Abstract
NaCl priming of seeds can improve seed germination and seedling growth and increase the tolerance to salinity, but most research on salt tolerance in priming plants is restricted to the germination and seedling stages. The aim of this study was to evaluate the effect of soil water salinity and seed salt priming on the physiological responses of adult Solanum lycopersicum Mill. ‘Río Grande’ plants. A group of seeds was germinated in freshwater (control), and another group was germinated in an 85 mM NaCl solution (salt priming). Plants from both groups were grown during a period of 8 weeks in hydroponic culture. Subsequently, control and priming plants were divided into two subgroups. One subgroup was kept in freshwater, while 85 mM NaCl was added to the nutrient solution of the second subgroup. Tissue water relations, gas exchange, fluorescence and growth parameters were obtained at 0–15 days after the beginning of the experiment. The addition of NaCl to adult plants led to a reduction of leaf solute potential, photosynthetic maximum carboxylation and transpiration rates, and stomatal conductance but neither the chlorophyll content nor any of the parameters associated with the growth of the plant were negatively affected. Salt seed priming induces physiological changes such as improved osmotic adjustment, maximum quantum yield of photosystem II and, partially, the water use efficiency, characteristics that are considered to improve tolerance to salt stress.
Similar content being viewed by others
Abbreviations
- C a :
-
Ambient CO2 concentration
- A max :
-
CO2 assimilation rate under conditions of saturating PPFD and CO2
- Γ:
-
CO2 compensation point
- ETR:
-
Electron transport rate
- A :
-
Instantaneous photosynthetic rate
- C i :
-
Intercellular CO2 concentration
- RWC:
-
Leaf relative water content
- Ψs :
-
Leaf solute potential
- FM′:
-
Maximal fluorescence in light-adapted leaves
- F M :
-
Maximal fluorescence in dark-adapted state
- Vcmax :
-
Maximum carboxylation rate
- FV/FM :
-
Maximum quantum yield of PSII in dark-adapted leaves
- Fo:
-
Minimal fluorescence
- q N :
-
Non-photochemical quenching
- Ψp:
-
Pressure potential
- PS:
-
Primed plants grown in NaCl
- ΦPSII :
-
Quantum yield of PSII
- RGR:
-
Relative growth rate
- SGR:
-
Seed germination rate
- F :
-
Steady state in light-adapted leaves
- g s :
-
Stomatal conductance
- E :
-
Transpiration rate
- Ψw :
-
Water potential
- WUE:
-
Water use efficiency
References
Alvarado AD, Bradford KJ (1988) Priming and storage of tomato (Lycopersicon esculentum) seeds. I. Effects of storage temperature on germination rate and viability. Seed Sci Technol 16:601–612
Amooaghaie R, Tabatabaie F (2017) Osmopriming-induced salt tolerance during seed germination of alfalfa most likely mediates through H2O2 signaling and upregulation of heme oxygenase. Protoplasma 254:1791–1803. https://doi.org/10.1007/s00709-016-1069-5
Argerich CA, Bradford KJ (1989) The effects of priming and ageing on seed vigour in tomato. J Exp Bot 40:599–607. https://doi.org/10.1093/jxb/40.5.599
Arif M, Jan MT, Khan NU, Khan A, Khan MJ, Munir I (2010) Effect of seed priming on growth parameters of soybean. Pak J Bot 42:2803–2812
Ashraf MY, Bhatti AS (2000) Effect of salinity on growth and chlorophyll content in rice. Pak J Sci Ind Res 43:130–131
Balibrea M, Dell’Amico J, Bolarín M, Pérez-Alfocea F (2000) Carbon partitioning and sucrose metabolism in tomato plants growing under salinity. Physiol Plant 110:503–511. https://doi.org/10.1111/j.1399-3054.2000.1100412.x
Begum F, Karmoker J, Fattach Q, Maniruzzaman A (1992) The Effect of salinity on germination and its correlation with K+, Na+, Cl− accumulation in germinating seeds of Triticum aestivum L. cv. Akbar. Plant Cell Physiol 33:1009–1014. https://doi.org/10.1093/oxfordjournals.pcp.a078324
Brocklehurst PA, Dearman J, Drew RLK (1984) Effects of osmotic priming on seed germination and seedling growth in leek. Sci Hortic 24:201–210. https://doi.org/10.1016/0304-4238(84)90103-1
Cano EA, Bolarin MC, Perez-Alfocea F, Caro M (1991) Effect of NaCl priming on increased salt tolerance in tomato. J Hortic Sci 66:621–628. https://doi.org/10.1080/00221589.1991.11516192
Cayuela E, Perez-Alfocea F, Caro M, Bolarin MC (1996) Priming of seeds with NaCl induces physiological changes in tomato plants grown under salt stress. Physiol Plant 96:231–236. https://doi.org/10.1111/j.1399-3054.1996.tb00207.x
Chartzoulakis K, Klapaki G (2000) Response of two greenhouse pepper hybrids to NaCl salinity during different growth stages. Sci Hortic 86:247–260. https://doi.org/10.1016/S0304-4238(00)00151-5
Chavez M, Flexas J, Pinheiro C (2009) Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann Bot 103:551–560. https://doi.org/10.1093/aob/mcn125
Cuartero J, Fernandez-Muñoz R (1999) Tomato and salinity. Sci Hortic 78:83–125. https://doi.org/10.1016/S0304-4238(98)00191-5
Cuartero J, Bolarín M, Asíns M, Moreno V (2006) Increasing salt tolerance in the tomato. J Exp Bot 57:1045–1058. https://doi.org/10.1093/jxb/erj102
Demir I, Mavi K (2008) Effect of salt and osmotic stresses on the germination of pepper seeds of different maturation stages. Braz Arch Biol Technol 51:897–902. https://doi.org/10.1590/S1516-89132008000500004
Demirkaya M (2014) Improvement in tolerance to salt stress during tomato cultivation. Turk J Biol 38:193–199. https://doi.org/10.3906/bi-1307-62
Dogan M, Tipirdamaz R, Demir Y (2010) Salt resistance of tomato species grown in sand culture. Plant Soil Environ 56:499–507. https://doi.org/10.17221/24/2010-pse
Durukan H, Demirbas A (2018) The effects of different salt doses on yield and nutrient uptake of tomato plant. Sci Pap Ser A Agron 61:71–76
Elouaer MA, Hannachi C (2012) Seed priming to improve germination and seedling growth of safflower (Carthamus tinctorius) under salt stress. Eurasia J Biosci 6:76–84. https://doi.org/10.5053/ejobios.2012.6.0.9
Evans G (1972) The quantitative analysis of plant growth. Studies in ecology, vol 1. Blackwell Scientific Publications, London
Farhoudi R, Saeedipour S, Mohammadreza D (2011) The effect of NaCl seed priming on salt tolerance, antioxidant enzyme activity, proline and carbohydrate accumulation of Muskmelon (Cucumis melo L.) under saline condition. Afr J Agric Res 6:1363–1370. https://doi.org/10.5897/AJAR10.1007
Farooq M, Basra SMA, Saleem BA, Nafees M, Chishti SA (2005) Enhancement of tomato seed germination and seedling vigor by osmopriming. Pak J Agric Sci 42:36–41
Farooq M, Hussai M, Nawaz A, Lee D, Alghamdi SS, Siddique KH (2017) Seed priming improves chilling tolerance in chickpea by modulating germination metabolism, trehalose accumulation and carbon assimilation. Plant Physiol Biochem 111:274–283. https://doi.org/10.1016/j.plaphy.2016.12.012
Flexas J, Bota J, Loreto F, Cornic G, Sharkey T (2004) Diffusive and metabolic limitations to photosynthesis under drought and salinity in C3 plants. Plant Biol 6:269–279. https://doi.org/10.1055/s-2004-820867
Flowers TJ (2004) Improving crop salt tolerance. J Exp Bot 55:307–319. https://doi.org/10.1093/jxb/erh003
Gebreegziabher BG, Qufa CA (2017) Plant physiological stimulation by seeds salt priming in maize (Zea mays): prospect for salt tolerance. Afr J Biotechnol 16:209. https://doi.org/10.5897/AJB2016.15819
Genty B, Briantais J, Baker N (1989) The relationships between the quantum yield of photosynthesis electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990:87–92. https://doi.org/10.1016/S0304-4165(89)80016-9
Gharbi F, Zribi L, Ben Daly A, Rejeb S, Hanchi B (2018) Photosynthetic responses of tomato leaves to salt and cadmium stresses: growth and chlorophyll a fluorescence kinetic analyses. Pol J Environ Stud 27:1–10
Ghassemi-Golezani K, Esmaeilpour B (2008) The effect of salt priming on the performance of differentially mature cucumber (Cucumis sativus) seeds. Not Bot Hortic Agrobot Cluj-Na 36:67–70. https://doi.org/10.15835/nbha36271
Gholami M, Mokhtarian F, Baninasab B (2015) Seed halopriming improves the germination performance of black seed (Nigella sativa) under salinity stress conditions. J Crop Sci Biotechnol 18:21–26. https://doi.org/10.1007/s12892-014-0078-1
Goykovic VC, Alanoca PN, Llave MC (2014) Efecto de la salinidad sobre la germinación y crecimiento vegetativo de plantas de tomate silvestres y cultivada. Interciencia 39:511–517
Greenway H, Munns R (1980) Mechanism of salt tolerance in nonhalophytes. Annu Rev Plant Physiol 31:149–190. https://doi.org/10.1146/annurevpp.31.060180.001053
Hajer AS, Malibari AA, Al-Zahrani HS, Almaghrabi OA (2006) Responses of three tomato cultivars to sea water salinity. 1. Effect of salinity on the seedling growth. Afr J Biotechnol 5:855–861
Haupt-Herting S, Klug K, Fock H (2001) A new approach to measure gross CO2 fluxes in leaves. Gross CO2 assimilation, photorespiration, and mitochondrial respiration in the light in tomato under drought stress. Plant Physiol 126:388–396. https://doi.org/10.1104/pp.126.1.388
Hunt R, Causton D, Shipley B, Askew A (2002) A modern tool for classical plant growth analysis. Ann Bot 90:485–488. https://doi.org/10.1093/aob/mcf214
Ibrahim EA (2016) Seed priming to alleviate salinity stress in germinating seeds. J Plant Physiol 192:38–46. https://doi.org/10.1016/j.jplph.2015.12.011
Ismail AI, El-Araby MM, Hegazi AZA, Moustafa SMA (2005) Optimization of priming benefits in tomato (Lycopersicon esculentum M.) and changes in some osmolytes the hydration phase. Asian J Plant Sci 4:691–701. https://doi.org/10.3923/ajps.2005.691.701
Jisha KC, Vijayakumari K, Puthur JT (2013) Seed priming for abiotic stress tolerance: an overview. Acta Physiol Plant 35:1381–1396. https://doi.org/10.1007/s11738-012-1186-5
Juan M, Rivero R, Romero L, Ruiz J (2005) Evaluation of some nutritional and biochemical indicators in selecting salt-resistant tomato cultivars. Environ Exp Bot 54:193–201. https://doi.org/10.1016/j.envexpbot.2004.07.004
Khan H, Ayub C, Pervez P, Bilal R, Shahid M, Ziaf K (2009) Effect of seed priming with NaCl on salinity tolerance of hot pepper (Capsicum annuum L.) at seedling stage. Soil Environ 28:81–87
Lichtenthaler H, Wellburn A (1983) Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochem Soc Trans 603:591–592. https://doi.org/10.1042/bst0110591
Mirabi E, Hasanabadi M (2012) Effect of seed priming on some characteristic of seedling and seed vigor of tomato (Lycopersicun esculentum). J Adv Lab Res Biol 3:237–240
Montesano F, van Iersel M (2007) Calcium can prevent toxic effects of Na+ on tomato leaf photosynthesis but does not restore growth. J Am Soc Hortic Sci 132:310–318
Mozafariyan M, Saghafi K, Bayat AE, Bakhtiari S (2013) The effects of different sodium chloride concentrations on the growth and photosynthesis parameters of tomato (Lycopersicum esculentum cv. Foria). Int J Agric Crop Sci 6:203–207
Munns R, Tester M (2008) Mechanisms of salinity tolerance. Ann Rev Plant Biol 59:651–681. https://doi.org/10.1146/annurev.arplant.59.032607.092911
Nascimento W (2003) Muskmelon seed germination and seedling development in response to seed priming. Sci Agric 60:71–75. https://doi.org/10.1590/S0103-90162003000100011
Nawaz A, Amjad M, Jahangir MM, Khan SM, Cui H, Hu J (2012) Induction of salt tolerance in tomato (Lycopersicon esculentum Mill.) seeds through sand priming. Aust J Crop Sci 6:1199–1203
Negrão S, Schmockel SM, Tester M (2017) Evaluating physiological responses of plants to salinity stress. Ann Bot 119:1–11
Pradhan N, Prakash P, Tiwari SK, Manimurugan C, Sharma RP, Singh PM (2014) Osmopriming of tomato genotypes with polyethylene glycol 6000 induces tolerance to salinity stress. Trends Biosci 7:4412–4417
Romero-Aranda R, Soria T, Cuartero J (2001) Tomato plant-water uptake and plant-water relationships under saline growth conditions. Plant Sci 160:65–272. https://doi.org/10.1016/S0168-9452(00)00388-5
Schreiber U, Bilger W, Neubauer C (1995) Chlorophyll fluorescence as a nonintrusive indicator of rapid assessment of in vivo photosynthesis. In: Schulze ED, Caldwell MM (eds) Ecophysiology of photosynthesis. Ecological studies, vol 100. Springer, London, pp 49–70. https://doi.org/10.1007/978-3-642-79354-7_3
Shannon MC, Gronwald JW, Tal M (1987) Effect of salinity on growth and accumulation of organic and inorganic ions in cultivated and wild tomato species. J Am Soc Hortic Sci 112:516–523
Singh EV, Sastry D, Singh V (2012) Effect of salinity on tomato (Lycopersicon esculentum Mill.) during seed germination stage. Physiol Mol Biol Plants 18:45–50. https://doi.org/10.1007/s12298-011-0097-z
Soughir M, Elouaer MA, Hannachi C (2013) The effect of NaCl priming on emergence, growth and yield of fenugreek under saline conditions. Cercet Agron Mold 46:73–83. https://doi.org/10.2478/v10298-012-0085-7
Souza MO, Pelacani CR, Willmes LA, De Castro RD, Hilhorst HW, Ligterink W (2016) Effect of osmopriming on germination and initial growth of Physalis angulata L. under salt stress and on expression of associated genes. An Acad Bras Cienc 88:503–516. https://doi.org/10.1590/0001-3765201620150043
Stofella PJ, Lipucci DP, Pardossi A, Toganoni F (1992) Seedling root morphology and shoot growth after seed priming or pre-emergence of bell pepper. J Am Soc Hortic Sci 27:214–215
Tezara W, Fernández MD, Donoso C, Herrera A (1998) Seasonal changes in photosynthesis and stomatal conductance of five species from a semiarid ecosystem. Photosynthetica 35:399–410
Turner NC, Jones M (1980) Turgor maintenance by osmotic adjustment: a review and evaluation. In: Turner NC, Kramer PJ (eds) Adaptations of plants to water and high temperature stress. Wiley, New York, pp 87–103
von Caemmerer S, Farquhar GD (1981) Some relationships between biochemistry of photosynthesis and gas exchange of leaves. Planta 153:376–387
Xu H, Gauthier L, Gosselin A (1997) Greenhouse tomato photosynthetic acclimation to water deficit and response to salt accumulation in the substrate. J Jpn Soc Hortic Sci 65:777–784. https://doi.org/10.2503/jjshs.65.777
Yamaguchi T, Blumwald E (2005) Developing salt-tolerant crop plants: challenges and opportunities. Trends Plant Sci 10:615–620. https://doi.org/10.1016/j.tplants.2005.10.002
Zhang P, Senge M, Dai Y (2016) Effects of salinity stress on growth, yield, fruit quality and water use efficiency of tomato under hydroponics system. Rev Agric Sci 4:46–55
Zribi L, Fatma G, Fatma R, Salwa R, Hassan N, Mohamed R (2009) Application of chlorophyll fluorescence for the diagnosis of salt stress in tomato “Solanum lycopersicum (variety Rio Grande)”. Sci Hortic 120:367–372. https://doi.org/10.1016/j.scienta.2008.11.025
Acknowledgements
Financial support was provided by the Decanato de Investigaciones USB. We are grateful to Dr. Wilmer Tezara for kindly facilitating the gas exchange and fluorescence equipment and A Herrera for helpful comments on previous versions of this manuscript. I want to thank anonymous reviewers for their insightful comments that improved the manuscript.
Author information
Authors and Affiliations
Contributions
PGG, NS and OM designed the research; PGG and OM carried out the experiments; PGG, NS and OM analyzed the data and wrote the paper. The authors declare no conflict of interest.
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
González-Grande, P., Suárez, N. & Marín, O. Effect of salinity and seed salt priming on the physiology of adult plants of Solanum lycopersicum cv. ‘Río Grande’. Braz. J. Bot 43, 775–787 (2020). https://doi.org/10.1007/s40415-020-00636-1
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s40415-020-00636-1