Abstract
Integrated signaling network involving abscisic acid (ABA), nitric oxide (NO), and indole-acetic acid (IAA) controls root morphogenesis during salt stress by a mechanism still poorly understood. The present data unveiled an ABA-NO-IAA interaction underlying radicular morphological responses to salinity. Three Solanum lycopersicum genotypes were analyzed: wild type, ABA-insensitive mutant (sitiens), and auxin-responsive (DR5::GUS) plants. Nitric oxide fluorescence, nitrate reductase activity, auxin signaling, and some molecular analyses were performed. Pharmacological inhibitors and NO donor sodium nitroprusside were also used to evaluate NaCl-induced root morphological responses. Sodium nitroprusside inhibited primary root length, increased lateral root emergence, and rescued salt inhibited lateral root growth. The results showed that NO integrates the ABA-IAA signaling network of root system responses under salt stress, involving: (a) ABA and molybdenum-dependent enzymes as responsible for salt-induced NO production; (b) modulations of the plasma membrane H+-ATPase coupling and isoforms differential expression; and (c) ABA-mediated and NO-dependent antioxidative enzymes activities.
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Astier J, Gross I, Durner J (2018) Nitric oxide production in plants: an update. J. Exp. Bot. 69(14):3401–3411
Astier J, Lindermayr C (2012) Nitric oxide-dependent posttranslational modification in plants: an update. Int. J. Mol. Sci. 13(11):15193–15208
Bartels D, Sunkar R (2005) Drought and salt tolerance in plants. Crit. Rev. Plant Sci. 24(1):23–58
Bethke PC, Badger MR, Jones RL (2004) Apoplastic synthesis of nitric oxide by plant tissues. Plant Cell. https://doi.org/10.1105/tpc.017822
Binzel ML (1995) NaCl-induced accumulation of tonoplast and plasma membrane H+-ATPase message in tomato. Physiol Plant. https://doi.org/10.1111/j.1399-3054.1995.tb00990.x
Blumwald E, Aharon GS, Apse MP (2000) Sodium transport in plant cells. Biochim Biophys Acta Biomembr 1465(1–2):140–151
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. https://doi.org/10.1016/0003-2697(76)90527-3
Bright J, Desikan R, Hancock JT et al (2006) ABA-induced NO generation and stomatal closure in Arabidopsis are dependent on H2O2 synthesis. Plant J. https://doi.org/10.1111/j.1365-313X.2005.02615.x
Correa-Aragunde N, Foresi N, Lamattina L (2015) Nitric oxide is a ubiquitous signal for maintaining redox balance in plant cells: regulation of ascorbate peroxidase as a case study. J. Exp Bot 66(10):2913–2921
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. https://doi.org/10.1007/s00425-003-1172-7
De Azevedo Neto AD, Prisco JT, Enéas-Filho J, Abreu CEB, Gomes-Filho E (2006) Effect of salt stress on antioxidative enzymes and lipid peroxidation in leaves and roots of salt-tolerant and salt-sensitive maize genotypes. Environ Exp Bot. https://doi.org/10.1016/j.envexpbot.2005.01.008
Dhindsa RS, Plumb-dhindsa P, Thorpe TA (1981) Leaf senescence: correlated with increased levels of membrane permeability and lipid peroxidation, and decreased levels of superoxide dismutase and catalase. J Exp Bot 32:93–101. https://doi.org/10.1093/jxb/32.1.93
Domingos P, Prado AM, Wong A, Gehring C, Feijó JA (2015) Nitric oxide: a multitasked signaling gas in plants. Mol Plant 8(4):506–520
Duan L, Dietrich D, Ng CH, Chan PMY, Bhalerao R, Bennet MJ, Dinneny JR (2013) Endodermal ABA signaling promotes lateral root quiescence during salt stress in Arabidopsis seedlings. Plant Cell. https://doi.org/10.1105/tpc.112.107227
Dunlap JR, Binzel ML (1996) NaCl reduces indole-3-acetic acid levels in the roots of tomato plants independent of stress-induced abscisic acid. Plant Physiol. https://doi.org/10.1104/pp.112.1.379
Facanha AR, De Meis L (1995) Inhibition of maize root H+-ATPase by fluoride and fluoroaluminate complexes. Plant Physiol 108:241–246
FAO (2015) Status of the world’s soil resources. FAO, Roma
Fernández-marcos M, Sanz L, Lewis DR, Muday GK, Lorenzo O (2011) Nitric oxide causes root apical meristem defects and growth inhibition while reducing PIN-FORMED 1 (PIN1) -dependent acropetal auxin transport. Proc Natl Acad Sci. https://doi.org/10.1073/pnas.1108644108
Galvan-Ampudia CS, Julkowska MM, Darwish E, Gandullo J, Korver RA, Brunoud G, Haring MA, Munnik T, Vernoux T, Testerink C (2013) Halotropism is a response of plant roots to avoid a saline environment. Curr Biol. https://doi.org/10.1016/j.cub.2013.08.042
Guo FQ, Okamoto M, Crawford NM (2003) Identification of a plant nitric oxide synthase gene involved in hormonal signaling. Science. https://doi.org/10.1126/science.1086770
Gupta KJ, Fernie AR, Kaiser WM, van Dongen JT (2011) On the origins of nitric oxide. Trends Plant Sci 16(3):160–168
Harrison E, Burbidge A, Okyere JP, Thompson AJ, Taylor IB (2011) Identification of the tomato ABA-deficient mutant sitiens as a member of the ABA-aldehyde oxidase gene family using genetic and genomic analysis. Plant Growth Regul. https://doi.org/10.1007/s10725-010-9550-1
Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Circular. California agricultural experiment station, 347 (2nd edit)
Janicka-Russak M (2011) Plant plasma membrane H+-ATPase in adaptation of plants to abiotic stresses. In: Shanker AK, Venkateswarlu B (eds) Abiotic stress response in plants - physiological, biochemical and genetic perspectives. Intech, Croatia, pp 197–218
Janicka-Russak M, Kłobus G (2007) Modification of plasma membrane and vacuolar H+-ATPases in response to NaCl and ABA. J Plant Physiol. https://doi.org/10.1016/j.jplph.2006.01.014
Jaworski EG (1971) Nitrate reductase assay in intact plant tissues. Biochem Biophys Res Commun. https://doi.org/10.1016/S0006-291X(71)80010-4
Jiang M, Zhang J (2001) Effect of abscisic acid on active oxygen species, antioxidative defence system and oxidative damage in leaves of maize seedlings. Plant Cell Physiol. https://doi.org/10.1093/pcp/pce162
Jiang M, Zhang J (2002) Role of abscisic acid in water stress-induced antioxidant defense in leaves of maize seedlings. Free Radic Res. https://doi.org/10.1080/1071576021000006563
Julkowska MM, Hoefsloot HCJ, Mol S, Feron R, de Boer G-J, Haring MA, Testerink C (2014) Capturing arabidopsis root architecture dynamics with root-fit reveals diversity in responses to salinity. Plant Physiol. https://doi.org/10.1104/pp.114.248963
Jung JKH, McCouch S (2013) Getting to the roots of it: genetic and hormonal control of root architecture. Front. Plant Sci 4:186
Kalampanayil BD, Wimmers LE (2001) Identification and characterization of a salt-stress-induced plasma membrane H+-ATPase in tomato. Plant Cell Environ 24:999–1000
Koevoets IT, Venema JH, Elzenga JTM, Testerink C (2016) Roots withstanding their environment: exploiting root system architecture responses to abiotic stress to improve crop tolerance. Front Plant Sci 7:1335
Kolbert Z, Barroso JB, Brouquisse R et al (2019) A forty year journey: the generation and roles of NO in plants. Nitric Oxide Biol Chem 93:53–70
Kolbert Z, Bartha B, Erdei L (2008) Exogenous auxin-induced NO synthesis is nitrate reductase-associated in Arabidopsis thaliana root primordia. J Plant Physiol. https://doi.org/10.1016/j.jplph.2007.07.019
Lindermayr C (2018) Crosstalk between reactive oxygen species and nitric oxide in plants: key role of S-nitrosoglutathione reductase. Free Radic Biol Med 122:110–115
Liu W, Li RJ, Han TT, Cai W, Fu Z-W, Lu Y-T (2015) Salt stress reduces root meristem size by nitric oxidemediated modulation of auxin accumulation and signaling in Arabidopsis. Plant Physiol. https://doi.org/10.1104/pp.15.00030
Lozano-Juste J, León J (2010) Enhanced abscisic acid-mediated responses in nia1nia2noa1-2 Triple mutant impaired in NIA/NR- and AtNOA1-dependent nitric oxide biosynthesis in Arabidopsis. Plant Physiol. https://doi.org/10.1104/pp.109.148023
Lu C, Chen MX, Liu R, Zhang L, Hou X, Liu S, Ding X, Jiang Y, Xu J, Zhang J, Zhao X, Liu Y-G (2019) Abscisic acid regulates auxin distribution to mediate maize lateral root development under salt stress. Front Plant Sci. https://doi.org/10.3389/fpls.2019.00716
Lu S, Zhuo C, Wang X, Guo Z (2014) Nitrate reductase (NR)-dependent NO production mediates ABA-and H2O2-induced antioxidant enzymes. Plant Physiol Biochem 74:9–15
Mäkelä P, Kontturi M, Pehu E, Somersalo S (1999) Photosynthetic response of drought- and salt-stressed tomato and turnip rape plants to foliar-applied glycinebetaine. Physiol Plant 105:45–50. https://doi.org/10.1034/j.1399-3054.1999.105108.x
McAdam SAM, Brodribb TJ, Ross JJ (2016) Shoot-derived abscisic acid promotes root growth. Plant Cell Environ 39:652–659. https://doi.org/10.1111/pce.12669
Melo NKG, Bianchetti RE, Lira BS, Oliveira PMR, Zuccarelli R, Dias DLO, Demarco D, Peres LEP, Rossi M, Freschi L (2016) Nitric oxide, ethylene, and auxin cross talk mediates greening and plastid development in deetiolating tomato seedlings. Plant Physiol. https://doi.org/10.1104/pp.16.00023
Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681. https://doi.org/10.1146/annurev.arplant.59.032607.092911
Mur LAJ, Mandon J, Persijn S et al (2013) Nitric oxide in plants: an assessment of the current state of knowledge. AoB Plants 5:pls052. https://doi.org/10.1093/aobpla/pls052
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. https://doi.org/10.1242/dev.136465
Ozfidan C, Turkan I, Sekmen AH, Seckin B (2012) Abscisic acid-regulated responses of aba2-1 under osmotic stress: the abscisic acid-inducible antioxidant defence system and reactive oxygen species production. Plant Biol. https://doi.org/10.1111/j.1438-8677.2011.00496.x
Paez-Valencia J, Sanchez-Lares J, Marsh E et al (2013) Enhanced proton translocating pyrophosphatase activity improves nitrogen use efficiency in romaine lettuce. Plant Physiol. https://doi.org/10.1104/pp.112.212852
Pérez-Torres CA, López-Bucio J, Cruz-Ramírez A, Ibarra-Laclette E, Dharmasiri S, Estelle M, Herrera-Estrella L (2008) Phosphate availability alters lateral root development in Arabidopsis by modulating auxin sensitivity via a mechanism involving the TIR1 auxin receptor. Plant Cell. https://doi.org/10.1105/tpc.108.058719
Pfaffl MW, Horgan GW, Dempfle L (2002) Relative expression software tool (REST©) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 30(9):e36. https://doi.org/10.1093/nar/30.9.e36
Qiao W, Li C, Fan LM (2014) Cross-talk between nitric oxide and hydrogen peroxide in plant responses to abiotic stresses. Environ Exp Bot 100:84–93
Reichheld JP, Vernoux T, Lardon F, Van Montagu, Inzé D (1999) Specific checkpoints regulate plant cell cycle progression in response to oxidative stress. Plant J. https://doi.org/10.1046/j.1365-313X.1999.00413.x
Rock CD, Sun X (2005) Crosstalk between ABA and auxin signaling pathways in roots of Arabidopsis thaliana (L.) Heynh. Planta. https://doi.org/10.1007/s00425-005-1521-9
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
Schopfer P (2001) Hydroxyl radical-induced cell-wall loosening in vitro and in vivo: Implications for the control of elongation growth. Plant J. https://doi.org/10.1046/j.1365-313x.2001.01187.x
Stohr C (2002) Generation and possible roles of NO in plant roots and their apoplastic space. J Exp Bot. https://doi.org/10.1093/jxb/erf110
Tivendale ND, Ross JJ, Cohen JD (2014) The shifting paradigms of auxin biosynthesis. Trends Plant Sci 19:44–51
Ulmasov T, Hagen G, Guilfoyle TJ (1997) ARF1, a transcription factor that binds to auxin response elements. Science. https://doi.org/10.1126/science.276.5320.1865
Vasquez-tello A, Zuily-fodil Y, Thi ATP, Da Silva JBV (1990) Electrolyte and Pi leakages and soluble sugar content as physiological tests for screening resistance to water stress in Phaseolus and Vigna species. J Exp Bot 41:827–832. https://doi.org/10.1093/jxb/41.7.827
Vidal EA, Alvarez JM, Araus V, Riveras E, Brooks MD, Krouk G, Ruffel S, Lejay L, Crawford NM, Coruzzi GM, Gutiérrez RA (2020) Nitrate 2020: Thirty years from transport to signaling networks. Plant Cell. https://doi.org/10.1105/tpc.19.00748
Wakeel A, Hanstein S, Pitann B, Schubert S (2010) Hydrolytic and pumping activity of H+-ATPase from leaves of sugar beet (Beta vulgaris L.) as affected by salt stress. J Plant Physiol. https://doi.org/10.1016/j.jplph.2009.12.018
Wang H, Xiao W, Niu Y, Chongwei Jin, Chai R, Tang C, Zhang Y (2013) Nitric oxide enhances development of lateral roots in tomato (Solanum lycopersicum L.) under elevated carbon dioxide. Planta. https://doi.org/10.1007/s00425-012-1763-2
Wang R, Tischner R, Gutiérrez RA, Hoffman M, Xing X, Chen M, Coruzzi G, Crawford NM (2004) Genomic analysis of the nitrate response using a nitrate reductase-null mutant of Arabidopsis. Plant Physiol. https://doi.org/10.1104/pp.104.044610
Wang Y, Li K, Li X (2009) Auxin redistribution modulates plastic development of root system architecture under salt stress in Arabidopsis thaliana. J Plant Physiol. https://doi.org/10.1016/j.jplph.2009.04.009
Wang Y, Zhang W, Li K, Sun F, Han C, Wang Y, Li X (2008) Salt-induced plasticity of root hair development is caused by ion disequilibrium in Arabidopsis thaliana. J Plant Res. https://doi.org/10.1007/s10265-007-0123-y
West G, Inzé D, Beemster GTS (2004) Cell cycle modulation in the response of the primary root of Arabidopsis to salt stress. Plant Physiol. https://doi.org/10.1104/pp.104.040022
Xia XJ, Zhou YH, Shi K, Zhou J, Foyer CH, Yu J-Q (2015) Interplay between reactive oxygen species and hormones in the control of plant development and stress tolerance. J Exp Bot 66:2839–2856
Xie Y, Mao Y, Lai D, Zhang W, Zheng T, Shen W (2013) Roles of NIA/NR/NOA1-dependent nitric oxide production and HY1 expression in the modulation of Arabidopsis salt tolerance. J Exp Bot. https://doi.org/10.1093/jxb/ert149
Xu W, Jia L, Shi W, Liang J, Zhou F, Li Q, Zhang J (2013) Abscisic acid accumulation modulates auxin transport in the root tip to enhance proton secretion for maintaining root growth under moderate water stress. New Phytol. https://doi.org/10.1111/nph.12004
Yamaguchi M, Sharp RE (2010) Complexity and coordination of root growth at low water potentials: recent advances from transcriptomic and proteomic analyses. Plant Cell Environ. https://doi.org/10.1111/j.1365-3040.2009.02064.x
Zandonadi DB, Santos MP, Dobbss LB et al (2010) Nitric oxide mediates humic acids-induced root development and plasma membrane H+-ATPase activation. Planta. https://doi.org/10.1007/s00425-010-1106-0
Zhang F, Wang Y, Wang D (2007) Role of nitric oxide and hydrogen peroxide during the salt resistance response. Plant Signal Behav. https://doi.org/10.4161/psb.2.6.4466
Zhang H, Forde BG (1998) An Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture. Science. https://doi.org/10.1126/science.279.5349.407
Zhang Y, Tan J, Guo Z, Lu S, He S, Shu W, Zhou B (2009) Increased abscisic acid levels in transgenic tobacco over-expressing 9 cis-epoxycarotenoid dioxygenase influence H2O2 and NO production and antioxidant defences. Plant Cell Environ. https://doi.org/10.1111/j.1365-3040.2009.01945.x
Zhang Y, Wang L, Liu Y et al (2006) Nitric oxide enhances salt tolerance in maize seedlings through increasing activities of proton-pump and Na+/H+ antiport in the tonoplast. Planta. https://doi.org/10.1007/s00425-006-0242-z
Zhao MG, Chen L, Zhang LL, Zhang WH (2009) Nitric reductase-dependent nitric oxide production is involved in cold acclimation and freezing tolerance in Arabidopsis. Plant Physiol. https://doi.org/10.1104/pp.109.140996
Zhou B, Guo Z, Xing J, Huang B (2005) Nitric oxide is involved in abscisic acid-induced antioxidant activities in Stylosanthes guianensis. J Exp Bot. https://doi.org/10.1093/jxb/eri319
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The authors would like to acknowledge the Brazilian National Council for Scientific and Technological Development (CNPq) and Coordination for the Improvement of Higher Education Personnel (CAPES) for financial support.
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MPS designed and conceived the experiment, performed the molecular analysis, analyzed data and wrote the paper. DBZ performed molecular analysis and reviewed the paper. AFLS Performed the data analysis. EPC performed molecular analysis. CJLO, LEPP, ARF and RBS reviewed the paper. All the authors reviewed and approved the final version of the manuscript.
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Santos, M.P., Zandonadi, D.B., de Sá, A.F.L. et al. Abscisic acid-nitric oxide and auxin interaction modulates salt stress response in tomato roots. Theor. Exp. Plant Physiol. 32, 301–313 (2020). https://doi.org/10.1007/s40626-020-00187-6
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DOI: https://doi.org/10.1007/s40626-020-00187-6