Abstract
Phytohormones have essential roles in plant growth responses under salinity. A better understanding of gibberellin (GA) function in woody plant responses under different sodium salts could help to develop new strategies to improve plant tolerance to salinity. In this study, the role of GA in morpho-physiological responses of halophytic woody Prosopis strombulifera plants under salinity was analyzed. Plants were grown in hydroponic solutions and exposed to NaCl, Na2SO4, or their iso-osmotic mixture at − 1.0, − 1.9, and − 2.6 MPa. Control (without salt) and salt-treated plants were sprayed with gibberellin A3 (GA3), or chlormequat chloride (CCC), an inhibitor of its synthesis. Growth responses, anatomical alterations and ABA, active GA forms (GA1, GA3, and GA4) and inactive GA forms (GA8 and GA34) endogenous levels were evaluated. The application of GA3 increased growth in control plants more than in salt-treated plants. Roots and leaves of salt-treated plants showed high levels of ABA and active GA forms after exposure to GA3, and lower endogenous levels of active GA when receiving the inhibitor. CCC triggered stress-alleviating responses in these plants, such as anatomical and hormonal changes that included an increase in spine length and the number of palisade cell layers, and a reduction in levels of ABA and GA4. Na2SO4-treated plants showed reduced growth, high ABA levels and an active GA metabolism to control the levels of active GA. This study indicates that the suppression of GA signaling would contribute to sodium salts tolerance in the native halophytic woody P. strombulifera plants.
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References
Aloni R (2013) Role of hormones in controlling vascular differentiation and the mechanism of lateral root initiation. Planta 238(5):819–830. https://doi.org/10.1007/s00425-013-1927-8
Anschütz U, Becker D, Shabala S (2014) Going beyond nutrition: regulation of potassium homoeostasis as a common denominator of plant adaptive responses to environment. J Plant Physiol 171(9):670–687. https://doi.org/10.1016/j.jplph.2014.01.009
Bagella S, Filigheddu R, Benesperi R, Giordani P, Minuto L, Viciani D, Casazza G (2019) Thorn, spine and prickle patterns in the Italian flora. Plant Biosyst 153(1):118–133. https://doi.org/10.1080/11263504.2018.1474961
Bechtold U, Ferguson JN, Mullineaux PM (2018) To defend or to grow: lessons from Arabidopsis C24. J Exp Bot 69(11):2809–2821. https://doi.org/10.1093/jxb/ery106
Binenbaum J, Weinstain R, Shani E (2018) Gibberellin localization and transport in plants. Trends Plant Sci 23(5):410–421. https://doi.org/10.1016/j.tplants.2018.02.005
Burkart A (1976) A monograph of the genus Prosopis (Leguminosae subfam. Mimosoideae). Catalogue of the recognized species of Prosopis. J Arnold Arbor 57:450–525
Cai R, Dai W, Zhang C, Wang Y, Wu M, Zhao Y, Cheng B (2017) The maize WRKY transcription factor ZmWRKY17 negatively regulates salt stress tolerance in transgenic Arabidopsis plants. Planta 246(6):1215–1231. https://doi.org/10.1007/s00425-017-2766-9
Chen HI, Li PF, Yang CH (2019) NAC-Like Gene GIBBERELLIN SUPPRESSING FACTOR regulates the gibberellin metabolic pathway in response to cold and drought stresses in arabidopsis. Sci Rep. https://doi.org/10.1038/s41598-019-55429-8
Colebrook EH, Thomas SG, Phillips AL, Hedden P (2014) The role of gibberellin signalling in plant responses to abiotic stress. J Exp Bot 217(1):67–75. https://doi.org/10.1242/jeb.089938
D’Ambrogio de Argüeso A (1986) Manual de técnicas en histología vegetal. Hemisferio Sur, Buenos Aires, p 83
Dayan J, Voronin N, Gong F, Sun TP, Hedden P, Fromm H, Aloni R (2012) Leaf-induced gibberellin signaling is essential for internode elongation, cambial activity, and fiber differentiation in tobacco stems. Plant Cell 24(1):66–79. https://doi.org/10.1105/tpc.111.093096
Devinar G, Llanes A, Masciarelli O, Luna V (2013) Different relative humidity conditions combined with chloride and sulfate salinity treatments modify abscisic acid and salicylic acid levels in the halophyte Prosopis strombulifera. Plant Growth Regul 70(3):247–256. https://doi.org/10.1007/s10725-013-9796-5
FAO (2017) FAO soils portal, salt-affected soils. http://www.fao.org/soils-portal/soil-management/management-of-some-problem-soils/salt-affected-soils/more-information-on-salt-affected-soils/en/ (Accessed February, 2020).
Finkelstein R (2013) Abscisic acid synthesis and response. In: The Arabidopsis book/American society of plant biologists
Flowers TJ, Colmer TD (2015) Plant salt tolerance: adaptations in halophytes. Ann Bot 115(3):327–331. https://doi.org/10.1093/aob/mcu267
Fukuda A, Nakamura A, Hara N, Toki S, Tanaka Y (2011) Molecular and functional analyses of rice NHX-type Na+/H+ antiporter genes. Planta 233(1):175–188. https://doi.org/10.1007/s00425-010-1289-4
Golldack D, Li C, Mohan H, Probst N (2013) Gibberellins and abscisic acid signal crosstalk: living and developing under unfavorable conditions. Plant Cell Rep 32(7):1007–1016. https://doi.org/10.1007/s00299-013-1409-2
Han LP, Wang X, Guo X, Rao MS, Steinberger Y, Cheng X, Xie GH (2011) Effects of plant growth regulators on growth, yield and lodging of sweet sorghum. Res Crops 12(2):372–382
He H, Liang G, Lu S, Wang P, Liu T, Ma Z, Mao J (2019) Genome-wide identification and expression analysis of GA2ox, GA3ox, and GA20ox are related to gibberellin oxidase genes in grape (Vitis vinifera L). Genes 10(9):680. https://doi.org/10.3390/genes10090680
Hedden P, Phillips AL (2000) Gibberellin metabolism: new insights revealed by the genes. Trends Plant Sci 5:523–530
Hedden P, Thomas SG (2016) Annual plant reviews, the gibberellins. Wiley. https://doi.org/10.1016/S1360-1385(00)01790-8
Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. In: Circular, 2nd edn. California Agricultural Experiment Station, p 347
Huang M, Fang Y, Liu Y, Jin Y, Sun J, Tao X, Zhao H (2015) Using proteomic analysis to investigate uniconazole-induced phytohormone variation and starch accumulation in duckweed (Landoltia punctata). BMC 15(1):81. https://doi.org/10.1186/s12896-015-0198-9
Johansen DA (1940) Plant microtechnique. McGraw-Hill Book Company Inc, London
Kim SK, Kim HY (2014) Effects of gibberellin biosynthetic inhibitors on oil, secoisolaresonolodiglucoside, seed yield and endogenous gibberellin content in flax. Korean J Plant Res 27(3):229–235
Leone M, Keller MM, Cerrudo I, Ballaré CL (2014) To grow or defend? Low red:far-red ratios reduce jasmonate sensitivity in arabidopsis seedlings by promoting DELLA degradation and increasing JAZ10 stability. New Phytol 204:355–367. https://doi.org/10.1111/nph.12971
Liu X, Hu P, Huang M, Tang Y, Li Y, Li L (2016) The NF-YC–RGL2 module integrates GA and ABA signaling to regulate seed germination in Arabidopsis. Nat Commun 7:12768. https://doi.org/10.1038/ncomms12768
Liu J, Shabala S, Shabala L, Zhou M, Meinke H, Venkataraman G, Zhao Q (2019) Tissue-specific regulation of Na+ and K+ transporters explains genotypic differences in salinity stress tolerance in rice. Front Plant Sci 10:1361. https://doi.org/10.3389/fpls.2019.01361
Llanes A, Bertazza G, Palacio G, Luna V (2013) Different sodium salts cause different solute accumulation in the halophyte Prosopis strombulifera. Plant Biol 15:118–125. https://doi.org/10.1111/j.1438-8677.2012.00626.x
Llanes A, Masciarelli O, Ordoñez R, Isla MI, Luna V (2014) Differential growth responses to sodium salts involve different abscisic acid metabolism and transport in Prosopis strombulifera. Biol Plant 58(1):80–88. https://doi.org/10.1007/s10535-013-0365-6
Llanes A, Arbona V, Gómez-Cadenas A, Luna V (2016) Metabolomic profiling of the halophyte Prosopis strombulifera shows sodium salt-specific response. Plant Physiol Biochem 108:145–157. https://doi.org/10.1016/j.plaphy.2016.07.010
Magome H, Yamaguchi S, Hanada A, Kamiya Y, Oda K (2008) The DDF1 transcriptional activator upregulates expression of a gibberellin-deactivating gene, GA2ox7, under high-salinity stress in Arabidopsis. Plant J 56(4):613–626. https://doi.org/10.1111/j.1365-313X.2008.03627.x
Magome H, Kamiya Y (2016) Inactivation processes. Ann Plant Rev 49:73–93
Mauseth JD (1988) Plant Anatomy. Benjamin Cummnings Pub. Co., Inc., California, pp 1–560
Medina EF, Mayrink GC, Dias CR, Vital CE, Ribeiro DM, Silva IR, Merchant A (2019) Physiological and biochemical responses of Eucalyptus seedlings to hypoxia. Ann for Sci 76(1):4
Moreno-Izaguirre E, Ojeda-Barrios D, Avila-Quezada G, Guerrero-Prieto V, Parra-Quezada R, Ruíz-Anchondo T (2016) Sodium sulfate exposure slows growth of native pecan seedlings. Phyton 84(1):80–85
Nandy P, Das S, Ghose M (2005) Relation of leaf micro-morphology with photosynthesis and water efflux in some Indian mangroves. Acta Bot Croat 64(2):331–340
Naz N, Fatima S, Hameed M, Naseer M, Batool R, Ashraf M, Ahmad KS (2016) Adaptations for salinity tolerance in Sporobolus ioclados (Nees ex Trin.) Nees from saline desert. Flora 223:46–55. https://doi.org/10.1016/j.flora.2016.04.013
Nobel PS (2003) Environmental biology of agaves and cacti. Cambridge University Press, Cambridge
Osakabe Y, Yamaguchi-Shinozaki K, Shinozaki K, Tran LSP (2014) ABA control of plant macroelement membrane transport systems in response to water deficit and high salinity. New Phytol 202(1):35–49. https://doi.org/10.1111/nph.12613
Qadir M, Quillérou E, Nangia V, Murtaza G, Singh M, Thomas RJ, Noble AD (2014) Economics of salt-induced land degradation and restoration. Nat Resour Forum 38(4):282–295. https://doi.org/10.1111/1477-8947.12054
Rademacher W (2016) Chemical regulators of gibberellin status and their application in plant production. Ann Plant Rev 49:359–403. https://doi.org/10.1002/9781119312994.apr0541
Reginato M, Sosa L, Llanes A, Hampp E, Vettorazzi N, Reinoso H, Luna V (2014) Na2SO4 and NaCl determine different growth responses and ion accumulation in the halophytic legume Prosopis strombulifera. Plant Biol 16:97–106
Reich M, Aghajanzadeh T, Helm J, Parmar S, Hawkesford MJ, De Kok LJ (2017) Chloride and sulfate salinity differently affect biomass, mineral nutrient composition and expression of sulfate transport and assimilation genes in Brassica rapa. Plant Soil 411(1–2):319–332. https://doi.org/10.1007/s11104-016-3026-7
Reinoso H, Sosa L, Ramirez L, Luna V (2004) Salt-induced changes in the vegetative anatomy of Prosopis strombulifera (Leguminosae). Can J Bot 82:618–628. https://doi.org/10.1139/b04-040
Reinoso H, Sosa L, Reginato M, Luna V (2005) Histological alterations induced by sodium sulfate in the vegetative anatomy of Prosopis strombulifera (Lam.) Benth. World J Agr Sci 2:109–119
Di Rienzo, J., Casanoves, F., Balzarini, M., Gonzalez, L., Tablada, M., Robledo, C., 2016. InfoStat. Grupo InfoStat, FCA. Universidad Nacional de Córdoba, Argentina. http://www.infostat.com.ar/. (Accessed February, 2020).
Rieu I, Eriksson S, Powers SJ, Gong F, Griffiths J, Woolley L, Phillips AL (2008) Genetic analysis reveals that C19-GA 2-oxidation is a major gibberellin inactivation pathway in Arabidopsis. Plant Cell 20(9):2420–2436. https://doi.org/10.1105/tpc.108.058818
Sah SK, Reddy KR, Li J (2016) Abscisic acid and abiotic stress tolerance in crop plants. Front Plant Sci 7:571. https://doi.org/10.1105/tpc.108.058818
Sakamoto T, Miura K, Itoh H, Tatsumi T, Ueguchi-Tanaka M, Ishiyama K, Kobayashi M, Agrawal GK, Takeda S, Abe K, Miyao A, Hirochika H, Kitano H, Ashikari M, Matsuoka M (2004) An overview of gibberellin metabolism enzyme genes and their related mutants in rice. Plant Physiol 134:1642–1653. https://doi.org/10.1104/pp.103.033696
Sancho-Knapik D, Sanz MÁ, Peguero-Pina JJ, Niinemets Ü, Gil-Pelegrín E (2017) Changes of secondary metabolites in Pinus sylvestris L. needles under increasing soil water deficit. Ann for Sci 74(1):24
Shi T, Rahmani RS, Gugger PF, Wang M, Li H, Zhang Y, Li Z, Wang Q, Van de Peer Y, Marchal K, Chen J (2020) Distinct expression and methylation patterns for genes with different fates following a single whole-genome duplication in flowering plants. Mol Biol Evol 37(8):2394–2413. https://doi.org/10.1093/molbev/msaa105
Shu K, Zhou W, Chen F, Luo X, Yang W (2018) Abscisic acid and gibberellins antagonistically mediate plant development and abiotic stress responses. Front Plant Sci 9:416. https://doi.org/10.3389/fpls.2018.00416
Shufang LS, Yu D, Sun Q, Jiang J (2018) Activation of gibberellin 20-oxidase 2 undermines auxin-dependent root and root hair growth in NaCl-stressed Arabidopsis seedlings. Plant Growth Regul 84(2):225–236. https://doi.org/10.1007/s10725-017-0333-9
Singh D, Singh CK, Kumari S, Tomar RSS, Karwa S, Singh R, Pal M (2017) Discerning morpho-anatomical, physiological and molecular multiformity in cultivated and wild genotypes of lentil with reconciliation to salinity stress. PLoS ONE 12(12):e0190462. https://doi.org/10.1371/journal.pone.0177465
Sosa L, Llanes A, Reinoso H, Reginato M, Luna V (2005) Osmotic and specific ion effects on the germination of Prosopis strombulifera. Ann Bot 96:261–267. https://doi.org/10.1093/aob/mci173
Taiz L, Zeiger E, Møller IM, Murphy A (2015) Plant physiology and development, 6th edn. Sinauer Associates Incorporated, pp 6–761
Taleisnik E, Rodríguez A, Bustos D, Luna D (2021) Plant Tolerance Mechanisms to Soil Salinity Contribute to the Expansion of Agriculture and Livestock Production in Argentina. In: Taleisnik E, Lavado R (eds) Saline and alkaline soils in latin America. Springer, Cham, pp 381–397
Tanveer M, Shabala S (2018) Targeting redox regulatory mechanisms for salinity stress tolerance in crops. In: Kumar V, Wani SH, Suprasanna P, Tran L-SP (eds) Salinity Responses and Tolerance in Plants, vol 1. Springer, Cham
Travaglia C, Balboa G, Espósito G, Reinoso H (2012) ABA action on the production and redistribution of field-grown maize carbohydrates in semiarid regions. Plant Growth Regul 67(1):27–34. https://doi.org/10.1007/s10725-012-9657-7
Ullah A, Sun H, Hakim Y, Zhang X (2018) A novel cotton WRKY gene, GhWRKY6-like, improves salt tolerance by activating the ABA signaling pathway and scavenging of reactive oxygen species. Physiol Plant 162(4):439–454. https://doi.org/10.1111/ppl.12651
Umezawa T, Nakashima K, Miyakawa T, Kuromori T, Tanokura M, Shinozaki K, Yamaguchi-Shinozaki K (2010) Molecular basis of the core regulatory network in ABA responses: sensing, signaling and transport. Plant Cell Physiol 51(11):1821–1839. https://doi.org/10.1093/pcp/pcq156
Vishwakarma K, Upadhyay N, Kumar N, Yadav G, Singh J, Mishra RK, Sharma S (2017) Abscisic acid signaling and abiotic stress tolerance in plants: a review on current knowledge and future prospects. Front Plant Sci 8:161. https://doi.org/10.3389/fpls.2017.00161
Wang Y, Zhao J, Lu W, Deng D (2017) Gibberellin in plant height control: old player, new story. Plant Cell Rep 36(3):391–398. https://doi.org/10.1007/s00299-017-2104-5
Yamaguchi S (2008) Gibberellin metabolism and its regulation. Ann Rev Plant Biol 59:225–251
Zhang ZL, Ogawa M, Fleet CM, Zentella R, Hu J, Heo JO, Sun TP (2011) Scarecrow-like 3 promotes gibberellin signaling by antagonizing master growth repressor DELLA in Arabidopsis. PNAS 108(5):2160–2165. https://doi.org/10.1073/pnas.1012232108
Zhang S, Yang R, Huo Y, Liu S, Yang G, Huang J, Wu C (2018) Expression of cotton PLATZ1 in transgenic Arabidopsis reduces sensitivity to osmotic and salt stress for germination and seedling establishment associated with modification of the abscisic acid, gibberellin, and ethylene signalling pathways. BMC Plant Biol 18(1):1–11. https://doi.org/10.1186/s12870-018-1416-0
Zhu Y, Nomura T, Xu Y, Zhang Y, Peng Y, Mao B, Zhu X (2006) ELONGATED UPPERMOST INTERNODE encodes a cytochrome P450 monooxygenase that epoxidizes gibberellins in a novel deactivation reaction in rice. Plant Cell 18(2):442–456. https://doi.org/10.1105/tpc.105.038455
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This work was partially supported by Secretaría de Ciencia y Técnica UNRC (SCyT-UNRC), Fondo para la Investigación Científica y Tecnológica (FONCyT) (PICT 2018–3148) and Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Argentina.
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All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by Analía Llanes and Santiago Biava; Claudia Travaglia contributed to the anatomical assays and data analysis. Oscar Masciarelli contributed to the hormonal data collection and analysis. The first draft of the manuscript was written by Analía Llanes and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
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344_2022_10725_MOESM1_ESM.pptx
Supplementary file1 (PPTX 9981 kb) Fig. 1 Transverse sections showing the anatomical features of a leaf of Prosopis strombulifera sprayed with distilled water (DW) (A, D, G, and J), gibberellins (GA3) (B, E, H, and K), or a gibberellin-synthesis inhibitor (CCC) (C, F, I, and L) at the lowest osmotic potential evaluated (Ψo: -2.6 MPa). A, B and C correspond to control (non-salt-treated) plants; D, E, and F to NaCl-treated plants, G, H, and I to Na2SO4-treated plants and J, K, and L to iso-osmotic mixture of both (NaCl + Na2SO4)-treated plants. Scale bar: 100 µm.
344_2022_10725_MOESM2_ESM.pptx
Supplementary file2 (PPTX 18911 kb) Fig. 2 Transverse sections showing the central vascular bundle features of a leaf of Prosopis strombulifera sprayed with distilled water (DW) (A, D, G, and J), gibberellins (GA3) (B, E, H, and K), or a gibberellin-synthesis inhibitor (CCC) (C, F, I, and L) at the lowest osmotic potential evaluated (Ψo: -2.6 MPa). A, B, and C correspond to control (non-salt-treated) plants; D, E, and F to NaCl-treated plants, G, H, and I to Na2SO4-treated plants and J, K, and L to iso-osmotic mixture of both (NaCl + Na2SO4)-treated plants. Scale bar: 40 µm.
344_2022_10725_MOESM3_ESM.docx
Supplementary file3 (DOCX 13 kb) Table 1 Salt treatments obtained by sequential addition of pulses of NaCl (50 mM), Na2SO4 (37.9 mM), or the iso-osmotic mixture of both. The applications were performed every 48 h until reaching the final osmotic potentials evaluated: -1.0, -1.9, or -2.6 MPa. Plants maintained in Hoagland solutions were considered as controls.
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Llanes, A., Biava, S., Travaglia, C. et al. Do Gibberellins Mediate Growth Responses of the Halophytic Woody Prosopis Strombulifera (Lam.) Benth Plants Exposed to Different Sodium Salts?. J Plant Growth Regul 42, 2545–2557 (2023). https://doi.org/10.1007/s00344-022-10725-y
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DOI: https://doi.org/10.1007/s00344-022-10725-y