Biochem Biophys Res Commun 484:292–297
Li Y, Varala K, Moose SP, Hudson ME (2012) The inheritance pattern of 24 nt siRNA clusters in Arabidopsis hybrids is influenced by proximity to transposable elements. PLoS ONE 7:e47043
Lim CW, Baek W, Han SW, Lee SC (2013) Arabidopsis PYl8 plays an important role for ABA signaling and drought stress responses. Plant Pathol J 29:471–476
Liu Z, Zhang M, Kong L et al (2014) Genome-wide identification, phylogeny, duplication, and expression analyses of two-component system genes in Chinese cabbage (Brassica rapa ssp. pekinensis). DNA Res 21:379–396
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25:402–408
Lohar DP, Schaff JE, Laskey JG et al (2004) Cytokinins play opposite roles in lateral root formation, and nematode and Rhizobial symbioses. Plant J 38:203–214
Ma QH, Tian B (2005) Characterization of a wheat histidine-containing phosphotransfer protein (HP) that is regulated by cytokinin-mediated inhibition of leaf senescence. Plant Sci 168:1507–1514
Marchadier E, Hetherington AM (2014) Involvement of two-component signalling systems in the regulation of stomatal aperture by light in Arabidopsis thaliana. New Phytol 203:462–468
Maruta T, Tanouchi A, Tamoi M et al (2010) Arabidopsis chloroplastic ascorbate peroxidase isoenzymes play a dual role in photoprotection and gene regulation under photooxidative stress. Plant Cell Physiol 51:190–200
Mhamdi A, van Breusegem F (2018) Reactive oxygen species in plant development. Development 145:209–236
Mignolet-Spruyt L, Xu E, Idänheimo N et al (2016) Spreading the news: subcellular and organellar reactive oxygen species production and signalling. J Exp Bot 67:3831–3844
Mira-Rodado V, Veerabagu M, Witthöft J et al (2012) Identification of two-component system elements downstream of AHK5 in the stomatal closure response of Arabidopsis thaliana. Plant Signal Behav 7:1467–1476
Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410
Mittler R (2017) ROS are good trends. Plant Sci 22:11–19
Mochida K, Yoshida T, Sakurai T et al (2010) Genome-wide analysis of two-component systems and prediction of stress-responsive two-component system members in soybean. DNA Res 17:303–324
Msanne J, Lin J, Stone JM, Awada T (2011) Characterization of abiotic stress-responsive Arabidopsis thaliana RD29A and RD29B genes and evaluation of transgenes. Planta 234:97–107
Nghia DHT, Chuong NN, Hoang XLT et al (2020) Heterologous expression of a soybean gene RR34 conferred improved drought resistance of transgenic Arabidopsis. Plants 9:494
Nguyen KH, van Ha C, Nishiyama R et al (2016) Arabidopsis type B cytokinin response regulators ARR1, ARR10, and ARR12 negatively regulate plant responses to drought. Proc Natl Acad Sci 113:3090–3095
Nguyen KH, Mostofa MG, Li W et al (2018) The soybean transcription factor GmNAC085 enhances drought tolerance in Arabidopsis. Environ Exp Bot 151:12–20
Nguyen KH, Mostofa MG, Tran CD, et al. (2020) The histidine phosphotransfer AHP4 plays a negative role in Arabidopsis plant response to drought. bioRxiv
Nguyen NC, Hoang XLT, Nguyen QT et al (2019) Ectopic expression of Glycine max GmNAC109 enhances drought tolerance and ABA sensitivity in Arabidopsis. Biomolecules 9:714
Nilson SE, Assmann SM (2007) The control of transpiration insights from Arabidopsis. Plant Physiol 143:19–27
Nir I, Moshelion M, Weiss D (2014) The Arabidopsis Gibberellin methyl transferase 1 suppresses gibberellin activity, reduces whole-plant transpiration and promotes drought tolerance in transgenic tomato. Plant Cell Environ 37:113–123
Nishimura C, Ohashi Y, Sato S et al (2004) Histidine kinase homologs that act as cytokinin receptors possess overlapping functions in the regulation of shoot and root growth in Arabidopsis. Plant Cell 16:1365–1377
Nishiyama R, Watanabe Y, Leyva-Gonzalez MA et al (2013) Arabidopsis AHP2, AHP3, and AHP5 histidine phosphotransfer proteins function as redundant negative regulators of drought stress response. Proc Natl Acad Sci 110:4840–4845
Pareek A, Singh A, Kumar M et al (2006) Whole-genome analysis of Oryza sativa reveals similar architecture of two-component signaling machinery with Arabidopsis. Plant Physiol 142:380–397
Passricha N, Saifi S, Khatodia S, Tuteja N (2016) Assessing zygosity in progeny of transgenic plants: current methods and perspectives. J Biol Methods 3:46
Patterson BD, MacRae EA, Ferguson IB (1984) Estimation of hydrogen peroxide in plant extracts using titanium(IV). Anal Biochem 139:487–492
Pham J, Desikan R (2012) Modulation of ROS production and hormone levels by AHK5 during abiotic and biotic stress signaling. Plant Signal Behav 7:893–897
Pischke MS, Jones LG, Otsuga D et al (2002) An Arabidopsis histidine kinase is essential for megagametogenesis. Proc Natl Acad Sci 99:15800–15805
Rasheed S, Bashir K, Matsui A et al (2016) Transcriptomic analysis of soil-grown Arabidopsis thaliana roots and shoots in response to a drought stress. Front Plant Sci 7:180
Rodríguez Y, Pérez E, Solórzano E et al (2001) Peroxidase and polyphenoloxidase activities in tomato roots inoculated with Glomus clarum or Glomus fasciculatum. Cult Trop 22:11–16
Rowland MA, Deeds EJ (2014) Crosstalk and the evolution of specificity in two-component signaling. Proc Natl Acad Sci 111:5550–5555
Roychoudhury A, Paul S, Basu S (2013) Cross-talk between abscisic acid-dependent and abscisic acid-independent pathways during abiotic stress. Plant Cell Rep 32:985–1006
Sade N, del Mar R-W, Umnajkitikorn K, Blumwald E (2018) Stress-induced senescence and plant tolerance to abiotic stress. J Exp Bot 69:845–853
Sakai H, Honma T, Takashi A et al (2001) ARR1, a transcription factor for genes immediately responsive to cytokinins. Science 294:1519–1521
Salomé PA, To JPC, Kieber JJ, McClung CR (2006) Arabidopsis response regulators ARR3 and ARR4 play cytokinin-independent roles in the control of circadian period. Plant Cell 18:55–69
Schaller GE, Kieber JJ, Shiu S-H (2008) Two-component signaling elements and Histidyl-Aspartyl phosphorelays. Arabidopsis Book 6:e0112
Shi X, Rashotte AM (2012) Advances in upstream players of cytokinin phosphorelay: receptors and histidine phosphotransfer proteins. Plant Cell Rep 31:789–799
Singh A, Kushwaha HR, Soni P et al (2015) Tissue specific and abiotic stress regulated transcription of histidine kinases in plants is also influenced by diurnal rhythm. Front Plant Sci 6:711
Skubacz A, Daszkowska-Golec A, Szarejko I (2016) The role and regulation of ABI5 (ABA-insensitive 5) in plant development, abiotic stress responses and phytohormone crosstalk. Front Plant Sci 7:1884
Stock AM, Robinson VL, Goudreau PN (2000) Two-component signal transduction. Annu Rev Biochem 69:183–215
Su T, Wang P, Li H et al (2018) The Arabidopsis catalase triple mutant reveals important roles of catalases and peroxisome-derived signaling in plant development. J Integrat Plant Biol 60:591–607
Sun L, Zhang Q, Wu J et al (2014) Two rice authentic histidine phosphotransfer proteins, OsAHP1 and OsAHP2, mediate cytokinin signaling and stress responses in rice. Plant Physiol 165:335–345
Tardieu F, Simonneau T, Muller B (2018) The physiological basis of drought tolerance in crop plants: a scenario-dependent probabilistic approach. Annu Rev Plant Biol 69:733–759
Thu NBA, Hoang XLT, Nguyen TDH et al (2015) Differential expression of two-component system–related drought-responsive genes in two contrasting drought-tolerant soybean cultivars DT51 and MTD720 under well-watered and drought conditions. Plant Mol Biol Rep 33:1599–1610
Tizaoui K, Kchouk ME (2012) Genetic approaches for studying transgene inheritance and genetic recombination in three successive generations of transformed tobacco. Genet Mol Biol 35:640–649
Tran LSP, Shinozaki K, Yamaguchi-Shinozaki K (2010) Role of cytokinin responsive two-component system in ABA and osmotic stress signalings. Plant Signal Behav 5:148–150
Tran LSP, Urao T, Qin F et al (2007) Functional analysis of AHK1/ATHK1 and cytokinin receptor histidine kinases in response to abscisic acid, drought, and salt stress in Arabidopsis. Proc Natl Acad Sci 104:20623–20628
Ueguchi C, Koizumi H, Suzuki T, Mizuno T (2001) Novel family of sensor histidine kinase genes in Arabidopsis thaliana. Plant Cell Physiol 42:231–235
Ullah A, Manghwar H, Shaban M et al (2018) Phytohormones enhanced drought tolerance in plants: a coping strategy. Environ Sci Pollut Res 25:33103–33118
Urao T, Yamaguchi-Shinozaki K, Shinozaki K (2000) Two-component systems in plant signal transduction. Trends Plant Sci 5:67–74
Vaahtera L, Brosché M (2011) More than the sum of its parts—how to achieve a specific transcriptional response to abiotic stress. In: Plant Science. American Society of Plant Physiologists, pp 421–430
Valentine JS (1994) Dioxygen Reactions. In: Chemistry B (ed) Bertini I, Gray HB, Lippard SJ, Valentine JS. University Science Books, Mill Valley, pp 313–523
Verslues PE, Agarwal M, Katiyar-Agarwal S et al (2006) Erratum: methods and concepts in quantifying resistance to drought, salt and freezing, abiotic stresses that affect plant water status. Plant J 46:1092
Vescovi M, Riefler M, Gessuti M et al (2012) Programmed cell death induced by high levels of cytokinin in Arabidopsis cultured cells is mediated by the cytokinin receptor CRE1/AHK4. J Exp Bot 63:2825–2832
Wang CJ, Yang W, Wang C et al (2012) Induction of drought tolerance in cucumber plants by a consortium of three plant growth-promoting rhizobacterium strains. PLoS ONE 7:e52565
Weaver LM, Gan S, Quirino B, Amasino RM (1998) A comparison of the expression patterns of several senescence-associated genes in response to stress and hormone treatment. Plant Mol Biol 37:455–469
Yang L, Liu Q, Liu Z et al (2016) Arabidopsis C3HC4-RING finger E3 ubiquitin ligase AtAIRP4 positively regulates stress-responsive abscisic acid signaling. J Integr Plant Biol 58:67–80
Yu J, Yang L, Liu X et al (2016) Overexpression of poplar pyrabactin resistance-like abscisic acid receptors promotes abscisic acid sensitivity and drought resistance in transgenic Arabidopsis. PLoS ONE 11:e0168040
Zhang L, Wang Y, Zhang Q et al (2020) Overexpression of HbMBF1a, encoding multiprotein bridging factor 1 from the halophyte Hordeum brevisubulatum, confers salinity tolerance and ABA insensitivity to transgenic Arabidopsis thaliana. Plant Mol Biol 102:1–17
Zhao Y, Chan Z, Gao J et al (2016) ABA receptor PYL9 promotes drought resistance and leaf senescence. Proc Natl Acad Sci 113:1949–1954
Acknowledgements
This research is funded by Vietnam National University Ho Chi Minh City (VNU-HCM) under grant number B2017-28-02. XLTH was funded by Vingroup Joint Stock Company and supported by the Domestic Master/PhD Scholarship Programme of Vingroup Innovation Foundation (VINIF), Vingroup Big Data Institute (VINBIGDATA), code VINIF.2020.TS.09.
Author information
Authors and Affiliations
Contributions
NNC was responsible for investigation, data curation, formal analysis, visualization and writing original draft preparation. XLTH was responsible for conceptualization, methodology, writing and review. DHTN participated in investigation, data curation and writing. NCN was responsible for methodology and visualization. DTTT was involved in methodology. TBT and TTMN were involved in investigation. NBAT was involved in conceptualization and methodology. QTN was responsible for review and editing. NPT was responsible for project administration, supervision, conceptualization, validation, review and funding.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare 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.
Rights and permissions
About this article
Cite this article
Chuong, N.N., Hoang, X.L.T., Nghia, D.H.T. et al. Ectopic expression of GmHP08 enhances resistance of transgenic Arabidopsis toward drought stress. Plant Cell Rep 40, 819–834 (2021). https://doi.org/10.1007/s00299-021-02677-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00299-021-02677-6