Skip to main content
SpringerLink
Log in

Chlorophyll a fluorescence analysis reveals divergent photosystem II responses to saline, alkaline and saline–alkaline stresses in the two Lotus japonicus model ecotypes MG20 and Gifu-129

  • Original Article
  • Published:
Acta Physiologiae Plantarum Aims and scope Submit manuscript

Abstract

Saline and alkaline stresses affect more than 10% of the World’s arable land, limiting agricultural production. Salt-induced stress may affect the photosystem II (PSII) function, altering fluorescence emission. Therefore, changes in fluorescence are used to quantify and analyze abiotic stress responses in plants. So far, no study has focused on the response of PSII to saline, alkaline and saline–alkaline stresses in the model legume Lotus japonicus. For the saline, alkaline and saline–alkaline treatments, plants of the L. japonicus ecotypes MG20 and Gifu-129 were cultivated in sand with nutrient solution, added with NaCl and NaHCO3 in different proportions. Growth, gas exchange, and chlorophyll a fluorescence transient kinetic and OJIP parameters were measured, and chlorophyll a and b were determined. The analysis of the kinetic of chlorophyll a fluorescence showed that NaCl-derived stress sources affect the photochemical events in PSII in both ecotypes, being this effect more evident under higher pH condition, whereas alkalinity per se has a mild or no effect on these events. The saline–alkaline stress induced a more severe effect on Gifu B-129, compared with Miyakojima MG20, whereas NaCl improved primary photochemistry in MG20. Our results allow us to accept the hypothesis that both ecotypes deploy differential responses under the three stressful treatments and that the saline–alkaline stress causes higher damage levels than saline and alkaline stresses alone in relation with structures and sub-processes of the PSII.

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

Similar content being viewed by others

References

  • Acosta-Motos JR, Diaz-Vivancos P, Alvarez S, Fernández-García N, Sánchez-Blanco MJ, Hernández JA (2015a) NaCl-induced physiological and biochemical adaptative mechanisms in the ornamental Myrtus communis L plants. J Plant Physiol 183:41–51

    Article  CAS  PubMed  Google Scholar 

  • Acosta-Motos JR, Diaz-Vivancos P, Álvarez S, Fernández-García N, Sanchez-Blanco MJ, Hernández JA (2015b) Physiological and biochemical mechanisms of the ornamental Eugenia myrtifolia L plants for coping with NaCl stress and recovery. Planta 242:829–846

    Article  CAS  PubMed  Google Scholar 

  • Appenroth KJ, Stöckel J, Srivastava A, Strasser RJ (2001) Multiple effects of chromate on the photosynthetic apparatus of Spirodela polyrhiza as probed by OJIP chlorophyll a fluorescence measurement. Environ Pollut 115:49–64

    Article  CAS  PubMed  Google Scholar 

  • Ashraf MHPJC, Harris PJC (2013) Photosynthesis under stressful environments: an overview. Photosynthetica 51:163–190

    Article  CAS  Google Scholar 

  • Babuin MF, Campestre MP, Rocco R, Bordenave CD, Escaray FJ, Antonelli C, Calzadilla P (2014) Response to long-term NaHCO3-derived alkalinity in model Lotus japonicus ecotypes Gifu B-129 and miyakojima MG-20: transcriptomic profiling and physiological characterization. PLoS ONE 9:e97106

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bordenave CD, Rocco R, Babuin MF, Campestre MP, Escaray FJ, Gárriz A, Antonelli C (2017) Characterization of the primary metabolome during the long-term response to NaHCO3-derived alkalinity in Lotus japonicus ecotypes Gifu B-129 and Miyakojima MG-20. Acta Physiol Plant 39:76

    Article  CAS  Google Scholar 

  • Calatayud A, Barreno E (2001) Chlorophyll a fluorescence antioxidant enzymes and lipid peroxidation in tomato in response to ozone and benomyl. Environ Pollut 115:283–289

    Article  CAS  PubMed  Google Scholar 

  • Campestre MP, Antonelli C, Calzadilla PI, Maiale SJ, Rodríguez AA, Ruiz OA (2016) The alkaline tolerance in Lotus japonicus is associated with mechanisms of iron acquisition and modification of the architectural pattern of the root. J Plant Physiol 206:40–48

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Chen S, Li J, Wang S, Hüttermann A, Altman A (2001) Salt nutrient uptake and transport and ABA of Populus euphratica a hybrid in response to increasing soil NaCl. Trees 15:186–194

    Article  CAS  Google Scholar 

  • Clark RB (1982) Iron deficiency in plants grown in the Great Plains of the US. J Plant Nut 5:251–268

    Article  CAS  Google Scholar 

  • Clark RB, Yusuf Y, Ross WM, Maranville JW (1982) Screening for sorghum genotypic differences to iron deficiency. J Plant Nut 5:587–604

    Article  CAS  Google Scholar 

  • Demetriou G, Neonaki C, Navakoudis E, Kotzabasis K (2007) Salt stress impact on the molecular structure and function of the photosynthetic apparatus—the protective role of polyamines. BBA-Bioenergetics 1767:272–280

    Article  CAS  PubMed  Google Scholar 

  • Di Renzo JA, Casanoves F, Balzarini MG, González L, Tablada M, Robledo CW (2008) Infostat versión Grupo InfoStat FCA. Universidad Nacional de Córdoba, Argentina

    Google Scholar 

  • Duarte B, Santos D, Marques JC, Caçador I (2013) Ecophysiological adaptations of two halophytes to salt stress: photosynthesis PS II photochemistry and anti-oxidant feedback–implications for resilience in climate change. Plant Physiol Bioch 67:178–188

    Article  CAS  Google Scholar 

  • Gazquez A, Maiale SJ, Rachoski MM, Vidal A, Ruiz OA, Menéndez AB, Rodríguez AA (2015) Physiological response of multiple contrasting rice (Oryza sativa L) cultivars to suboptimal temperatures. J Agron Crop Sci 201:117–127

    Article  CAS  Google Scholar 

  • Gazquez A, Vilas JM, Lerner JEC, Maiale SJ, Calzadilla PI, Menéndez AB, Rodríguez AA (2018) Rice tolerance to suboptimal low temperatures relies on the maintenance of the photosynthetic capacity. Plant Physiol Bioch 127:537–552

    Article  CAS  Google Scholar 

  • Goh CH, Ko SM, Koh S, Kim YJ, Bae HJ (2012) Photosynthesis and environments: photoinhibition and repair mechanisms in plants. J Plant Biol 55:93–101

    Article  CAS  Google Scholar 

  • Goltsev VN, Kalaji HM, Paunov M, Bąba W, Horaczek T, Mojski J, Kociel H (2016) Variable chlorophyll fluorescence and its use for assessing physiological condition of plant photosynthetic apparatus. Russ J Plant Physiol 63:869–893

    Article  CAS  Google Scholar 

  • Gómez-Bellot MJ, Nortes PA, Ortuño MF, Romero C, Fernandez-Garcia N, Sánchez-Blanco MJ (2015) Influence of arbuscular mycorrhizal fungi and treated wastewater on water relations and leaf structure alterations of viburnum tinus L plants during both saline and recovery periods. J Plant Physiol 188:96–105

    Article  PubMed  CAS  Google Scholar 

  • Gong B, Wena D, VandenLangenberg K, Wei M, Yanga F, Shi Q, Wanga X (2013) Comparative effects of NaCl and NaHCO3 stress on photosynthetic parameters, nutrient metabolism, and the antioxidant system in tomato leaves. Sci Hort 157:1–12

    Article  CAS  Google Scholar 

  • Handberg K, Stougaard J (1992) Lotus japonicus an autogamous diploid legume species for classical and molecular genetics. Plant J 2:487–496

    Article  Google Scholar 

  • Haupt-Herting S, Fock HP (2002) Oxygen exchange in relation to carbon assimilation in water-stressed leaves during photosynthesis. Ann Bot-London 89:851–859

    Article  CAS  Google Scholar 

  • Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. In: Circular California agricultural experiment station, vol 347, 2nd edn

  • Hong CY, Chao YY, Yang MY, Cho SC, Kao CH (2009) Na+ but not Cl− or osmotic stress is involved in NaCl-induced expression of glutathione reductase in roots of rice seedlings. J Plant Physiol 166:1598–1606

    Article  CAS  PubMed  Google Scholar 

  • Jafarinia M, Shariati M (2012) Effects of salt stress on photosystem II of canola plant (Barassica napus L) probing by chlorophyll a fluorescence measurements. Iran J Sci Technol 36:71–76

    CAS  Google Scholar 

  • James RA, Rivelli AR, Munns R, von Caemmerer S (2002) Factors affecting CO2 assimilation leaf injury and growth in salt-stressed durum wheat. Funct Plant Biol 29:1393–1403

    Article  CAS  PubMed  Google Scholar 

  • Jia XM, Wang H, Svetla S, Zhu Y-F, Hu Y, Chen L, Zhao T, Wang YX (2019) Comparative physiological responses and adaptive strategies of apple Malus halliana to salt, alkali and saline-alkali stress. Sci Hortic 245:154–162

    Article  CAS  Google Scholar 

  • Jiang HX, Chen LS, Zheng JG, Han S, Tang N, Smith BR (2008) Aluminum-induced effects on photosystem II photochemistry in citrus leaves assessed by the chlorophyll a fluorescence transient. Tree Physiol 28:1863–1871

    Article  CAS  PubMed  Google Scholar 

  • Kalaji HM, Bosa K, Kościelniak J, Żuk-Gołaszewska K (2011) Effects of salt stress on photosystem II efficiency and CO2 assimilation of two syrian barley landraces. Environ Exp Bot 73:64–72

    Article  CAS  Google Scholar 

  • Krüger GH, Tsimilli-Michael M, Strasser RJ (1997) Light stress provokes plastic and elastic modifications in structure and function of photosystem II in camellia leaves. Physiol Plant 101:265–277

    Article  Google Scholar 

  • Kukavica B, Morina F, Janjić N, Boroja M, Jovanović L, Veljović-Jovanović S (2013) Effects of mixed saline and alkaline stress on the morphology and anatomy of Pisum sativum L: the role of peroxidase and ascorbate oxidase in growth regulation. Arch Biol Sci 65:265–278

    Article  Google Scholar 

  • Kumar A, Kumar A, Kumar P, Lata C, Kumar S (2018) Effect of individual and interactive alkalinity and salinity on physiological, biochemical and nutritional traits of marvel grass. Ind J Exp Biol 56:573–581

    CAS  Google Scholar 

  • Kyle DJ, Osmond CB, Arntzen CJ (eds) (1987) Photoinhibition, topics in photosynthesis, vol 9. Elsevier, Amsterdam, pp 289–307

    Google Scholar 

  • Läuchli A, Lüttge U (2002) Salinity: environment-plants-molecules. Kluwer Academic Publishers, Dordrecht, pp 229–248

    Google Scholar 

  • Li R, Shi F, Fukuda K (2010) Interactive effects of various salt and alkali stresses on growth organic solutes and cation accumulation in a halophyte Spartina alterniflora (Poaceae). Environ Exp Bot 68:66–74

    Article  CAS  Google Scholar 

  • Li Z, Cong R, Yang Q, Zhou J (2017) Effects of saline-alkali stress on growth and osmotic adjustment substances in willow seedlings. Acta Ecol Sin 37:8511–8517

    CAS  Google Scholar 

  • Lichtenthaler FW (1987) Karl Freudenberg, Burckhardt Helferich, Hermann OL Fischer A centennial tribute. Carbohyd Res 164:1–22

    Article  CAS  Google Scholar 

  • Marschner H (1995) Mineral nutrition of higher plants, 2nd edn. Academic Press, London

    Google Scholar 

  • Mathur S, Mehta P, Jajoo A (2013) Effects of dual stress (high salt and high temperature) on the photochemical efficiency of wheat leaves (Triticum aestivum). Physiol Mol Biol Plant 19:179–188

    Article  CAS  Google Scholar 

  • Mehta P, Jajoo A, Mathur S, Bharti S (2010a) Chlorophyll a fluorescence study revealing effects of high salt stress on photosystem II in wheat leaves. Plant Physiol Biochem 48:16–20

    Article  CAS  PubMed  Google Scholar 

  • Mehta P, Allakhverdiev SI, Jajoo A (2010b) Characterization of photosystem II heterogeneity in response to high salt stress in wheat leaves (Triticum aestivum). Photosynth Res 105:249–255

    Article  CAS  PubMed  Google Scholar 

  • Melchiorre M, Quero GE, Parola R, Racca R, Trippi VS, Lascano R (2009) Physiological characterization of four model lotus diploid genotypes: L. japonicus (MG20 and Gifu) L. filicaulis and L. burttii under salt stress. Plant Sci 177:618–628

    Article  CAS  Google Scholar 

  • Munns R (2002) Comparative physiology of salt and water stress. Plant Cell Environ 25:239–250

    Article  CAS  PubMed  Google Scholar 

  • Munns R (2005) Genes and salt tolerance: bringing them together. New Phytol 167:645–663

    Article  CAS  PubMed  Google Scholar 

  • Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681

    Article  CAS  PubMed  Google Scholar 

  • Pan X, Zhang D, Chen X, Li L, Mu G, Li L, Song W (2010) Sb uptake and photosynthesis of Zea mays growing in soil watered with Sb mine drainage: an OJIP chlorophyll fluorescence study. Pol J Environ Stud 19:981

    CAS  Google Scholar 

  • Papageorgiou G (1975) Chlorophyll fluorescence: an intrinsic probe of photosynthesis. In: Govindjee (ed) Bioenergetics of photosynthesis. Academic Press, pp 319–371

  • Parida AK, Das AB (2005) Salt tolerance and salinity effects on plants: a review. Ecotoxi Environ Saf 60:324–349

    Article  CAS  Google Scholar 

  • Paz RC, Rocco RA, Reinoso H, Menéndez AB, Pieckenstain FL, Ruiz OA (2012) Comparative study of alkaline saline and mixed saline–alkaline stresses with regard to their effects on growth nutrient accumulation and root morphology of Lotus tenuis. J Plant Growth Regul 31:448–459

    Article  CAS  Google Scholar 

  • Paz RC, Reinoso H, Espasandin FD, González Antivilo FA, Sansberro PA, Rocco RA, Ruiz OA (2014) Akaline saline and mixed saline–alkaline stresses induce physiological and morpho-anatomical changes in Lotus tenuis shoots. Plant Biol 16:1042–1049

    CAS  PubMed  Google Scholar 

  • Pietrini F, Chaudhuri D, Thapliyal AP, Massacci A (2005) Analysis of chlorophyll fluorescence transients in mandarin leaves during a photo-oxidative cold shock and recovery. Agr Ecosyst Environ 106:189–198

    Article  CAS  Google Scholar 

  • Sanchez DH, Lippold F, Redestig H, Hannah MA, Erban A, Krämer U, Kopka J (2008) Integrative functional genomics of salt acclimatization in the model legume Lotus japonicus. Plant J 53:973–987

    Article  CAS  PubMed  Google Scholar 

  • Sanchez DH, Szymanski J, Erban A, Udvardi MK, Kopka J (2010) Mining for robust transcriptional and metabolic responses to long-term salt stress: a case study on the model legume Lotus japonicus. Plant Cell Environ 33:468–480

    Article  CAS  PubMed  Google Scholar 

  • Sanchez DH, Pieckenstain FL, Szymanski J, Erban A, Bromke M, Hannah MA, Kraemer U (2011) Comparative functional genomics of salt stress in related model and cultivated plants identifies and overcomes limitations to translational genomics. PLoS One 6:e17094

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sanchez DH, Schwabe F, Erban A, Udvardi MK, Kopka J (2012) Comparative metabolomics of drought acclimation in model and forage legumes. Plant Cell Environ 35:136–149

    Article  CAS  PubMed  Google Scholar 

  • Sato S, Tabata S (2006) Lotus japonicus as a platform for legume research. Curr Opin Plant Biol 9:128–132

    Article  CAS  PubMed  Google Scholar 

  • Sayed OH (1998) Analysis of photosynthetic responses and adaptation to nitrogen starvation in Chlorella using in vivo chlorophyll fluorescence. Photosynthetica 35:611–619

    Article  Google Scholar 

  • Schreiber UBWN, Bilger W, Neubauer C (1995) Chlorophyll fluorescence as a nonintrusive indicator for rapid assessment of in vivo photosynthesis. Ecophysiology of photosynthesis. Springer, Berlin, Heidelberg, pp 49–70

    Chapter  Google Scholar 

  • Shi D, Sheng Y (2005a) Effect of various salt–alkaline mixed stress conditions on sunflower seedlings and analysis of their stress factors. Environ Exp Bot 54:8–21

    Article  CAS  Google Scholar 

  • Shi D, Wang D (2005b) Effects of various salt-alkaline mixed stresses on Aneurolepidium chinense (Trin) Kitag. Plant Soil 271:15–26

    Article  CAS  Google Scholar 

  • Shi D, Yin L (1993) Difference between salt (NaCl) and alkaline (Na2CO3) stresses on Puccinellia tenuiflora (Griseb.) Scribn et Merr Plants. Acta Bot Sin 3:144–149

    Google Scholar 

  • Strasser RJ, Govindjee (1992) On the O-J-I-P fluorescence transients in leaves and Dl mutants of Chlamydomonas reinhardtii. In: Murata N (ed) Research in photosynthesis, vol II, pp 29–32. Kluwer Academic, Dordrecht

    Google Scholar 

  • Strasser BJ, Strasser RJ (1995) Measuring fast fluorescence transients to address environmental questions: the JIP-Test. In: Mathis P (ed) Photosynthesis: from light to biosphere. KAP Press, Dordrecht, pp 977–980. https://doi.org/10.1007/978-94-009-0173-5_1142

    Chapter  Google Scholar 

  • Strasser RJ, Srivastava A, Govindjee G (1995) Polyphasic chlorophyll a fluorescence transient in plants and cyanobacteria. Photochem Photobiol 61:32–42

    Article  CAS  Google Scholar 

  • Strasser RJ, Srivastava A, Tsimilli-Michael M (1999) Screening the vitality and photosynthetic activity of plants by fluorescence transient. In: Behl RK, Punia MS, Lather BPS (eds) Crop improvement for food security. SSARM, Hisar, pp 72–115

    Google Scholar 

  • Strasser RJ, Srivastava A, Tsimilli-Michael M (2000) The fluorescence transient as a tool to characterise and screen photosynthetic samples. In: Yunus M, Pathre U, Mohanty P (eds) Probing photosynthesis: mechanisms, regulation and adaptation. Taylor and Francis, London, New York, pp 445–483

    Google Scholar 

  • Strasser RJ, Tsimilli-Michael M, Srivastava A (2004) Analysis of the chlorophyll a fluorescence transient. Chlorophyll a fluorescence. Springer, Dordrecht, pp 321–362

    Book  Google Scholar 

  • Strauss AJ, Krüger GHJ, Strasser RJ, Van Heerden PDR (2006) Ranking of dark chilling tolerance in soybean genotypes probed by the chlorophyll a fluorescence transient OJIP. Environ Exp Bot 56:147–157

    Article  CAS  Google Scholar 

  • Tang C, Turner NC (1999) The influence of alkalinity and water stress on the stomatal conductance photosynthetic rate and growth of Lupinus angustifolius L and Lupinus pilosus. Aust J Exp Agr 39:457–464

    Article  Google Scholar 

  • Tester M, Davenport R (2003) Na+ tolerance and Na+ transport in higher plants. Ann Bot-London 91:503–527

    Article  CAS  Google Scholar 

  • Tsai YC, Hong CY, Liu LF, Kao CH (2004) Relative importance of Na+ and Cl– in NaCl− induced antioxidant systems in roots of rice seedlings. Physiol Plant 122:86–94

    Article  CAS  Google Scholar 

  • Tsimilli-Michael M, Strasser RJ (2008) In vivo assessment of plants’ vitality: applications in detecting and evaluating the impact of mycorrhization on host plants. In: Varma A (ed) Mycorrhiza. Springer, Berlin, Heidelberg, pp 679–703

    Chapter  Google Scholar 

  • Vu TS, Zhang D, Xiao W, Chi C, Xing Y (2015) Mechanisms of combined effects of salt and alkaline stresses on seed germination and seedlings of Melilotus officinales (Fabaceae) in Northeast of China. Pak J Bot 47:1603–1611

    Google Scholar 

  • Wang G, Chen L, Hao Z, Li X, Liu Y (2011) Effects of salinity stress on the photosynthesis of Wolffia arrhiza as probed by the OJIP test. Fresenius Environ Bull 20:432–438

    CAS  Google Scholar 

  • Wen X, Qiu N, Lu Q, Lu C (2005) Enhanced thermotolerance of photosystem II in salt-adapted plants of the halophyte Artemisia anethifolia. Planta 220:486–497

    Article  CAS  PubMed  Google Scholar 

  • Xia J, Li Y, Zou D (2004) Effects of salinity stress on PSII in Ulva lactuca as probed by chlorophyll fluorescence measurements. Aquat Bot 80:129–137

    Article  CAS  Google Scholar 

  • Xiang L, Hu L, Xu W, Zhen A, Zhang L, Hu X (2016) Exogenous γ-aminobutyric acid improves the structure and function of photosystem II in muskmelon seedlings exposed to salinity-alkalinity stress. PLoS One 11:e0164847

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yamane K, Kawasaki M, Taniguchi M, Miyake H (2008) Correlation between chloroplast ultrastructure and chlorophyll fluorescence characteristics in the leaves of rice (Oryza sativa L.) grown under salinity. Plant Prod Sci 11:139–145

    Article  CAS  Google Scholar 

  • Yang C, Chong J, Li C, Kim C, Shi D, Wang D (2007) Osmotic adjustment and ion balance traits of an alkali resistant halophyte Kochia sieversiana during adaptation to salt and alkali conditions. Plant Soil 294:263–276

    Article  CAS  Google Scholar 

  • Yang CW, Jianaer A, Li CY, Shi DC, Wang DL (2008) Comparison of the effects of salt-stress and alkali-stress on photosynthesis and energy storage of an alkali-resistant halophyte Chloris virgata. Photosynthetica 46:273–278

    CAS  Google Scholar 

  • Yang CW, Xu HH, Wang LL, Liu J, Shi DC, Wang DL (2009) Comparative effects of salt-stress and alkali-stress on the growth, photosynthesis, solute accumulation, and ion balance of barley plants. Photosynthetica 47:79–86

    Article  CAS  Google Scholar 

  • Yeo A (1998) Molecular biology of salt tolerance in the context of whole-plant physiology. J Exp Bot 49(323):915–929

    CAS  Google Scholar 

  • Zushi K, Matsuzoe N (2017) Using of chlorophyll a fluorescence OJIP transients for sensing salt stress in the leaves and fruits of tomato. Sci Hort 219:216–221

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by Grants from the Agencia Nacional de promoción Científica y Tecnológica/FONCyT PICTs 2034 and 1611, and the Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET, Argentina).

Author information

Author notes

  1. César Daniel Bordenave and Rubén Rocco should be regarded as first authors, both have contributed equally.

Authors and Affiliations

  1. Instituto Tecnológico de Chascomús, Consejo Nacional de Investigaciones Científicas y Técnicas, Universidad Nacional de General San Martín (INTECH-CONICET-UNSAM), Intendente Marino KM 8.2-CC 164, B7130IWA, Chascomús, Buenos Aires, Argentina

    César Daniel Bordenave, Rubén Rocco, Santiago Javier Maiale, Maria Paula Campestre, Oscar Adolfo Ruiz & Andrés Alberto Rodríguez

  2. Departamento de Biodiversidad y Biología Experimental, Facultad de Ciencias Exactas y Naturales, Instituto de Micología y Botánica (INMIBO-CONICET), Universidad de Buenos Aires, Piso 4 Pab II Ciudad Universitaria (1428), Buenos Aires, Argentina

    Ana Bernardina Menéndez

Authors
  1. César Daniel Bordenave
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Rubén Rocco
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Santiago Javier Maiale
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Maria Paula Campestre
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Oscar Adolfo Ruiz
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Andrés Alberto Rodríguez
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Ana Bernardina Menéndez
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ana Bernardina Menéndez.

Additional information

Communicated by U. Feller.

Publisher's Note

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

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 30 kb)

Supplementary material 2 (DOCX 7 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bordenave, C.D., Rocco, R., Maiale, S.J. et al. Chlorophyll a fluorescence analysis reveals divergent photosystem II responses to saline, alkaline and saline–alkaline stresses in the two Lotus japonicus model ecotypes MG20 and Gifu-129. Acta Physiol Plant 41, 167 (2019). https://doi.org/10.1007/s11738-019-2956-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11738-019-2956-0

Keywords

Search

Navigation