Introduction

Tomato (Solanum lycopersicum L.) placed in family Solanaceae is one of the most widely cultivated vegetables across the globe. Tomato berries are nutraceuticaly important because of the presence of diverse phytochemicals such as vitamin C, lycopene, beta-carotene, flavonoids and hydroxycinnamic acid derivatives making them an indispensable component of our daily diet. There is a major surge for tomato berries due to the presence of lycopene, a fat-soluble pigment valued for its anti-oxidant and anti-cancer properties ¹. To meet the growing demands, cultivation of this important vegetable needs to be enhanced. Currently, tomato is cultivated in 50 Lakh hectare land world-wide out of which nearly 8.12 Lakh hectare is under cultivation in India (FAOSTAT 2020). With limited agrarian land and paucity of fresh water resources, the possibility of increasing the production of tomato is either by utilizing unproductive or salt affected land for its cultivation or unportable water generally high in dissolved salts for irrigation ². Tomato is relatively susceptible to salinity during seed germination and seedling establishment phase. The commercial production of tomato is done by sowing seeds directly in the field rather than transplanting ³. Saline habitats increase the time required for germination and lower the germination percentage in tomato ^4,5. However, rapid and synchronized seed germination is essential in tomato for proper stand establishment and increasing its production in salt stressed environments. Presently, seed priming is becoming a lucrative method for alleviating salinity stress in tomato during germination which happens to be the most susceptible stage in the life cycle of this plant ⁶. Priming permits certain pre‐germinative physiological and biochemical changes to occur without radicle emergence form the seed coat ^7,8 supporting better growth and development of primed seeds in environmentally challenged conditions ⁹. Seed priming was beneficial for successful adaptation of tomato and numerous other crops in presence of salt stress as reported earlier ^{6, 10-13}. This review focuses on different seed priming methods that were effective in tomato for mitigating salt stress and improving its productivity in salinity stressed habitats.

Salinity and Priming Methods

The priming methods which successfully counteracted the harmful effects of salinity stress in tomato (Table 1) by improving the germination and growth parameters are being discussed below.

Hydropriming

Hydropriming is a traditional method of soaking seeds in water with or without aeration followed by drying to original moisture content prior to sowing. It is important to standardize the soaking conditions such as duration, temperature and seed to water ratio for uniform hydration and germination ¹⁴. Hydropriming is a simple, cost-effective and environmentally safe method¹⁵. Hydroprimed seeds of tomato exhibited better germination percentage and adjusted well in saline conditions ¹⁶.

Osmopriming

In osmopriming seeds are immersed in osmotic solution of low water potential for gradual and controlled imbibition preferably under aeration and dried to initial weight before sowing. Generally, osmolytes such as polyethylene glycol (PEG), sugar alcohols (mannitol, sorbitol), glycerol are utilized in osmopriming ¹⁷. Priming treatments using osmotic solutions are effective compared to hydropriming as they permit gradual entry of water within the seeds reducing accumulation of reactive oxygen species and preventing oxidative injury ¹⁸. Osmopriming with PEG increased the germination percentage and plant height ¹⁹. It also lowered lipid peroxidation, relative electrolyte leakage and malondialdehyde levels ²⁰ which helped in improving the tolerance of tomato towards salt stress.

When inorganic salt solutions of sodium chloride, potassium chloride, calcium chloride, magnesium nitrate, copper sulphate, zinc sulphate etc. are used as osmotic agents for priming individually or in combinations it is known as halopriming ²¹. Priming with sodium chloride at seed sowing rather than post-emergence (4-leaf stage) helped in enhancing the yield in presence of salt stress ²². Positive effects of halopriming such as early emergence, enhanced germination and seedling vigor under NaCl mediated abiotic stress is documented in tomato^8,23-27. Biochemical parameters such as chlorophyll, sugar, proteins, antioxidant enzymes remained less impacted in primed seeds as compared to non-primed seeds^28,29.  Halopriming is a promising method to alleviate the effect of salt stress in tomato resulting in better germination parameters and biochemical functions.

Solid Matrix Priming

Seeds are incubated with solid matrices of inorganic or organic origin that serve as water carrier permitting slow and controlled hydration akin to seed imbibition in nature³⁰. It is performed in a sealed container that allows air circulation but prevents evaporation. Post priming seeds are separated from solid matrix, washed and dried. The materials used for solid matrix priming should have high water holding capacity, less bulk density and low osmotic potential ¹⁵. Some of the naturally occurring solid matrices used for priming include calcium silicate, calcined clay, vermiculite, cocopeat, perlite ³¹, sand, charcoal, sawdust, compost, press mud ³², Sphagnum moss, Wheat bran etc. ³³ Solid matrix priming is cost-effective substitute to osmopriming as it avoids handling large volumes of osmotic solutions or maintenance of temperature and aeration ³⁴. Solid matrix priming with sand particles improved the germination parameters, seedling height, antioxidant enzymes and reduced malondialdehyde content in tomato in presence of salinity stress ³⁵.

Hormonal Priming

Plant growth regulators or phytohormones are organic compounds synthesized in small amounts within the plants, that facilitate proper growth and development. There are nine phytohormone’s namely auxin, cytokinin, gibberellin, abscisic acid, ethylene, jasmonic acid, salicylic acid, brassinosteroids and strigolactones ³⁶. Priming of seeds with phytohormones termed as hormonal priming is helpful in increasing the germination response under abiotic stress. Hormonal priming increases the enzymatic activity of amylases and proteases that help in breakdown of reserve food materials such as starch and protein for its mobilization to the embryo thus hastening the germination events ³⁷. Priming with plant growth regulators such as salicylic acid and jasmonic acid accelerate germination percentage and improve seedling establishment by maintaining the functions of auxins and cytokinins within the plant ³⁸. There are reports on hormonal priming with kinetin, gibberellin, salicylic acid and ascorbic acid in tomato ^39-43. Improvement in germination percentage and seed vigour was achieved on priming with ascorbic acid, salicylic acid⁴⁰ and gibberellic acid ⁴¹ in stressful conditions. Priming with kinetin ³⁹ and ascorbic acid ⁴³ reduced lipid peroxidation and hydrogen peroxide levels resulting in improved tolerance towards salt stress. The germination percentage and biochemical parameters enhanced on ascorbic acid treatment thus negating the effect of salinity on emergence and early seedling growth ⁴⁴.

Chemical Priming

Seeds are soaked in natural or synthetic chemical agents for preparing them to withstand stress during emergence and early growth phases ⁴⁵. Chemical priming is emerging as an effective method for handling abiotic stress ⁴⁶. Several chemicals are employed as priming agents such as amino acids ^16,44,47, hydrogen peroxide ⁴², hydrogen sulphide, nitric oxide, chitosan, menadione sodium bisulfite ²⁷, selenium, ethanol, putrescine, choline, butanolide, polyamines etc.^13,45 for stress management. Priming of tomato seeds with proline improved germination percentage, radicle length and seedling dry weight ⁴⁷. Accumulation of total soluble sugars, proteins and antioxidant enzymes in proline primed seeds helped them withstand salt stress ⁴⁴.

Biopriming

Biostimulants are natural substances required in small amounts which help the plant by enhancing the nutrient uptake and utilization, improving availability of nutrients, increasing tolerance to abiotic stress and leading towards better crop quality and yield. Biostimulants comprise of various natural substances such as humic acid, fulvic acid, plant and animal protein hydrolysates, seaweed extracts, botanicals, chitosan, mycorrhiza, plant growth promoting rhizobacteria, inorganic compounds like silicon etc. ⁴⁸ They can be applied to the seeds, plants or rhizosphere. Many biostimulants are being used as seed biopriming agents for better tolerance towards abiotic stress ^49,50 amongst them sea weed extracts and Bacillus paralicheniformis suspension have shown promising response in ameliorating salt stress in tomato. Priming with Bacillus paralicheniformis suspension and Ulva lactuca methanol extract and its fractions increased the germination percentage and biomass accumulation ^51,52.

Physical Priming Methods

Seed priming with physical agents presents a promising advancement compared to the usual water or chemical based methods ⁵³. Physical priming methods are less expensive and more environment friendly alternative to the traditional priming procedures. Some of the physical agents generally employed in seed invigoration are magnetic fields, electromagnetic waves (microwaves, infra-red rays, UV rays, X-rays, gamma rays), ultrasonic waves, cold plasma, laser beams and low energy electronic beams ^53-55. Physical priming agents showed improvement in seed germination rate, seedling vigour and better tolerance towards abiotic stress ⁵⁶. Improved germination response might be attributed to enhanced activities of hydrolysing enzymes, whereas better adaptability in stressed environments could be due to increased activity of antioxidant enzymes in response to physical priming agents. UV-C seed priming mitigated the effect of salt stress in tomato seedlings. Increment in antioxidant activities in UV-C primed seeds helped them to adapt well in presence of salinity stress ⁵⁷.

Table 1: Priming methods implemented in tomato for mitigating salinity stress.

Conclusion

With limited farming land and fresh water resources, the area under cultivation can be increased by utilizing unproductive or salt affected land and poor-quality water high in salts for agriculture purpose. Tomato is moderately sensitive to salinity during seed germination and early seedling stage. Some of the seed priming methods such as hydropriming, osmopriming, solid matrix priming, hormonal priming, chemical priming, biopriming and priming with physical agents were effective in coping with salt stress in tomato. Primed seeds of tomato presented better germination percentage, speed, vigor, uniformity as compared to unprimed seeds in presence of salinity stress. Priming treatments were effective in improving the biochemical parameters such as chlorophyll, total soluble sugars, proteins and antioxidant enzymes in tomato seedlings proving advantageous for sustainability in salt stressed conditions. Seed priming is simple and profitable technique that farmers can easily implement during tomato cultivation. Primed tomato seeds will be better equipped for tolerating salt stress that happens to be a persistent problem in changing climatic conditions and is one of the major threats to global food security.  

Acknowledgements

The financial support received through University Grants Commission (UGC); New Delhi (Minor Research Project 47-1442/10 WRO) is gratefully acknowledged. The author would like to thank The Principal, Fergusson College (Autonomous), Pune for providing the necessary facilities.

Conflict of Interest

Author declares no conflict of interest.

Funding Sources

This study was funded by University Grants Commission (UGC); New Delhi (Minor Research Project 47-1442/10 WRO).

References 

1. Gerszberg A., Hnatuszko-Konka K., Kowalczyk, T and Kononowicz A.K. Tomato (Solanum lycopersicum L.) in the service of biotechnology. Plant Cell Tissue Organ Culture. 2015; 120:881-902.
2. Phogat V., Sharma S.K., Kumar S., Satyavan and Gupta S.K. Vegetable cultivation with poor quality water. In: Technical Bulletin. Department of Soil Science; CCS Haryana Agricultural University, Hisar, India. 2010; pp. 1-72.
3. Foolad M.R., Subbiah P., Hargrave G and Lin G.Y. Genetic relationships among cold, salt and drought tolerance during seed germination in an interspecific cross of tomato. Euphytica. 2003; 130:199-206.
4. Foolad M. R. Recent advances in genetics of salt tolerance in tomato. Plant Cell Tissue and Organ Culture. 2004; 76:101-119.
5. Seth R and Kendurkar S. V. In vitro screening: An effective method for evaluation of commercial cultivars of tomato towards salinity stress. International Journal of Current Microbiology and Applied Science. 2015; 4: 725-730.
6. Delian E., Badulescu L., Dobrescu A., Chira L and Lagunovschi-Luchian V. A brief overview of seed priming benefits in tomato. Romanian Biotechnological Letters. 2017; 22(3): 12505-12513.
7. Ashraf M and Foolad M. R. Pre-sowing seed treatment – A shotgun approach to improve germination, plant growth and crop yield under saline and non-saline conditions. Advances in Agronomy. 2005; 88: 223-271.
8. Ebrahimi R., Ahmadizadehi M and Rahbarin P. Enhancing stand establishment of tomato cultivars under salt stress condition. South West Journal of Horticulture Biology and Environment. 2014; 5(1): 19-42.
9. Jisha K. C. and Puther, J. T. Halopriming of seeds imparts tolerance to NaCl and PEG induced stress in Vigna radiata (L.) Wilczek varieties. Physiology and Molecular Biology of Plants. 2014; 20(3): 303-312.
10. Ibrahim E. A. Seed priming to alleviate salinity stress in germinating seeds. Journal of Plant Physiology. 2016; 192: 38-46. 
11. Banerjee A. and Roychoudhury A.: Seed priming technology in the amelioration of salinity stress in plants. In: Advances in Seed Priming (Rakshit A & Singh H. B, ed), Singapore: Springer. 2018; pp 81-93.  https://doi.org/10.1007/978-981-13-0032-5_5
12. Verma S.R. and Solanki H. A. Alleviating salinity stress during seed germination by priming techniques: A review. International Journal of Scientific Research in Science and Technology. 2021; 8(2): 198-202.
13. Hussain S., Ali B., Saquib M.: Seed priming to enhance salt and drought stress tolerance in plants: advances and prospects. In: Climate Change and Crop stress: Molecules to Ecosystem (Shanker AK, Shanker C, Anand A. & Maheswari M, ed). USA: Academic Press. 2022; pp 441-464. https://doi.org/10.1016/B978-0-12-816091-6.00012-2. 
14. Thakur, M., Sharma, P. and Anand, A. Seed priming-induced early vigor in crops: An alternate strategy for abiotic stress tolerance. In: Priming and Pretreatment of Seeds and Seedlings (Hasanuzzaman M & Fotopoulos V, ed), Singapore: Springer Nature. 2019; pp 1- 10. https://doi.org/10.1007/978-981-13-8625-1
15. Sher, A., Taskeen S., Ahmad N., Ijaz M., Sattar A. and Ahmad S. Methods of seed priming. In: Priming and Pretreatment of Seeds and Seedlings (Hasanuzzaman M & Fotopoulos V, ed), Singapore: Springer Nature. 2019; pp 1- 10. https://doi.org/10.1007/978-981-13-8625-1.
16. Seth R. Hydropriming alleviates salinity stress in commercial cultivars of Tomato (Solanum lycopersicum L.) under in vitro conditions. Advances in Plant Sciences. 2017; 30 (2): 157-160.
17. Ullah A., Babar S., Tanveer M., Nadeem F., Sharma A., Lee D.J and Rehman A. Abiotic stress tolerance in plants through pre-sowing seed treatments with mineral elements and growth regulators. In: Priming and Pretreatment of Seeds and Seedlings (Hasanuzzaman M & Fotopoulos V, ed). Singapore: Springer Nature. 2019. pp 427-445. https://doi.org/10.1007/978-981-13-8625-1.
18. Waqas M., Korres N. E., Khan M. D., Nizami A. S., Deeba F., Ali I. and Hussain H. Advances in the concept and methods of seed priming. In: Priming and Pretreatment of Seeds and Seedlings (Hasanuzzaman M & Fotopoulos V, ed). Singapore: Springer Nature. 2019; pp 11-41. https://doi.org/10.1007/978-981-13-8625-1_2
19. Pradhan N., Prakash P., Manimurugan C., Tiwari S.K., Sharma R.P., Singh P.M. Screening of tomato genotypes using osmopriming with PEG 6000 under salinity stress. Research in Environment and Life Sciences. 2015; 8(2): 245-250.
20. Zhang M., Wang Z., Yuan L., Yin C., Cheng J., Wang L., Huang J. and Zhang H. Osmopriming improves tomato seed vigor under aging and salinity stress. African Journal of Biotechnology. 2012; 11 (23): 6305-6311.
21. Gour T., Lal R., Heikrujam M., Gupta A., Singh V., Vashishtha A., Agarwal L. K., Kumar R., Chetri S.P.K and Sharma K.: Halopriming: Sustainable approach for abiotic stress management in crops. In: Plant Stress Challenges and Management in the New Decade (Roy S, Mathur P, Chakraborty A.P. & Saha S.P, ed). Switzerland AG: Springer Nature. 2022; pp 135-147.
22. Cano E. A., Bolarin M. C., Perez-Alfocea F and Cano M. Effect of NaCl priming on increased salt tolerance in tomato. Journal of Horticultural Science. 1991; 66 (5): 621-628.
23. Cayuela E., Perez-Alfocea K., Caro M and Bolarin M.C. Priming of seed with NaCl induces physiological changes in tomato plants grown under salt stress. Physiologia Plantarum. 1996; 96: 231-236.
24. Iseri O.D., Sahin F.I and Haberal M. Sodium chloride priming improves salinity response of tomato at seedling stage. Journal of Plant Nutrition. 2014; 37(3): 374-392.
25. Vaktabhai C.K. and Kumar S. Seedling invigoration by halo priming in tomato against salt stress. Journal of Pharmacognosy and Phytochemistry. 2017; 6(6): 716-722.
26. Biswas S., Rasal-Monir M., Islam M., Modak S and Kabir M.H. Induction of salt tolerance in tomato through seed priming. Plant. 2019; 7(3): 47-53.
27. Niazi A. and Sharifi, F. Effect of chemical seed priming on seed germination and seedling vigor of tomato (Solanum lycopersicum L.) under salinity stress. Iranian Journal of Horticultural Science and Technology. 2019; 20(2): 143-156.
28. Demirkaya M. Improvement in tolerance to salt stress during tomato cultivation. Turkish Journal of Biology. 2014; 38: 193-199.
29. Gonzalez-Grande P., Suarez N and Marin O. Effect of salinity and seed salt priming on the physiology of adult plants of Solanum lycopersicum cv. Rio Grande. Brazilian Journal of Botany. 2020; 43: 775-787.
30. McDonald, M.B. 2000. Seed pre-treatments. In: Seed Technology and its Biological Basis (Black M & Bewley J D, ed). Sheffield Academic Press, Sheffield. 2000; pp 287-325.
31. Kanwar R. and Mehta D.K. Studies on solid matrix priming in bitter gourd (Momordica charantia L.). Journal of Applied and Natural Science. 2017; 9(1): 395-401.
32. Jisha K.C., Vijayakumari, K and Puthur, J.P. Seed priming for abiotic stress tolerance: an overview. Acta Physiologiae Plantarum. 2013; 5: 1381-1396.
33. Mehta D. K., Thakur C., Thakur K. S. and Thakur S. Effect of solid matrix priming of seed on emergence, growth and yield of cucumber. Green Farming. 2013; 4(3): 364-366.
34. Paparella S., Araujo S.S., Rossi G., Wijarasinghe M., Carboneral D. and Balestrazzi A. Seed priming: state of art and new perspectives. Plant Cell Reports. 2015; 34: 1281- 1293. https://doi.org/10.1007/s00299-015-1784-y
35. Nawaz A., Amjad M., Jahangir M.M., Khan S.M., Cui H. and Hu J. Induction of salt tolerance in tomato (Lycopersicon esculentum Mill.) seeds through sand priming. Australian Journal of Crop Science. 2012; 6(7): 1199-1203.
36. Smith S.M., Li C., and Li J. Hormone function in plants. In: Hormone Metabolism and Signaling in Plants (Li J., Li C. & Smith S. M., ed). Academic Press. 2007; pp 1-38.https://doi.org/10.1016/B978-0-12-811562-6.00001-3.
37. Sarfraz M., Hussain S., Ijaz M., Nawaz A., Yasir T. A., Sher A., Wasaya A. and Ahmad S. Abiotic stress tolerance in plants by priming and pretreatments with phytohormones. In: Priming and Pretreatment of Seeds and Seedlings (Hasanuzzaman M & Fotopoulos V, ed). Singapore: Springer Nature. 2019; pp 447-457. https://doi.org/10.1007/978-981-13-8625-1.
38. Rhaman M.S., Imran S., Rauf F., Khatun M., Baskin C.C., Murata Y and Hasanuzzaman, M. Seed priming with phytohormones: An effective approach for the mitigation of abiotic stress. Plants. 2021; 10:37. http://doi.org/10.3390/plants10010037
39. Theerakulpisut P., Lontom W., Kulya J., Bunnag S and Techawongstein S. Effect of seed priming on physiological changes in tomato grown under salt stress. Acta Horticulturae. 2011; 914: 295-300.
40. Ghoohestani A., Gheisary H., Zahedi S.M and Dolatkhahi A. Effect of seed priming of tomato with salicylic acid, ascorbic acid, hydrogen peroxide on germination and plantlet growth in saline conditions. International Journal of Agronomy and Plant Production. 2012; 3 (S), 700-704.
41. Nandhitha G.K., Sivakumar R and Vishnuveni M. Impact of seed treatment with plant growth regulators and nutrients on alleviation of salinity stress in tomato under in vitro conditions. Applied Biological Research. 2016; 18 (2): 203-207.
42. Gaba R., Gupta N and Jindal S.K. Effect of seed treatment on seed germination and vigour parameters in seeds subjected to salt stress in tomato (Solanum lycopersicum L.). Indian Journal of Ecology. 2018; 45 (4): 892-894.
43. Alves R. C., Rossatto D. R., Silva J. S., Checchio M. V., Oliveira K. R., Oliveria F. A., Queiroz S. F., Cruz M. C. P and Gratao P. L. Seed priming with ascorbic acid enhances salt tolerance in micro-tom tomato plants by modifying the antioxidant defence components. Biocatalysis and Agriculture Biotechnology. 2021; 31:101927. https://doi.org/10.1016/j.bcab.2021.101927.
44. Kaur H., Gupta N and Jindal S.K. Influence of proline and ascorbic acid on seed germination behaviour of tomato (Solanum lycopersicum L.) under salt stress. Agriculture Research Journal. 2021; 58(6): 1053-1059.
45. Savvides A., Ali S., Tester M and Fotopoulos V. Chemical priming of plants against multiple abiotic stresses: Mission possible? Trends in Plant Science. 2016; 21(4): 329-340.
46. Sako K., Nguyen H.M and Seki M. Advances in chemical priming to enhance abiotic stress tolerance in plants. Plant Cell Physiology. 2021; 61(12):1955-2003.
47. Hojagan M. P., Arouiee H., Tabatabaei S.J and Neamati S. H. Priming impacts on seed quality of tomato (Lycopersicon esculentum) under salinity condition. International Journal of Agronomy and Agricultural Research. 2017; 11(3):104-109.
48. Jardin P. D. Plant biostimulants: Definition, concept, main categories and regulation. Scientia Horticulturae. 2015; 196: 3-14.
49. Chakraborti S., Bera K., Sadhukhan S and Dutta P. Bio-priming of seeds: Plant stress management and its underlying cellular, biochemical and molecular mechanisms. Plant Stress. 2022; 3: 100052. https://doi.org/10.1016/j.stress.2021.100052
50. Franzoni G., Cocetta G., Prinsi B., Ferrante A and Espen L. Biostimulants on crops: Their impact under abiotic stress conditions. Horticulturae. 2022; 8: 189. https://doi.org/10.3390/horticulturae8030189
51. Parinith G.R., Lakshmi S., Renganayaki P. R and Nakkeeran S. Alleviation of salinity stress via seed priming in tomato (Solanum lycopersicum) with Bacillus paralicheniformis. The Pharma Innovation Journal. 2022; 11(8):201-206.
52. El Boukhari M.E.M., Barakate M., Choumani N., Bouhia Y and Lyamlouli K. Ulva lactuca extract and fractions as seed priming agents mitigate salinity stress in tomato seedling. Plants. 2021; 10 (6): 1104. https://doi.org/10.3390/plants10061104.
53. Bera K., Dutta P and Sadhukhan S. Seed priming with non-ionizing physical agents:plant responses and underlying physiological mechanisms. Plant Cell Reports. 2022; 41(1): 53-73. doi: 10.1007/s00299-021-02798-y.
54. Thakur M., Tiwari S., Kataria S and Anand A. Recent advances in seed priming strategies for enhancing planting value of vegetable seeds. Scientia Horticulturae. 2022; 305, 111355. https://doi.org/10.1016/j.scienta.2022.111355.
55. Afzal I., Rehman H. U., Naveed M and Basra S. M. A. Recent advances in seed enhancements. In: New Challenges in Seed Biology-Basic and Translational Research Driving Seed Technology (Araujo S & Balestrazzi A, ed). IntechOpen. 2016; pp 47-74. DOI:10.5772/64791
56. Araujo S.S., Paparella S., Dondi D., Bentivoglio A., Carbonera D and Balestrazzi A. Physical methods of seed invigoration: Advantages and challenges in seed technology. Frontiers in Plant Science. 2016; 7: 646. doi: 10.3389/fpls.2016.00646
57. Alamer K.H and Attia H. UV-C seed priming improves tomato plant growth against salt stress. Journal of Taibah University for Science. 2022; 16 (1):1118- 1191. doi: 10.1080/16583655.2022.2153443.