Skip to main content
SpringerLink
Log in

Transcriptional analysis reveals sodium nitroprusside affects alfalfa in response to PEG-induced osmotic stress at germination stage

  • Original Article
  • Published:
Protoplasma Aims and scope Submit manuscript

Abstract

Drought is one of the most common environmental factors that affect alfalfa germination and development. Nitric oxide (NO) could mediate stress tolerance in plants. The goal of this study was to determine exogenous NO donor–mediated drought adaption molecular mechanisms during the alfalfa germination stage. In this study, physiological and transcriptome analyses were performed on 7 days of the growth period seedlings by sodium nitroprusside (SNP) and polyethylene glycol (PEG) treatment. The results showed that SNP supplementation alleviated malondialdehyde accumulation, increased levels of proline and soluble sugars, and enhanced antioxidant enzyme activity under osmotic stress conditions. RNA-Seq experiments identified 5828 genes exhibiting differential expression in seedlings treated with PEG, SNP, or SNP+PEG relative to seedlings treated with distilled water. Of these DEGs, 3235 were upregulated, and 2593 were downregulated relative to the controls. Fifteen DEGs were amplified by qRT-PCR to verify the changes in expression determined by RNA-Seq, revealing that PIF3, glnA, PLCG1, and RP-S11e exhibited enhanced expression under the SNP+PEG treatment. SNP was found to modulate redox homeostasis-related genes such as GSTs, SOD2, GPX, and RBOH, and triggered calcium signaling transduction. It also induced some key genes relating to the abscisic acid, ethylene, and auxin signaling transduction in response to PEG stress. Conversely, genes associated with secondary metabolite biosynthesis and the metabolism of starch and sucrose during osmotic stress were downregulated by SNP. These results provide new insights into SNP-mediated drought adaption mechanisms at transcriptome-wide in alfalfa and reveal key drought tolerance pathways in this species.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Ahmad P, Umar S, Sharma S (2010) Mechanism of free radical scavenging and role of phytohormones in plants under abiotic stresses. In: Ashraf M, Ozturk M, Ahmad M (eds) Plant adaptation and phytoremediation. Springer, Dordrecht, pp 99–118

    Chapter  Google Scholar 

  • Akram NA, Iqbal M, Muhammad A, Ashraf M, Al-Qurainy F, Shafiq S (2018) Aminolevulinic acid and nitric oxide regulate oxidative defense and secondary metabolisms in canola (Brassica napus L.) under drought stress. Protoplasma 255:163–174

    Article  CAS  PubMed  Google Scholar 

  • Anders S, Huber W (2010) Differential expression analysis for sequence count data. Genome Biol 11:R106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Aranjuelo I, Molero G, Erice G, Avice JC, Nogués S (2011) Plant physiology and proteomics reveals the leaf response to drought in alfalfa (Medicago sativa L). J Exp Bot 62:111–123

    Article  CAS  PubMed  Google Scholar 

  • Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1–15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ashraf M, Akram NA, Al-Qurainy F, Foolad MR (2011) Drought tolerance: roles of organic osmolytes, growth regulators and mineral nutrients. Adv Agron 111:249–296

    Article  CAS  Google Scholar 

  • Barrs HD, Weatherley PE (1962) A reexamination of the relative turgidity technique for estimating water deficit in leaves. Austral J Biol Sci 15:413–428

    Article  Google Scholar 

  • Barry CS, Giovannoni JJ (2006) Ripening in the tomato green-ripe mutant is inhibited by ectopic expression of a protein that disrupts ethylene signaling. Proc Natl Acad Sci U S A 103:7923–7928

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:305–307

    Article  Google Scholar 

  • Benjamini Y, Hochberg Y (2000) On the adaptive control of the false discovery rate in multiple testing with independent statistics. J Educ Behav Stat 25:66–83

    Article  Google Scholar 

  • Boriboonkaset T, Theerawitaya C, Yamada N, Pichakum A, Supaibulwatana K, Cha-um S, Takabe T, Kirdmanee C (2013) Regulation of some carbohydrate metabolism-related genes, starch and soluble sugar contents, photosynthetic activities and yield attributes of two contrasting rice genotypes subjected to salt stress. Protoplasma 250:1157–1167

    Article  CAS  PubMed  Google Scholar 

  • Castroluna A, Ruiz OM, Quiroga AM, Pedranzani HE (2014) Effects of salinity and drought stress on germination, biomass and growth in three varieties of Medicago sativa L. Avances en Investigación Agropecuaria 18:39–50

    Google Scholar 

  • Chaves MM (1991) Effects of water deficits on carbon assimilation. J Exp Bot 42:1–16

    Article  CAS  Google Scholar 

  • Chaves MM, Flexas J, Pinheiro C (2009) Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann Bot 103:551–560

    Article  CAS  PubMed  Google Scholar 

  • Chen H, Qualls RG, Miller GC (2002) Adaptive responses of Lepidium latifolium to soil flooding: biomass allocation, adventitious rooting, aerenchyma formation and ethylene production. Environ Exp Bot 48:119–128

    Article  Google Scholar 

  • Chen C, Qualls RG, Blank RR (2005) Effect of soil flooding on photosynthesis, carbohydrate partitioning and nutrient uptake in the invasive exotic Lepidium latifolium. Aquat Bot 82:250–268

    Article  CAS  Google Scholar 

  • Chen C, Letnik I, Hacham Y, Dobrev P, Ben-Daniel B, Vanková R, Amir R, Miller G (2014) ASCORBATE PEROXIDASE6 protects Arabidopsis desiccating and germinating seeds from stress and mediates cross talk between reactive oxygen species, abscisic acid, and auxin. Plant Physiol 166:370–383

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chen C, Li Q, Wang Q, Lu D, Zhang H, Wang J, Fu R (2017) Transcriptional profiling provides new insights into the role of nitric oxide in enhancing Ganoderma oregonense resistance to heat stress. Sci Rep 7:15694

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Christianson JA, Llewellyn DJ, Dennis ES, Wilson IW (2010) Comparisons of early transcriptome responses to low-oxygen environments in three dicotyledonous plant species. Plant Signal Behav 5:1006–1009

    Article  PubMed  PubMed Central  Google Scholar 

  • Correa-Aragunde N, Graziano M, Lamattina L (2004) Nitric oxide plays a central role in determining lateral root development in tomato. Planta 218:900–905

    Article  CAS  PubMed  Google Scholar 

  • Cramer GR, Urano K, Delrot S, Pezzotti M, Shinozaki K (2011) Effects of abiotic stress on plants: a systems biology perspective. BMC Plant Bio 11:163

    Article  Google Scholar 

  • Dubois M, Gilles K, Hamilton JK, Rebers PA, Smith F (1951) A colorimetric method for the determination of sugars. Nature 168:167

    Article  CAS  PubMed  Google Scholar 

  • Fan HF, Du CX, Ding L, Xu YL (2013) Effects of nitric oxide on the germination of cucumber seeds and antioxidant enzymes under salinity stress. Acta Physiol Plant 35:2707–2719

    Article  CAS  Google Scholar 

  • Fancy NN, Bahlmann AK, Loake GJ (2017) Nitric oxide function in plant abiotic stress. Plant Cell Environ 40:462–472

    Article  CAS  PubMed  Google Scholar 

  • Ferreres F, Figueiredo R, Bettencourt S, Carqueijeiro I, Oliveira J, Gil-Izquierdo A, Pereira DM, Valent OP, Andrade PB, Duarte P, Barceló AR, Sottomayor M (2011) Identification of phenolic compounds in isolated vacuoles of the medicinal plant Catharanthus roseus and their interaction with vacuolar class III peroxidase: an H2O2 affair? J Exp Bot 62:2841–2854

    Article  CAS  PubMed  Google Scholar 

  • Fini A, Guidi L, Ferrini F, Brunetti C, Di Ferdinando M, Biricolti S, Pollastria S, Calamia L, Tattini M (2012) Drought stress has contrasting effects on antioxidant enzymes activity and phenylpropanoid biosynthesis in Fraxinus ornus leaves: an excess light stress affair? J Plant Physiol 169:929–939

    Article  CAS  PubMed  Google Scholar 

  • Gong B, Miao L, Kong W, Bai J, Wang X, Wei M, Shi Q (2014) Nitric oxide, as a downstream signal, plays vital role in auxin induced cucumber tolerance to sodic alkaline stress. Plant Physiol Bioch 83:258–266

    Article  CAS  Google Scholar 

  • Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L et al (2013) Trinity: reconstructing a full-length transcriptome without a genome from RNA-Seq data. Nat Biotechnol 29:644–652

    Article  CAS  Google Scholar 

  • Groß F, Durner J, Gaupels F (2013) Nitric oxide, antioxidants and prooxidants in plant defense responses. Front Plant Sci 4:419

    Article  PubMed  PubMed Central  Google Scholar 

  • Grün S, Lindermayr C, Sell S, Durner J (2006) Nitric oxide and gene regulation in plants. J Exp Bot 57:507–516

    Article  PubMed  CAS  Google Scholar 

  • Hodges DM, DeLong JM, Forney CF, Prange RK (1999) Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 207:604–611

    Article  CAS  Google Scholar 

  • Hopper DW, Ghan R, Schlauch KA, Cramer GR (2016) Transcriptomic network analyses of leaf dehydration responses identify highly connected ABA and ethylene signaling hubs in three grapevine species differing in drought tolerance. BMC Plant Bio 16:118

    Article  CAS  Google Scholar 

  • Hu XY, Neill SJ, Tang ZC, Cai WM (2005) Nitric oxide mediates gravitropic bending in soybean roots. Plant Physiol 137:663–670

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jacobsen JV, Barrero JM, Hughes T, Julkowska M, Taylor JM, Xu Q, Gubler F (2013) Roles for blue light, jasmonate and nitric oxide in the regulation of dormancy and germination in wheat grain (Triticum aestivum L.). Planta 238:121–138

    Article  CAS  PubMed  Google Scholar 

  • Kanehisa M, Araki M, Goto S, Hattori M, Hirakawa M, Itoh M, Katayama T, Kawashima S, Okuda S, Tokimatsu T, Yamanishi Y (2008) KEGG for linking genomes to life and the environment. Nucleic Acids Res 36:480–484

    Article  CAS  Google Scholar 

  • Kasote DM, Katyare SS, Hegde MV, Bae H (2015) Significance of antioxidant potential of plants and its relevance to therapeutic applications. Int J Biol Sci 11:982–991

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kurusu T, Kuchitsu K, Tada Y (2015) Plant signaling networks involving Ca2+ and Rboh/Nox-mediated ROS production under salinity stress. Front Plant Sci 6:27

    Article  Google Scholar 

  • Langmead B, Trapnell C, Pop M, Salzberg SL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10:R25

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lei Y, Xu Y, Hettenhausen C, Lu C, Shen G, Zhang C, Li J, Song J, Lin H, Wu J (2018) Comparative analysis of alfalfa (Medicago sativa L.) leaf transcriptomes reveals genotype-specific salt tolerance mechanisms. BMC Plant Biol 18:35

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Leterrier M, Valderrama R, Chaki M, Araki M, Palma JM, Barroso JB, Corpas FJ (2012) Function of nitric oxide under environmental stress conditions. In: Khan NA, Nazar R, Iqbal N, Anjum NA (eds) Phytohormones and abiotic stress tolerance in plants. Springer, Berlin, pp 99–113

    Chapter  Google Scholar 

  • Li L, Wang Y, Shen W (2012) Roles of hydrogen sulfide and nitric oxide in the alleviation of cadmium-induced oxidative damage in alfalfa seedling roots. Biometals 25:617–631

    Article  CAS  PubMed  Google Scholar 

  • Li Q, Huang WL, Xiong C, Zhao J (2018) Transcriptome analysis reveals the role of nitric oxide in Pleurotus eryngii responses to Cd2+ stress. Chemosphere 201:294–302

    Article  CAS  PubMed  Google Scholar 

  • Liao W, Huang G, Yu J, Zhang M (2012) Nitric oxide and hydrogen peroxide alleviate drought stress in marigold explants and promote its adventitious root development. Plant Physiol Bioch 58:6–15

    Article  CAS  Google Scholar 

  • Liu S, Dong YJ, Xu LL, Kong J (2014) Effects of foliar applications of nitric oxide and salicylic acid on salt-induced changes in photosynthesis and antioxidative metabolism of cotton seedlings. Plant Growth Regul 73:67–78

    Article  CAS  Google Scholar 

  • Livak KJ, Schnmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-∆∆CT method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Lombardo MC, Graziano M, Polacco JC, Lamattina L (2006) Nitric oxide functions as a positive regulator of root hair development. Plant Signal Behav 1:28–33

    Article  PubMed  PubMed Central  Google Scholar 

  • Lu XY, Kim H, Zhong SL, Chen HB, Hu ZQ, Zhou BY (2014) De novo transcriptome assembly for rudimentary leaves in Litchi chinesis Sonn. and identification of differentially expressed genes in response to reactive oxygen species. BMC Genomics 15:805

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Luo X, Bai X, Sun XL, Zhu D, Liu BH, Ji W, Cai H, Cao L, Wu J, Hu MR, Liu X, Lili T, Zhu AY (2013) Expression of wild soybean WRKY20 in Arabidopsis enhances drought tolerance and regulates ABA signaling. J Exp Bot 64:2155–2169

    Article  CAS  PubMed  Google Scholar 

  • Ma X, Wang P, Zhou S, Sun Y, Liu N, Li X, Hou Y (2015) De novo transcriptome sequencing and comprehensive analysis of the drought-responsive genes in the desert plant Cynanchum komarovii. BMC Genomics 16:753

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mao X, Cai T, Olyarchuk JG, Wei L (2005) Automated genome annotation and pathway identification using the KEGG Orthology (KO) as a controlled vocabulary. Bioinformatics 21:3787–3793

    Article  CAS  PubMed  Google Scholar 

  • Mao J, Li W, Mi B, Dawuda MM, Calderón-Urrea A, Gh Z, Zhang Y, Chen B (2017) Different exogenous sugars affect the hormone signal pathway and sugar metabolism in “Red Globe” (Vitis vinifera L.) plantlets grown in vitro as shown by transcriptomic analysis. Planta 246:537–552

    Article  CAS  PubMed  Google Scholar 

  • Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R (2009) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ 33:453–467

    Article  PubMed  CAS  Google Scholar 

  • Mishina T, Lamb C, Zeier J (2007) Expression of a nitric oxide degrading enzyme induces a senescence program in Arabidopsis. Plant Cell Environ 30:39–52

    Article  CAS  PubMed  Google Scholar 

  • Murcia G, Fontana A, Pontin M, Baraldi R, Bertazza G, Piccoli P (2017) ABA and GA3 regulate the synthesis of primary and secondary metabolites related to alleviation from biotic and abiotic stresses in grapevine. Phytochemistry 135:34–52

    Article  CAS  PubMed  Google Scholar 

  • Najafabadi MY, Ehsanzadeh P (2017) Photosynthetic and antioxidative upregulation in drought-stressed sesame (Sesamum indicum L.) subjected to foliar-applied salicylic acid. Photosynthetica 55:611–622

    Article  CAS  Google Scholar 

  • Orman-Ligeza B, Parizot B, de Rycke R, Fernandez A, Himschoot E, Van Breusegem F, Bennett MJ, Périlleux C, Beeckman T, Draye X (2016) RBOH-mediated ROS production facilitates lateral root emergence in Arabidopsis. Development 143:3328–3339

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ötvös K, Pasternak TP, Miskolczi P, Domoki M, Dorjgotov D, Sz Cs A, Bottka S, Dudits D, Fehér A (2005) Nitric oxide is required for, and promotes auxin-mediated activation of, cell division and embryogenic cell formation but does not influence cell cycle progression in alfalfa cell cultures. Plant J 43:849–860

    Article  PubMed  CAS  Google Scholar 

  • Pagliano C, Saracco G, Barber J (2013) Structural, functional and auxiliary proteins of photosystem II. Photosynth Res 116:167–188

    Article  CAS  PubMed  Google Scholar 

  • Pantin F, Renaud J, Barbier F, Vavasseur A, Le Thiec D, Rose C, Bariac T, Casson S, McLachlan DH, Hetherington AM, Muller B, Simonneau T (2013) Developmental priming of stomatal sensitivity to abscisic acid by leaf microclimate. Curr Biol 23:1805–1811

    Article  CAS  PubMed  Google Scholar 

  • Sakihama Y, Cohen MF, Grace SC, Yamasaki H (2002) Plant phenolic antioxidant and prooxidant activities: phenolics-induced oxidative damage mediated by metals in plants. Toxicology 177:67–80

    Article  CAS  PubMed  Google Scholar 

  • Samac DA, Bucciarelli B, Miller SS, Yang SS, O Rourke JA, Shin S, Vance CP (2015) Transgene silencing of sucrose synthase in alfalfa (Medicago sativa L.) stem vascular tissue suggests a role for invertase in cell wall cellulose synthesis. BMC Plant Bio 15:283

    Article  CAS  Google Scholar 

  • Sánchez-Rodríguez J, Pérez P, Martínez-Carrasco R (1999) Photosynthesis, carbohydrate levels and chlorophyll fluorescence-estimated intercellular CO2 in water-stressed Casuarina equisetifolia Forst. & Forst. Plant Cell Environ 22:867–873

    Article  Google Scholar 

  • Sanz L, Albertos P, Mateos I, Sánchez-Vicente I, Lechón T, Fernández-Marcos M, Lorenzo O (2015) Nitric oxide (NO) and phytohormones crosstalk during early plant development. J Exp Bot 66:2857–2868

    Article  CAS  PubMed  Google Scholar 

  • Serpa V, Vernal J, Lamattina L, Grotewold E, Cassia R, Terenzi H (2007) Inhibition of AtMYB2 DNA-binding by nitric oxide involves cysteine S-nitrosylation. Biochem Bioph Res Co 361:1048–1053

    Article  CAS  Google Scholar 

  • Shafiq S, Akram NA, Ashraf M, Arshad A (2014) Synergistic effects of drought and ascorbic acid on growth, mineral nutrients and oxidative defense system in canola (Brassica napus L.) plants. Acta Physiol Plant 36:1539–1553

    Article  CAS  Google Scholar 

  • Shi H, Ye T, Zhu J, Chan Z (2014) Constitutive production of nitric oxide leads to enhanced drought stress resistance and extensive transcriptional reprogramming in Arabidopsis. J Exp Bot 65:4119–4131

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Silveira NM, Hancock JT, Frungillo L, Siasou E, Marcos FCC, Salgado I, Machado EC, Ribeiro RV (2017) Evidence towards the involvement of nitric oxide in drought tolerance of sugarcane. Plant Physiol Biochem 115:354–359

    Article  CAS  PubMed  Google Scholar 

  • Simontacchi M, Galatro A, Ramos-Artuso F, Santa-María GE (2015) Plant survival in a changing environment: the role of nitric oxide in plant responses to abiotic stress. Front Plant Sci 6:977

    Article  PubMed  PubMed Central  Google Scholar 

  • Singh PK, Indoliya Y, Chauhan AS, Singh SP, Singh AP, Dwivedi S, Tripathi RD, Chakrabarty D (2017) Nitric oxide mediated transcriptional modulation enhances plant adaptive responses to arsenic stress. Sci Rep 7:3592

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Spartz AK, Lee SH, Wenger JP, Gonzalez N, Itoh H, Inzé D, Peer WA, Murphy AS, Overvoorde PJ, Gray WM (2012) The SAUR19 subfamily of SMALL AUXIN UP RNA genes promote cell expansion. Plant J 70:978–990

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun CL, Lu LL, Liu LJ, Liu WJ, Yu Y, Liu XX, Hu Y, Jin CW, Lin XY (2014) Nitrate reductase-mediated early nitric oxide burst alleviates oxidative damage induced by aluminum through enhancement of antioxidant defenses in roots of wheat (Triticum aestivum). New Phytol 201:1240–1250

    Article  CAS  PubMed  Google Scholar 

  • Tattini M, Loreto F, Fini A, Guidi L, Brunetti C, Velikova V, Gori A, Ferrini F (2015) Isoprenoids and phenylpropanoids are part of the antioxidant defense orchestrated daily by drought-stressed Platanus×acerifolia plants during Mediterranean summers. New Phytol 207:613–626

    Article  CAS  PubMed  Google Scholar 

  • Terrile MC, París R, Calderón-Villalobos LIA, Iglesias MJ, Lamattina L, Estelle M, Casalongué CA (2012) Nitric oxide influences auxin signaling through S-nitrosylation of the Arabidopsis TRANSPORT INHIBITORRESPONSE 1 auxin receptor. Plant J 70:492–500

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tewari RK, Kim S, Hahn E, Paek K (2008) Involvement of nitric oxide-induced NADPH oxidase in adventitious root growth and antioxidant defense in Panax ginseng. Plant Biotechnol Rep 2:113–122

    Article  Google Scholar 

  • Tian QY, Sun DH, Zhao MG, Zhang WH (2007) Inhibition of nitric oxide synthase (NOS) underlies aluminum-induced inhibition of root elongation in Hibiscus moscheutos. New Phytol 174:322–331

    Article  CAS  PubMed  Google Scholar 

  • Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, Baren MJV (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28:511–515

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Trchounian A, Petrosyan M, Sahakyan N (2016) Plant cell redox homeostasis and reactive oxygen species. In: Gupta D, Palma J, Corpas F (eds) Redox state as a central regulator of plant-cell stress responses. Springer, Cham, pp 25–50

    Chapter  Google Scholar 

  • Wang W, Kim Y, Lee H, Kim K, Deng X, Kwak S (2009) Analysis of antioxidant enzyme activity during germination of alfalfa under salt and drought stresses. Plant Physiol Bioch 47:570–577

    Article  CAS  Google Scholar 

  • Wang Y, Li L, Cui W, Xu S, Shen W, Wang R (2012) Hydrogen sulfide enhances alfalfa (Medicago sativa) tolerance against salinity during seed germination by nitric oxide pathway. Plant Soil 351:107–119

    Article  CAS  Google Scholar 

  • Wang PC, Zhu JK, Lang ZB (2015) Nitric oxide suppresses the inhibitory effect of abscisic acid on seed germination by S-nitrosylation of SnRK2 proteins. Plant Signal Behav 10:e1031939

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wang H, Huang J, Li Y, Li C, Hou J, Liang W (2016) Involvement of nitric oxide-mediated alternative pathway in tolerance of wheat to drought stress by optimizing photosynthesis. Plant Cell Rep 35:2033–2044

    Article  CAS  PubMed  Google Scholar 

  • Wu S, Hu C, Tan Q, Xu S, Sun X (2017) Nitric oxide mediates molybdenum-induced antioxidant defense in wheat under drought stress. Front Plant Sci 8:1085

    Article  PubMed  PubMed Central  Google Scholar 

  • Xu Y, Burgess P, Zhang X, Huang B (2016) Enhancing cytokinin synthesis by overexpressing ipt alleviated drought inhibition of root growth through activating ROS-scavenging systems in Agrostis stolonifera. J Exp Bot 67(6):1979–1992

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu M, Lamattina L, Spoel SH, Loake GJ (2014) Nitric oxide function in plant biology: a redox cue in deconvolution. New Phytol 202:1142–1156

    Article  CAS  PubMed  Google Scholar 

  • Zhang J, Jia W, Yang J, Ismail AM (2006) Role of ABA in integrating plant responses to drought and salt stresses. Field Crop Res 97(1):111–119

    Article  Google Scholar 

  • Zhang G, Chen M, Li L, Xu Z, Chen X, Guo J, Ma Y (2009) Overexpression of the soybean GmERF3 gene, an AP2/ERF type transcription factor for increased tolerances to salt, drought, and diseases in transgenic tobacco. J Exp Bot 13:3781–3796

    Article  CAS  Google Scholar 

  • Zheng L, Meng Y, Ma J, Zhao X, Cheng T, Ji J, Chang E, Meng C, Deng N, Chen L, Shi S, Jiang Z (2015) Transcriptomic analysis reveals importance of ROS and phytohormones in response to short-term salinity stress in Populus tomentosa. Front Plant Sci 6:678

    Article  PubMed  PubMed Central  Google Scholar 

  • Zheng Y, Jiao C, Sun H, Rosli HG, Pombo MA, Zhang P, Banf M, Dai X, Martin GB, Giovannoni JJ, Zhao PX, Rhee SY, Fei Z (2016) iTAK: a program for genome-wide prediction and classification of plant transcription factors, transcriptional regulators, and protein kinases. Mol Plant 9:1667–1670

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

Funding for this study was provided by the National Natural Science Foundation of China (NSFC) (No. 31560663).

Author information

Author notes

  1. Ying Zhao & Xiaohong Wei

    Present address: College of Life Science and Technology, Gansu Agricultural University, No. 1 Yingmen Village, Anning District, Lanzhou, 730070, Gansu Province, People’s Republic of China

Authors and Affiliations

  1. College of Business Administration, Kent State University, Kent, OH, USA

    Yu Long

  2. College of Agronomy, Gansu Agricultural University, Lanzhou, China

    Xiangzhuo Ji

Authors
  1. Ying Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xiaohong Wei
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yu Long
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xiangzhuo Ji
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

XW designed the research plan. YZ performed the experiments. YZ and XJ analyzed the data. YZ draft the manuscript. XW and YL contributed suggestions for manuscript revision.

Corresponding author

Correspondence to Xiaohong Wei.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Handling Editor: Bhumi Nath Tripathi

Publisher’s note

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

Electronic supplementary material

ESM 1

(XLS 56 kb)

ESM 2

(DOCX 10879 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhao, Y., Wei, X., Long, Y. et al. Transcriptional analysis reveals sodium nitroprusside affects alfalfa in response to PEG-induced osmotic stress at germination stage. Protoplasma 257, 1345–1358 (2020). https://doi.org/10.1007/s00709-020-01508-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00709-020-01508-x

Keywords

Search

Navigation