Investigation of salinity tolerance to different cultivars of highbush blueberry (Vaccinium corymbosum L.) grown in vitro
DOI:
https://doi.org/10.15835/nbha52113691Keywords:
electron paramagnetic resonance spectroscopy, morphological parameters, Mn (II), salt stress, stress tolerance index, water contentAbstract
Salinity is one of the most critical abiotic stresses affecting various physiological, biochemical, and molecular functions of plants. This study aimed to assess the effects of different salt concentrations on in vitro blueberry shoots (‘Bluecrop’, ‘Blueray’, ‘Brigitta Blue’, ‘Duke’, ‘Goldtraube’, ‘Hortblue Petite’, and ‘Patriot’ cultivars) and to understand the mechanisms employed by this species under saline conditions. The Woody Plant Medium (WPM) proliferation medium was supplemented with 10, 50, 100, and 150 mM NaCl to induce salt stress. After ten weeks of in vitro culture under salinity stress, various parameters were evaluated, including the number of shoots obtained/explant, shoot length, fresh weight, dry weight, water content, stress tolerance index (STI), and McKinney index (MKI). Additionally, the behaviour of blueberry cultivars under salt stress was analyzed using electron paramagnetic resonance spectroscopy (EPR). Compared to the control (culture medium without NaCl), all treatments with NaCl reduced shoot length and the number of shoots obtained/explant in all studied blueberry cultivars. ‘Brigitta Blue’ reported the shortest shoots (0.04 ± 0.02 cm) at a concentration of 150 mM NaCl, followed by ‘Blueray’ with 0.05 ± 0.03 cm. Also, the lowest number of shoots/explant was recorded for both cultivars under 150 mM NaCl, namely 0.12 ± 0.07 shoots/explant (‘Brigitta Blue’) and 0.11 ± 0.04 shoots/explant (‘Blueray’). Salt tolerance, as expressed by ITS and MKI, confirmed that ‘Goldtraube’ exhibited higher salt tolerance, with the highest ITS values and the lowest MKI values. Further validation presented ‘Goldtraube’ as the most unresolved spectra of the Mn (II) hyperfine structure under all salt concentrations, therefore ‘Goldtraube’ was the most tolerant to saline stress.
References
Aasim M, Akin F, Ali SA, Taskin MB, Colak MS, Khawar KM (2023). Artificial neural network modeling for deciphering the in vitro induced salt stress tolerance in chickpea (Cicer arietinum L). Physiology and Molecular Biology of Plants 29(2):289. https://doi.org/10.1007/S12298-023-01282-Z
Ami K, Planchais S, Cabassa C, Guivarch A, Véry AA, Khelifi M, Djebbar R, Abrous-Belbachir O, Carol P (2020). Different proline responses of two Algerian durum wheat cultivars to in vitro salt stress. Acta Physiologiae Plantarum 42(2):21 https://doi.org/10.1007/s11738-019-3004-9ï
Amini F, Ehsanpour AA, Hoang, Q T, Shin J S (2007). Protein pattern changes in tomato under in vitro salt stress. Russian Journal of Plant Physiology 54(4):464-471. https://doi.org/10.1134/S102144370704005X
Balasubramaniam T, Shen G, Esmaeili N, Zhang H (2023). Plants’ response mechanisms to salinity stress. Plants 12(12):2253. https://doi.org/10.3390/plants1212225
Bashir MA, Silvestri C, Coppa E, Brunori E, Cristofori V, Rugini E, … Astolfi S (2021). Response of olive shoots to salinity stress suggests the involvement of sulfur metabolism. Plants 10(2):350. https://doi.org/10.3390/PLANTS10020350
Beinert H, Palmer G (1965). Contributions of EPR spectroscopy to our knowledge of oxidative enzymes. Advances in Enzymology and Related Areas of Molecular Biology 27:105-198. https://doi.org/10.1002/9780470122723.CH3
Bimurzayev N, Sari H, Kurunc A, Doganay KH, Asmamaw M (2021). Effects of different salt sources and salinity levels on emergence and seedling growth of faba bean genotypes. Scientific Reports 11(1):1-17. https://doi.org/10.1038/s41598-021-97810-6
Brudvig GW, Beck WF, Paula JC (2003). Mechanism of photosynthetic water oxidation. Annual Review of Biophysics and Biophysical Chemistry 18(1):25-46. https://doi.org/10.1146/ANNUREV.BB.18.060189.000325
Bryla DR, Scagel CF, Lukas SB, Sullivan DM (2021). Ion-specific limitations of sodium chloride and calcium chloride on growth, nutrient uptake, and mycorrhizal colonization in northern and southern highbush blueberry. Journal of the American Society for Horticultural Science 146(6):399-410. https://doi.org/10.21273/JASHS05084-21
Carpıcı EB, Celık N, Bayram G (2009). Effects of salt stress on germination of some maize (Zea mays L.) cultivars. African Journal of Biotechnology 8(19):4918-4922. https://www.ajol.info/index.php/ajb/article/view/65187
Chambers FM, Cloutman E, Daniell JRG, Mauquoy D, Jones PS (2013). Long-term ecological study (palaeoecology) to chronicle habitat degradation and inform conservation ecology: An exemplar from the Brecon Beacons, South Wales. Biodiversity and Conservation 22(3):719-736. https://doi.org/10.1007/S10531-013-0441-4/METRICS
Chourasia KN, More SJ, Kumar A, Kumar D, Singh B, Bhardwaj V, Kumar, … Lal MK (2022). Salinity responses and tolerance mechanisms in underground vegetable crops: an integrative review. Planta 255(3):68. https://doi.org/10.1007/s00425-022-03845-y
Chunthaburee S, Dongsansuk A, Sanitchon J, Pattanagul W, Theerakulpisut P (2016). Physiological and biochemical parameters for evaluation and clustering of rice cultivars differing in salt tolerance at seedling stage. Saudi Journal of Biological Sciences 23(4):467-477. https://doi.org/10.1016/J.SJBS.2015.05.013
Clapa D, Bunea C, Borsai O, Pintea A, Hârţa M, Ştefan R, Fira A (2018). The role of sequestrene 138 in highbush blueberry (Vaccinium corymbosum L.) micropropagation. HortScience 53(10):1487-1493. https://doi.org/10.21273/HORTSCI13269-18
Csillag I, Damian G (2016) EPR Study of organically-grown versus greenhouse strawberries. Studia Universitatis Babeș-Bolyai Physica 21-26.
Debus RJ (1992). The manganese and calcium ions of photosynthetic oxygen evolution. Biochimica et Biophysica Acta (BBA) - Bioenergetics 1102(3):269-352. https://doi.org/10.1016/0005-2728(92)90133-M
Denaxa NK, Nomikou A, Malamos N, Liveri E, Roussos PA, Papasotiropoulos V (2022). Salinity effect on plant growth parameters and fruit bioactive compounds of two strawberry cultivars, coupled with environmental conditions monitoring. Agronomy 12(10):2279. https://doi.org/10.3390/AGRONOMY12102279
Dogan M (2020). Effect of salt stress on in vitro organogenesis from nodal explant of Limnophila aromatica (Lamk.) Merr. and Bacopa monnieri (L.) Wettst. and their physio-morphological and biochemical responses. Physiology and Molecular Biology of Plants 26(4): 803-816. https://doi.org/10.1007/S12298-020-00798-Y/METRICS
El-Mahdy MT, Youssef M, Elazab DS (2022). In vitro screening for salinity tolerance in pomegranate (Punica granatum L.) by morphological and molecular characterization. Acta Physiologiae Plantarum 44(2):1-11. https://doi.org/10.1007/S11738-022-03361-2/METRICS
El-Zaiat RA, El-Sayed I, Taha, LS, Abrahim EA (2020). Enzyme activity of micropropagated Antigonon leptopus plant under effect of salinity stress. Plant Archives 20:3599-3605.
Erturk U, Sivritepe N, Yerlikaya C, Bor M, Ozdemir F, Turkan I (2007). Responses of the cherry rootstock to salinity in vitro. Biologia Plantarum 51(3):597-600. https://doi.org/10.1007/S10535-007-0132-7/METRICS
Filek M, Łabanowska M, Kurdziel M, Wesełucha-Birczyńska A, Bednarska-Kozakiewicz E (2016). Structural and biochemical response of chloroplasts in tolerant and sensitive barley genotypes to drought stress. Journal of Plant Physiology 207:61-72. https://doi.org/10.1016/J.JPLPH.2016.09.012
Fortini EA, Batista DS, Felipe SHS, Silva TD, Correia LNF, Farias LM, … Otoni WC (2023). Physiological, epigenetic, and proteomic responses in Pfaffia glomerata growth in vitro under salt stress and 5-azacytidine. Protoplasma 260(2):467-482. https://doi.org/10.1007/S00709-022-01789-4
Gallegos-Cedillo VM, Alvaro JE, Capatos TH, Hachmann TL, Carrasco G, Urrestarazu M (2018). Effect of pH and silicon in the fertigation solution on vegetative growth of blueberry plants in organic agriculture. HortScience 53(10):1423-1428. https://doi.org/10.21273/HORTSCI13342-18
Granata I, Regni L, Micheli M, Silvestri C, Germanà MA (2023). Application of encapsulation technology: in vitro screening of two Ficus carica L. genotypes under different NaCl concentrations. Horticulturae 9(12):1344. https://doi.org/10.3390/HORTICULTURAE9121344
Grigoriado K, Maloupa E (2008). Micropropagation and salt tolerance of in vitro grown Crithmum maritimum L. Plant Cell, Tissue and Organ Culture 94(2):209-217. https://doi.org/10.1007/S11240-008-9406-9
Hannachi S, Werbrouck S, Bahrini I, Abdelgadir A, Siddiqui HA (2021). Agronomical, physiological and biochemical characterization of in vitro selected eggplant somaclonal variants under NaCl stress. Plants 10(11):2544. https://doi.org/10.3390/PLANTS10112544
Hao S, Wang Y, Yan Y, Liu Y, Wang J, Chen S (2021). A review on plant responses to salt stress and their mechanisms of salt resistance. Horticulturae 7(6):132. https://doi.org/10.3390/horticulturae7060132
Imler CS, Arzola CI, Nunez GH (2019). Ammonium uptake is the main driver of rhizosphere pH in southern highbush blueberry. HortScience 54(5):955-959. https://doi.org/10.21273/HORTSCI13764-18
Isayenkov SV (2012). Physiological and molecular aspects of salt stress in plants. Cytology and Genetics 46(5):302-318. https://doi.org/10.3103/S0095452712050040
Isayenkov SV, Maathuis FJM (2019). Plant salinity stress: Many unanswered questions remain. Frontiers in Plant Science 10:435515. http://dx.doi.org/10.3389/fpls.2019.00080
İzgü T, Kahraman R, Düzgören B, Şen EY, Yalçın Y (2023). Salinity stress in in vitro culture. In: Proceedings of the 9th International Agriculture Congress, Anatolia Academy of Sciences 243.
Javed R, Gürel E (2019). Salt stress by NaCl alters the physiology and biochemistry of tissue culture-grown Stevia rebaudiana Bertoni. Turkish Journal of Agriculture and Forestry 43(1):11-20. https://doi.org/10.3906/tar-1711-71
Khenifi ML, Boudjeniba M, Kameli A (2011). Effects of salt stress on micropropagation of potato (Solanum tuberosum L.). African Journal of Biotechnology 10(40):7840-7845. https://doi.org/10.5897/AJB10.982
Kozos K, Ochmian I (2016). The influence of fertilisation urea phosphate on growth and yielding bush of two highbush blueberry cultivars (V. corymbosum). Folia Pomer. Univ. Technol. Stetin., Agric., Aliment., Pisc., Zootech 325(37):29-38. https://doi.org/10.21005/AAPZ2016.37.1.04
Kumar S, Li G, Yang J, Huang X, Ji Q, Liu Z, Ke W, Hou H (2021). Effect of salt stress on growth, physiological parameters, and ionic concentration of water dropwort (Oenanthe javanica) cultivars. Frontiers in Plant Science 12:660409. https://doi.org/10.3389/FPLS.2021.660409/BIBTEX
Kumari R, Kumar P, Sharma VK, Kumar H (2016). In vitro seed germination and seedling growth for salt tolerance in rice cultivars. Journal of Cell and Tissue Research 16(3):5901-5910.
Labanowska M, Filek M, Kurdziel M, Bidzińska E, Miszalski Z, Hartikainen H (2013). EPR spectroscopy as a tool for investigation of differences in radical status in wheat plants of various tolerances to osmotic stress induced by NaCl and PEG-treatment. Journal of Plant Physiology 170(2):136-145. https://doi.org/10.1016/J.JPLPH.2012.09.013
Lloyd G, McCown B (1980). Commercially-feasible micropropagation of mountain laurel, Kalmia latifolia, by use of shoot-tip culture. Combined Proceedings, International Plant Propagators' Society 30:421-427.
Machado RM, Bryla DR, Vargas O (2012). Effects of salinity induced by ammonium sulfate fertilizer on root and shoot growth of highbush blueberry. Acta Horticulturae 1017:407-414. https://doi.org/10.17660/ActaHortic.2014.1017.49
Matsumoto K, Kobayashi T (2020). Relative tolerance of Japanese apple (Malus spp.) rootstock strains to NaCl stress. Acta Horticulturae 1289:9-17. https://doi.org/10.17660/actahortic.2020.1289.2
Messiga AJ, Haak D, Dorais M (2018). Blueberry yield and soil properties response to long-term fertigation and broadcast nitrogen. Scientia Horticulturae 230:92-101. https://doi.org/10.1016/j.scienta.2017.11.019
Molnár I, Cozma L, Dénes TÉ, Vass I, Vass IZ, Rakosy-Tican E (2021). Drought and saline stress tolerance induced in somatic hybrids of Solanum chacoense and potato cultivars by using mismatch repair deficiency. Agriculture 11(8):696. https://doi.org/10.3390/AGRICULTURE11080696/S1
Morsy MA, Khaled MM (2002) Novel EPR characterization of the antioxidant activity of tea leaves. Spectrochimica Acta Part A: Molecular and Biomolecular Spectroscopy 58(6):1271-1277. https://doi.org/10.1016/S1386-1425(01)00716-8
Muchate NS, Rajurkar NS, Suprasanna P, Nikam TD (2019). NaCl induced salt adaptive changes and enhanced accumulation of 20-hydroxyecdysone in the in vitro shoot cultures of Spinacia oleracea (L.). Scientific Reports 9(1):12522. https://doi.org/10.1038/S41598-019-48737-6
Muralitharan M, Chandler S, Van SR (1992). Effects of NaCl and Na2SO4 on growth and solute composition of highbush blueberry (Vaccinium corymbosum). Functional Plant Biology 19(2):155. https://doi.org/10.1071/PP9920155
Ochmian I, Kozos K, Jaroszewska A, Malinowski R (2021). Chemical and enzymatic changes of different soils during their acidification to adapt them to the cultivation of highbush blueberry. Agronomy 11(1):44. https://doi.org/10.3390/agronomy11010044
Ochmian I, Malinowski R, Kubus M, Malinowska K, Sotek Z, Racek M (2019). The feasibility of growing highbush blueberry (V. corymbosum L.) on loamy calcic soil with the use of organic substrates. Scientia Horticulturae 257:108690. https://doi.org/10.1016/j.scienta.2019.108690
Ortega-Albero N, González-Orenga S, Vicente O, Rodríguez-Burruezo A, Fita A (2023). Responses to salt stress of the interspecific hybrid Solanum insanum × Solanum melongena and its parental species. Plants 12(2):295. https://doi.org/10.3390/PLANTS12020295
Ortiz-Delvasto N, Garcia-Ibañez P, Olmos-Ruiz R, Bárzana G, Carvajal M (2023). Substrate composition affects growth and physiological parameters of blueberry. Scientia Horticulturae 308:111528. https://doi.org/10.1016/j.scienta.2022.111528
Papadakis IE, Veneti G, Chatzissavvidis C, Therios I (2018). Physiological and growth responses of sour cherry (Prunus cerasus L.) plants subjected to short-term salinity stress. Acta Botanica Croatica 77(2):197-202. https://doi.org/10.2478/botcro-2018-0012
Parihar P, Singh S, Singh R, Singh VP, Prasad SM (2015). Effect of salinity stress on plants and its tolerance strategies: a review. Environmental Science and Pollution Research 22(6):4056-4075. https://doi.org/10.1007/s11356-014-3739-1
Passamani LZ, Barbosa RR, Reis RS, Heringer AS, Rangel PL, Santa-Catarina C, … Silveira V (2017). Salt stress induces changes in the proteomic profile of micropropagated sugarcane shoots. PLoS One 12(4):e0176076. https://doi.org/10.1371/JOURNAL.PONE.0176076
Pérez-Tornero O, Tallón CI, Porras I, Navarro JM (2009). Physiological and growth changes in micropropagated Citrus macrophylla explants due to salinity. Journal of Plant Physiology 166(17):1923-1933. https://doi.org/10.1016/J.JPLPH.2009.06.009
Polivanova OB, Bedarev VA (2022). Hyperhydricity in plant tissue culture. Plants 11(23):3313. https://doi.org/10.3390/plants11233313
Radi H, Bouchiha F, El Maataoui S, Oubassou EZ, Rham I, Alfeddy MN, Aissam S, Mazri MA (2023). Morphological and physio-biochemical responses of cactus pear (Opuntia ficus indica (L.) Mill.) organogenic cultures to salt and drought stresses induced in vitro. Plant Cell, Tissue and Organ Culture 154(2):337-350. https://doi.org/10.1007/S11240-023-02454-1/METRICS
Reed G, Cohn M (1970). Electron paramagnetic resonance spectra of manganese(II)-protein complexes: manganese(Ii)-concanavalin A. Journal of Biological Chemistry 245(3):662-664. https://doi.org/10.1016/S0021-9258(18)63380-0
Reed GH, William J, Ray Jr (2002). Electron paramagnetic resonance studies of manganese (II) coordination in the phosphoglucomutase system. Biochemistry 10(17):3190-3197. https://doi.org/10.1021/BI00793A005
Schreiber MJ, Nunez GH (2021). Calcium carbonate can be used to manage soilless substrate Ph for blueberry production. Horticulturae 7(4):74. https://doi.org/10.3390/HORTICULTURAE7040074/S1
Steffen-Heins A, Steffens B (2015). EPR spectroscopy and its use in planta-a promising technique to disentangle the origin of specific ROS. Frontiers in Environmental Science 3:128489. https://doi.org/10.3389/FENVS.2015.00015/BIBTEX
Urbinati G, Nota P, Frattarelli A, Lucioli S, Forni C, Caboni E (2020). Morpho-physiological responses of sea buckthorn (Hippophae rhamnoides) to NaCl stress. Plant Biosystems - An International Journal Dealing with All Aspects of Plant Biology 154(6):827-834. https://doi.org/10.1080/11263504.2019.1701121
Villafranca JJ, Ash DE, Wedler FC (2002). Manganese(II) and substrate interaction with unadenylylated glutamine synthetase (Escherichia coli W). II. Electron paramagnetic resonance and nuclear magnetic resonance studies of enzyme-bound manganese(II) with substrates and a potential transition-state analogue, methionine sulfoximine. Biochemistry 15(3):544-553. https://doi.org/10.1021/BI00648A014
Wang YH, Zhang G, Chen Y, Gao J, Sun YR, Sun MF, Chen JP (2019). Exogenous application of gibberellic acid and ascorbic acid improved tolerance of okra seedlings to NaCl stress. Acta Physiologiae Plantarum 41(6):1-10. https://doi.org/10.1007/S11738-019-2869-Y/METRICS
Win KT, Fukuyo T, Keiki O, Ohwaki Y (2018). The ACC deaminase expressing endophyte Pseudomonas spp. Enhances NaCl stress tolerance by reducing stress-related ethylene production, resulting in improved growth, photosynthetic performance, and ionic balance in tomato plants. Plant Physiology and Biochemistry 127:599-607. https://doi.org/10.1016/J.PLAPHY.2018.04.038
Wróblewska W, Czernyszewicz E (2017). The level and price volatility of blueberry fruits (vaccinium corymbosum l.) obtained by producer and on the wholesale market during 2007-2016. Annals of the polish association of Agricultural and Agribusiness Economists XIX(2):275-281. https://doi.org/10.5604/01.3001.0010.1217
Yildirim E, Ekinci M, Turan M, Dursun A, Kul R, Parlakova F (2015). Roles of glycine betaine in mitigating deleterious effect of salt stress on lettuce (Lactuca sativa L.). Archives of Agronomy and Soil Science 61(12):1673-1689. https://doi.org/10.1080/03650340.2015.1030611
Zaki HEM, Radwan KSA (2022a). The use of osmoregulators and antioxidants to mitigate the adverse impacts of salinity stress in diploid and tetraploid potato genotypes (Solanum spp.). Chemical and Biological Technologies in Agriculture 9:19. https://doi.org/10.1186/S40538-022-00286-3/TABLES/6
Zaki HEM, Radwan KSA (2022b). Response of potato (Solanum tuberosum L.) cultivars to drought stress under in vitro and field conditions. Chemical and Biological Technologies in Agriculture 9:1. https://doi.org/10.1186/S40538-021-00266-Z/FIGURES/4
Zaki HEM, Yokoi S (2016). A comparative in vitro study of salt tolerance in cultivated tomato and related wild species. Plant Biotechnology 33(5):361. https://doi.org/10.5511/PLANTBIOTECHNOLOGY.16.1006A
Zayed B, Abdelaal M, Deweedar G (2017). Response of rice yield and soil to sulfur application under water and salinity stresses. Egyptian Journal of Agronomy 3:239-249. https://doi.org/10.21608/agro.2017.1274.1067
Zhou Y, Liu Y, Zhang X, Gao X, Shao T, Long X, Rengel Z (2022). Effects of soil properties and microbiome on highbush blueberry (Vaccinium corymbosum) growth. Agronomy 12(6):1263. https://doi.org/10.3390/AGRONOMY12061263
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