Ultrasonic treatment to enhance seed germination and vigour of wheat (Triticum durum) in association with γ-aminobutyric acid (GABA) shunt pathway
Nezar H. Samarah
A * , Nisreen A. AL-Quraan B and Batool S. Al-Wraikat A
+ Author Affiliations
- Author Affiliations
A Department of Plant Production, Faculty of Agriculture, Jordan University of Science and Technology, P.O. Box 3030, Irbid, 22110, Jordan.
B Department of Biotechnology and Genetic Engineering, Faculty of Science and Arts, Jordan University of Science and Technology, Irbid 22110, Jordan.
Functional Plant Biology 50(4) 277-293 https://doi.org/10.1071/FP22211
Submitted: 14 September 2022 Accepted: 27 December 2022 Published: 13 January 2023
© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing
Abstract
Treatments of wheat (Triticum durum L.) seeds with sonication or hydropriming may enhance seed germination and vigour in association with γ-aminobutyric acid (GABA). Therefore, the objective of this study is to examine the effect of sonication and hydropriming treatments on seed germination of wheat through the characterisation of seed germination performance, GABA shunt metabolite level (GABA, glutamate, and alanine), and the level of glutamate decarboxylase (GAD) mRNA transcription. Wheat seeds were exposed to three treatments for 0, 5, 10, 15, and 20 min: (1) sonication with water; (2) sonication without water; and (3) hydropriming without sonication. Treated seeds were evaluated for germination percentage, mean time to germinate, germination rate index in the warm germination test, and seedling emergence and shoot length in the cold test. GABA shunt metabolites level (GABA, glutamate, and alanine), and the level of GAD mRNA transcription were measured for the seeds after treatments and for seedlings during germination and cold tests. Seeds treated with sonication or hydropriming treatments had a higher germination rate index (faster germination) in the standard germination test, and higher seedling emergence and shoot length in the cold test. Seeds treated with sonication or hydropriming treatments showed an enhancement in GABA shunt and their metabolites (alanine and glutamate), and GAD mRNA transcription level compared to untreated-control seeds. In conclusion, the sonication or hydropriming treatments significantly improved the germination performance of wheat and enhanced GABA metabolism to maintain the C:N metabolic balance, especially under cold stress.
Keywords: cold test, GABA: gamma-aminobutyric acid, GAD: glutamate decarboxylase, hydropriming, seed germination, Triticum durum, ultrasonic, wheat.
References
Acharya P, Jayaprakasha GK, Semper J, Patil BS (2020) 1H nuclear magnetic resonance and liquid chromatography coupled with mass spectrometry-based metabolomics reveal enhancement of growth-promoting metabolites in onion seedlings treated with green-synthesized nanomaterials. Journal of Agricultural and Food Chemistry 68, 13206–13220.| 1H nuclear magnetic resonance and liquid chromatography coupled with mass spectrometry-based metabolomics reveal enhancement of growth-promoting metabolites in onion seedlings treated with green-synthesized nanomaterials.Crossref | GoogleScholarGoogle Scholar |
Aladjadjiyan A (2012) Physical factors for plant growth stimulation improve food quality. In ‘Food production – approaches, challenges and tasks’. (Ed. A Aladjadjiyan) p. 270. (IntechOpen)
AL-Quraan NA, Locy RD, Singh NK (2010) Expression of calmodulin genes in wild type and calmodulin mutants of Arabidopsis thaliana under heat stress. Plant Physiology and Biochemistry 48, 697–702.
| Expression of calmodulin genes in wild type and calmodulin mutants of Arabidopsis thaliana under heat stress.Crossref | GoogleScholarGoogle Scholar |
AL-Quraan NA, Locy RD, Singh NK (2012) Heat and cold stresses phenotypes of Arabidopsis thaliana calmodulin mutants: regulation of gamma-aminobutyric acid shunt pathway under temperature stress. International Journal of Plant Biology 3, e2
| Heat and cold stresses phenotypes of Arabidopsis thaliana calmodulin mutants: regulation of gamma-aminobutyric acid shunt pathway under temperature stress.Crossref | GoogleScholarGoogle Scholar |
AL-Quraan NA, Sartawe FA-B, Qaryouti MM (2013) Characterization of γ-aminobutyric acid metabolism and oxidative damage in wheat (Triticum aestivum L.) seedlings under salt and osmotic stress. Journal of Plant Physiology 170, 1003–1009.
| Characterization of γ-aminobutyric acid metabolism and oxidative damage in wheat (Triticum aestivum L.) seedlings under salt and osmotic stress.Crossref | GoogleScholarGoogle Scholar |
AL-Quraan NA, AL-Ajlouni ZI, Obedat DI (2019) The GABA shunt pathway in germinating seeds of wheat (Triticum aestivum L.) and barley (Hordeum vulgare L.) under salt stress. Seed Science Research 29, 250–260.
| The GABA shunt pathway in germinating seeds of wheat (Triticum aestivum L.) and barley (Hordeum vulgare L.) under salt stress.Crossref | GoogleScholarGoogle Scholar |
AL-Quraan NA, AL-Akhras M-AH, Talafha D’aZ (2022) The influence of laser beam and high light intensity on lentil (Lens culinaris) and wheat (Triticum aestivum) seedlings growth and metabolism. Plant Biosystems - An International Journal Dealing with all Aspects of Plant Biology 156, 95–115.
| The influence of laser beam and high light intensity on lentil (Lens culinaris) and wheat (Triticum aestivum) seedlings growth and metabolism.Crossref | GoogleScholarGoogle Scholar |
Andriamparany JN, Buerkert A (2019) Effect of ultrasonic dormancy breaking on seed germination and seedling growth of three wild yam species (Dioscorea spp.) from SW-Madagascar. Genetic Resources and Crop Evolution 66, 1167–1174.
| Effect of ultrasonic dormancy breaking on seed germination and seedling growth of three wild yam species (Dioscorea spp.) from SW-Madagascar.Crossref | GoogleScholarGoogle Scholar |
Angelovici R, Galili G, Fernie AR, Fait A (2010) Seed desiccation: a bridge between maturation and germination. Trends in Plant Science 15, 211–218.
| Seed desiccation: a bridge between maturation and germination.Crossref | GoogleScholarGoogle Scholar |
Ansari O, Sharif Zadeh F (2012) Osmo and hydro priming mediated germination improvement under cold stress conditions in mountain rye (Secale montanum). Cercetări Agronomice în Moldova 45, 53–62.
| Osmo and hydro priming mediated germination improvement under cold stress conditions in mountain rye (Secale montanum).Crossref | GoogleScholarGoogle Scholar |
Ashraf M, Foolad MR (2005) Pre-sowing seed treatment – a shotgun approach to improve germination, plant growth, and crop yield under saline and non-saline conditions. Advances in Agronomy 88, 223–271.
| Pre-sowing seed treatment – a shotgun approach to improve germination, plant growth, and crop yield under saline and non-saline conditions.Crossref | GoogleScholarGoogle Scholar |
Awad TS, Moharram HA, Shaltout OE, Asker D, Youssef MM (2012) Applications of ultrasound in analysis, processing and quality control of food: a review. Food Research International 48, 410–427.
| Applications of ultrasound in analysis, processing and quality control of food: a review.Crossref | GoogleScholarGoogle Scholar |
Banakar VV, Sabnis SS, Gogate PR, Raha A, Saurabh (2022) Ultrasound assisted continuous processing in microreactors with focus on crystallization and chemical synthesis: a critical review. Chemical Engineering Research and Design 182, 273–289.
| Ultrasound assisted continuous processing in microreactors with focus on crystallization and chemical synthesis: a critical review.Crossref | GoogleScholarGoogle Scholar |
Batushansky A, Kirma M, Grillich N, Toubiana D, Pham PA, Balbo I, Fromm H, Galili G, Fernie AR, Fait A (2014) Combined transcriptomics and metabolomics of Arabidopsis thaliana seedlings exposed to exogenous GABA suggest its role in plants is predominantly metabolic. Molecular Plant 7, 1065–1068.
| Combined transcriptomics and metabolomics of Arabidopsis thaliana seedlings exposed to exogenous GABA suggest its role in plants is predominantly metabolic.Crossref | GoogleScholarGoogle Scholar |
Bergmeyer HU (1983) ‘Methods of enzymatic analysis. Vol. 2.’ 3rd edn. pp. 267–268. (Verlag Chemie: Weinheim)
Beyaz R, Ozgen Y, Cavdar A, Yildiz M (2020) The effect of gamma radiation and magnetic field on seed germination andseedling growth at low temperature in sorghum x sudangrass hybrids. Maydica 65, 1–6.
Bonto AP, Tiozon RN, Sreenivasulu N, Camacho DH (2021) Impact of ultrasonic treatment on rice starch and grain functional properties: a review. Ultrasonics Sonochemistry 71, 105383
| Impact of ultrasonic treatment on rice starch and grain functional properties: a review.Crossref | GoogleScholarGoogle Scholar |
Bouché N, Fromm H (2004) GABA in plants: just a metabolite? Trends in Plant Science 9, 110–115.
| GABA in plants: just a metabolite?Crossref | GoogleScholarGoogle Scholar |
Bown AW, MacGregor KB, Shelp BJ (2006) Gamma-aminobutyrate: defense against invertebrate pests? Trends in Plant Science 11, 424–427.
| Gamma-aminobutyrate: defense against invertebrate pests?Crossref | GoogleScholarGoogle Scholar |
Carvalho GRd, Polachini TC, Darros-Barbosa R, Bon J, Telis-Romero J (2018) Effect of intermittent high-intensity sonication and temperature on barley steeping for malt production. Journal of Cereal Science 82, 138–145.
| Effect of intermittent high-intensity sonication and temperature on barley steeping for malt production.Crossref | GoogleScholarGoogle Scholar |
Chen G, Wang Q, Liu Y, Li Y, Cui J, Liu Y, Liu H, Zhang Y (2012) Modelling analysis for enhancing seed vigour of switchgrass (Panicum virgatum L.) using an ultrasonic technique. Biomass and Bioenergy 47, 426–435.
| Modelling analysis for enhancing seed vigour of switchgrass (Panicum virgatum L.) using an ultrasonic technique.Crossref | GoogleScholarGoogle Scholar |
Che-Othman MH, Jacoby RP, Millar AH, Taylor NL (2020) Wheat mitochondrial respiration shifts from the tricarboxylic acid cycle to the GABA shunt under salt stress. New Phytologist 225, 1166–1180.
| Wheat mitochondrial respiration shifts from the tricarboxylic acid cycle to the GABA shunt under salt stress.Crossref | GoogleScholarGoogle Scholar |
Chou Y-J, Cheng K-C, Hsu F-C, Wu JS-B, Ting Y (2021) Producing high quality mung bean sprout using atmospheric cold plasma treatment: better physical appearance and higher γ-aminobutyric acid (GABA) content. Journal of the Science of Food and Agriculture 101, 6463–6471.
| Producing high quality mung bean sprout using atmospheric cold plasma treatment: better physical appearance and higher γ-aminobutyric acid (GABA) content.Crossref | GoogleScholarGoogle Scholar |
Dastanpoor N, Fahimi H, Shariati M, Davazdahemami S, Hashemi SMM (2013) Effects of hydropriming on seed germination and seedling growth in sage (Salvia officinalis L.). African Journal of Biotechnology 12, 1223–1228.
| Effects of hydropriming on seed germination and seedling growth in sage (Salvia officinalis L.).Crossref | GoogleScholarGoogle Scholar |
Delcour JA, Joye IJ, Pareyt B, Wilderjans E, Brijs K, Lagrain B (2012) Wheat gluten functionality as a quality determinant in cereal-based food products. Annual Review of Food Science and Technology 3, 469–492.
| Wheat gluten functionality as a quality determinant in cereal-based food products.Crossref | GoogleScholarGoogle Scholar |
Ding J, Hou GG, Nemzer BV, Xiong S, Dubat A, Feng H (2018a) Effects of controlled germination on selected physicochemical and functional properties of whole-wheat flour and enhanced γ-aminobutyric acid accumulation by ultrasonication. Food Chemistry 243, 214–221.
| Effects of controlled germination on selected physicochemical and functional properties of whole-wheat flour and enhanced γ-aminobutyric acid accumulation by ultrasonication.Crossref | GoogleScholarGoogle Scholar |
Ding J, Ulanov AV, Dong M, Yang T, Nemzer BV, Xiong S, Zhao S, Feng H (2018b) Enhancement of gama-aminobutyric acid (GABA) and other health-related metabolites in germinated red rice (Oryza sativa L.) by ultrasonication. Ultrasonics Sonochemistry 40, 791–797.
| Enhancement of gama-aminobutyric acid (GABA) and other health-related metabolites in germinated red rice (Oryza sativa L.) by ultrasonication.Crossref | GoogleScholarGoogle Scholar |
Ding J, Johnson J, Chu YF, Feng H (2019) Enhancement of γ-aminobutyric acid, avenanthramides, and other health-promoting metabolites in germinating oats (Avena sativa L.) treated with and without power ultrasound. Food Chemistry 283, 239–247.
| Enhancement of γ-aminobutyric acid, avenanthramides, and other health-promoting metabolites in germinating oats (Avena sativa L.) treated with and without power ultrasound.Crossref | GoogleScholarGoogle Scholar |
Fait A, Fromm H, Walter D, Galili G, Fernie AR (2008) Highway or byway: the metabolic role of the GABA shunt in plants. Trends in Plant Science 13, 14–19.
| Highway or byway: the metabolic role of the GABA shunt in plants.Crossref | GoogleScholarGoogle Scholar |
Feizi H, Javedanipoor E (2021) Role of Spermidine and γ-Aminobutyric Acid and hydro priming on alleviation of salinity effect in germination and growth parameters of cucumber (Cucumis sativus L. cv. Beit Alpha) seed. Iranian Journal of Seed Science and Technology 10, 103–118.
| Role of Spermidine and γ-Aminobutyric Acid and hydro priming on alleviation of salinity effect in germination and growth parameters of cucumber (Cucumis sativus L. cv. Beit Alpha) seed.Crossref | GoogleScholarGoogle Scholar |
Feng H, Yang W (2011) Ultrasonic processing. In ‘Nonthermal processing technologies for food.’ (Eds. HQ Zhang, GV Barbosa-Cánovas, VM Balasubramaniam, CP Dunne, DF Farkas, JTC Yuan) pp. 135–154. (Wiley-Blackwell and IFT Press: UK)
Forti C, Shankar A, Singh A, Balestrazzi A, Prasad V, Macovei A (2020) Hydropriming and biopriming improve Medicago truncatula seed germination and upregulate DNA repair and antioxidant genes. Genes 11, 242
| Hydropriming and biopriming improve Medicago truncatula seed germination and upregulate DNA repair and antioxidant genes.Crossref | GoogleScholarGoogle Scholar |
Goussous SJ, Samarah NH, Alqudah AM, Othman MO (2010) Enhancing seed germination of four crop species using an ultrasonic technique. Experimental Agriculture 46, 231–242.
| Enhancing seed germination of four crop species using an ultrasonic technique.Crossref | GoogleScholarGoogle Scholar |
Guo Y, Chen H, Song Y, Gu Z (2011) Effects of soaking and aeration treatment on γ-aminobutyric acid accumulation in germinated soybean (Glycine max L.). European Food Research and Technology 232, 787–795.
| Effects of soaking and aeration treatment on γ-aminobutyric acid accumulation in germinated soybean (Glycine max L.).Crossref | GoogleScholarGoogle Scholar |
Guo Y, Wu B, Guo X, Liu D, Wu P, Ma H, Pan Z (2021) Ultrasonication and thermosonication blanching treatments of carrot at varying frequencies: effects on peroxidase inactivation mechanisms and quality characterization evaluation. Food Chemistry 343, 128524
| Ultrasonication and thermosonication blanching treatments of carrot at varying frequencies: effects on peroxidase inactivation mechanisms and quality characterization evaluation.Crossref | GoogleScholarGoogle Scholar |
Hao J, Wu T, Li H, Wang W, Liu H (2016) Dual effects of slightly acidic electrolyzed water (SAEW) treatment on the accumulation of γ-aminobutyric acid (GABA) and rutin in germinated buckwheat. Food Chemistry 201, 87–93.
| Dual effects of slightly acidic electrolyzed water (SAEW) treatment on the accumulation of γ-aminobutyric acid (GABA) and rutin in germinated buckwheat.Crossref | GoogleScholarGoogle Scholar |
Hasan M, Bashir T, Bae H (2017) Use of ultrasonication technology for the increased production of plant secondary metabolites. Molecules 22, 1046
| Use of ultrasonication technology for the increased production of plant secondary metabolites.Crossref | GoogleScholarGoogle Scholar |
Ji D, Ma H, Chen X (2021) Ultrasonication increases γ-aminobutyric acid accumulation in coffee leaves and affects total phenolic content and angiotensin-converting enzyme inhibitory activity. Journal of Food Processing and Preservation 45, e15777
| Ultrasonication increases γ-aminobutyric acid accumulation in coffee leaves and affects total phenolic content and angiotensin-converting enzyme inhibitory activity.Crossref | GoogleScholarGoogle Scholar |
Jiang Q, Zhang M, Xu B (2020) Application of ultrasonic technology in postharvested fruits and vegetables storage: a review. Ultrasonics Sonochemistry 69, 105261
| Application of ultrasonic technology in postharvested fruits and vegetables storage: a review.Crossref | GoogleScholarGoogle Scholar |
Kaspal M, Kanapaddalagamage MH, Ramesh SA (2021) Emerging roles of γ Aminobutyric Acid (GABA) gated channels in plant stress tolerance. Plants 10, 2178
| Emerging roles of γ Aminobutyric Acid (GABA) gated channels in plant stress tolerance.Crossref | GoogleScholarGoogle Scholar |
Kinnersley AM, Turano FJ (2000) Gamma aminobutyric acid (GABA) and plant responses to stress. Critical Reviews in Plant Sciences 19, 479–509.
| Gamma aminobutyric acid (GABA) and plant responses to stress.Crossref | GoogleScholarGoogle Scholar |
Lahijanian S, Nazari M (2017) Increasing germination speed of common bean (Phaseolus vulgaris) seeds by ultrasound treatments. Seed Technology 38, 49–55.
Li J, Yin LY, Jongsma MA, Wang CY (2011) Effects of light, hydropriming and abiotic stress on seed germination, and shoot and root growth of pyrethrum (Tanacetum cinerariifolium). Industrial Crops and Products 34, 1543–1549.
| Effects of light, hydropriming and abiotic stress on seed germination, and shoot and root growth of pyrethrum (Tanacetum cinerariifolium).Crossref | GoogleScholarGoogle Scholar |
Li R, Li Z-J, Wu N-N, Tan B (2022) Effect of pre-treatment on the functional properties of germinated whole grains: a review. Cereal Chemistry 99, 253–269.
| Effect of pre-treatment on the functional properties of germinated whole grains: a review.Crossref | GoogleScholarGoogle Scholar |
Lindsey BE, Rivero L, Calhoun CS, Grotewold E, Brkljacic J (2017) Standardized method for high-throughput sterilization of Arabidopsis seeds. JoVE (Journal of Visualized Experiments) e56587
| Standardized method for high-throughput sterilization of Arabidopsis seeds.Crossref | GoogleScholarGoogle Scholar |
Liu J, Wang Q, Karagić Đ, Liu X, Cui J, Gui J, Gu M, Gao W (2016) Effects of ultrasonication on increased germination and improved seedling growth of aged grass seeds of tall fescue and Russian wildrye. Scientific Reports 6, 22403
| Effects of ultrasonication on increased germination and improved seedling growth of aged grass seeds of tall fescue and Russian wildrye.Crossref | GoogleScholarGoogle Scholar |
Liu H, Li Z, Zhang X, Liu Y, Hu J, Yang C, Zhao X (2021) The effects of ultrasound on the growth, nutritional quality and microbiological quality of sprouts. Trends in Food Science & Technology 111, 292–300.
| The effects of ultrasound on the growth, nutritional quality and microbiological quality of sprouts.Crossref | GoogleScholarGoogle Scholar |
López-Ribera I, Vicient CM (2017) Use of ultrasonication to increase germination rates of Arabidopsis seeds. Plant Methods 13, 31
| Use of ultrasonication to increase germination rates of Arabidopsis seeds.Crossref | GoogleScholarGoogle Scholar |
Machikowa T, Kulrattanarak T, Wonprasaid S (2013) Effects of ultrasonic treatment on germination of synthetic sunflower seeds. In ‘Proceedings of world academy of science, engineering and technology.’ (World Academy of Science, Engineering and Technology (WASET))
Maresca D, Lakshmanan A, Abedi M, Bar-Zion A, Farhadi A, Lu GJ, Szablowski JO, Wu D, Yoo S, Shapiro MG (2018) Biomolecular ultrasound and sonogenetics. Annual Review of Chemical and Biomolecular Engineering 9, 229–252.
| Biomolecular ultrasound and sonogenetics.Crossref | GoogleScholarGoogle Scholar |
Mayer RR, Cherry JH, Rhodes D (1990) Effects of heat shock on amino acid metabolism of cowpea cells. Plant Physiology 94, 796–810.
| Effects of heat shock on amino acid metabolism of cowpea cells.Crossref | GoogleScholarGoogle Scholar |
Mazzucotelli E, Tartari A, Cattivelli L, Forlani G (2006) Metabolism of γ-aminobutyric acid during cold acclimation and freezing and its relationship to frost tolerance in barley and wheat. Journal of Experimental Botany 57, 3755–3766.
| Metabolism of γ-aminobutyric acid during cold acclimation and freezing and its relationship to frost tolerance in barley and wheat.Crossref | GoogleScholarGoogle Scholar |
Miano AC, Forti VA, Abud HF, Gomes-Junior FG, Cicero SM, Augusto PED (2015) Effect of ultrasound technology on barley seed germination and vigour. Seed Science and Technology 43, 297–302.
| Effect of ultrasound technology on barley seed germination and vigour.Crossref | GoogleScholarGoogle Scholar |
Miano AC, Rojas ML, Augusto PED (2019) Structural changes caused by ultrasound pretreatment: direct and indirect demonstration in potato cylinders. Ultrasonics Sonochemistry 52, 176–183.
| Structural changes caused by ultrasound pretreatment: direct and indirect demonstration in potato cylinders.Crossref | GoogleScholarGoogle Scholar |
Michaeli S, Fromm H (2015) Closing the loop on the GABA shunt in plants: are GABA metabolism and signaling entwined? Frontiers in Plant Science 6, 419
| Closing the loop on the GABA shunt in plants: are GABA metabolism and signaling entwined?Crossref | GoogleScholarGoogle Scholar |
Mirabella R, Rauwerda H, Struys EA, Jakobs C, Triantaphylidès C, Haring MA, Schuurink RC (2008) The Arabidopsis her1 mutant implicates GABA in E-2-hexenal responsiveness. The Plant Journal 53, 197–213.
| The Arabidopsis her1 mutant implicates GABA in E-2-hexenal responsiveness.Crossref | GoogleScholarGoogle Scholar |
Mohammed MEA, Alhajhoj MR (2019) Importance and applications of ultrasonic technology to improve food quality. In ‘Food processing’. (Eds RA Marc, AV Díaz, GDP Izquierdo) pp. 141–153. (IntechOpen)
Molina-Rueda JJ, Pascual MB, Cánovas FM, Gallardo F (2010) Characterization and developmental expression of a glutamate decarboxylase from maritime pine. Planta 232, 1471–1483.
| Characterization and developmental expression of a glutamate decarboxylase from maritime pine.Crossref | GoogleScholarGoogle Scholar |
Naumenko N, Potoroko I, Kalinina I (2022) Stimulation of antioxidant activity and γ-aminobutyric acid synthesis in germinated wheat grain Triticum aestivum L. by ultrasound: increasing the nutritional value of the product. Ultrasonics Sonochemistry 86, 106000
| Stimulation of antioxidant activity and γ-aminobutyric acid synthesis in germinated wheat grain Triticum aestivum L. by ultrasound: increasing the nutritional value of the product.Crossref | GoogleScholarGoogle Scholar |
Oliveira FIP, Gallão MI, Rodrigues S, Fernandes FAN (2011) Dehydration of Malay apple (Syzygium malaccense L.) using ultrasound as pre-treatment. Food and Bioprocess Technology 4, 610–615.
| Dehydration of Malay apple (Syzygium malaccense L.) using ultrasound as pre-treatment.Crossref | GoogleScholarGoogle Scholar |
Pascual MB, Molina-Rueda JJ, Canovas FM, Gallardo F (2008) Spatial distribution of cytosolic NADP+-isocitrate dehydrogenase in pine embryos and seedlings. Tree Physiology 28, 1773–1782.
| Spatial distribution of cytosolic NADP+-isocitrate dehydrogenase in pine embryos and seedlings.Crossref | GoogleScholarGoogle Scholar |
Patel RV, Pandya KY, Jasrai RT, Brahmbhatt N (2017) Effect of hydropriming and biopriming on seed germination of Brinjal and Tomato seed. Research Journal of Agriculture and Forest 5, 1–14.
Rajjou L, Debeaujon I (2008) Seed longevity: survival and maintenance of high germination ability of dry seeds. Comptes Rendus Biologies 331, 796–805.
| Seed longevity: survival and maintenance of high germination ability of dry seeds.Crossref | GoogleScholarGoogle Scholar |
Ramesh SA, Tyerman SD, Xu B, Bose J, Kaur S, Conn V, Domingos P, Ullah S, Wege S, Shabala S, Feijó JA, Ryan PR, Gilliham M (2015) GABA signalling modulates plant growth by directly regulating the activity of plant-specific anion transporters. Nature Communications 6, 7879
| GABA signalling modulates plant growth by directly regulating the activity of plant-specific anion transporters.Crossref | GoogleScholarGoogle Scholar |
Ramteke AA, Meshram UP, Yaul AR (2015) Effect of ultrasonic waves on seed germination of Lycopersicon esculentum and Anethum graveolens. International Journal of Chemical and Physical Sciences 4, 333–336.
Renault H, El Amrani A, Berger A, Mouille G, Soubigou-Taconnat L, Bouchereau A, Deleu C (2013) γ-Aminobutyric acid transaminase deficiency impairs central carbon metabolism and leads to cell wall defects during salt stress in Arabidopsis roots. Plant, Cell & Environment 36, 1009–1018.
| γ-Aminobutyric acid transaminase deficiency impairs central carbon metabolism and leads to cell wall defects during salt stress in Arabidopsis roots.Crossref | GoogleScholarGoogle Scholar |
Scott-Taggart CP, Van Cauwenberghe OR, McLean MD, Shelp BJ (1999) Regulation of Γ-aminobutyric acid synthesis in situ by glutamate availability. Physiologia Plantarum 106, 363–369.
| Regulation of Γ-aminobutyric acid synthesis in situ by glutamate availability.Crossref | GoogleScholarGoogle Scholar |
Sharafi Y, Aghdam MS, Luo Z, Jannatizadeh A, Razavi F, Fard JR, Farmani B (2019) Melatonin treatment promotes endogenous melatonin accumulation and triggers GABA shunt pathway activity in tomato fruits during cold storage. Scientia Horticulturae 254, 222–227.
| Melatonin treatment promotes endogenous melatonin accumulation and triggers GABA shunt pathway activity in tomato fruits during cold storage.Crossref | GoogleScholarGoogle Scholar |
Sharma AD, Rathore SVS, Srinivasan K, Tyagi RK (2014) Comparison of various seed priming methods for seed germination, seedling vigour and fruit yield in okra (Abelmoschus esculentus L. Moench). Scientia Horticulturae 165, 75–81.
| Comparison of various seed priming methods for seed germination, seedling vigour and fruit yield in okra (Abelmoschus esculentus L. Moench).Crossref | GoogleScholarGoogle Scholar |
Shekarl F, Mustafavi S-H, Abbasi A (2015) Sonication of seeds increase germination performance of sesame under low temperature stress. Acta Agriculturae Slovenica 105, 203–212.
Shelp BJ, Bown AW, McLean MD (1999) Metabolism and functions of gamma-aminobutyric acid. Trends in Plant Science 4, 446–452.
| Metabolism and functions of gamma-aminobutyric acid.Crossref | GoogleScholarGoogle Scholar |
Shewry PR, Hey SJ (2015) The contribution of wheat to human diet and health. Food and Energy Security 4, 178–202.
| The contribution of wheat to human diet and health.Crossref | GoogleScholarGoogle Scholar |
Sita K, Kumar V (2020) Role of Gamma Amino Butyric Acid (GABA) against abiotic stress tolerance in legumes: a review. Plant Physiology Reports 25, 654–663.
| Role of Gamma Amino Butyric Acid (GABA) against abiotic stress tolerance in legumes: a review.Crossref | GoogleScholarGoogle Scholar |
Srivastava AK, Lokhande VH, Patade VY, Suprasanna P, Sjahril R, D’Souza SF (2010) Comparative evaluation of hydro-, chemo-, and hormonal-priming methods for imparting salt and PEG stress tolerance in Indian mustard (Brassica juncea L.). Acta Physiologiae Plantarum 32, 1135–1144.
| Comparative evaluation of hydro-, chemo-, and hormonal-priming methods for imparting salt and PEG stress tolerance in Indian mustard (Brassica juncea L.).Crossref | GoogleScholarGoogle Scholar |
Sun Y, Ji D, Ma H, Chen X (2022) Ultrasound accelerated γ-aminobutyric acid accumulation in coffee leaves through influencing the microstructure, enzyme activity, and metabolites. Food Chemistry 385, 132646
| Ultrasound accelerated γ-aminobutyric acid accumulation in coffee leaves through influencing the microstructure, enzyme activity, and metabolites.Crossref | GoogleScholarGoogle Scholar |
Uzma Jalil S, Khan MIR, Ansari MI (2019) Role of GABA transaminase in the regulation of development and senescence in Arabidopsis thaliana. Current Plant Biology 19, 100119
| Role of GABA transaminase in the regulation of development and senescence in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |
Vilkhu K, Mawson R, Simons L, Bates D (2008) Applications and opportunities for ultrasound assisted extraction in the food industry – a review. Innovative Food Science & Emerging Technologies 9, 161–169.
| Applications and opportunities for ultrasound assisted extraction in the food industry – a review.Crossref | GoogleScholarGoogle Scholar |
Wang Q, Chen G, Yersaiyiti H, Liu Y, Cui J, Wu C, Zhang Y, He X (2012) Modeling analysis on germination and seedling growth using ultrasound seed pretreatment in switchgrass. PLoS ONE 7, e47204
| Modeling analysis on germination and seedling growth using ultrasound seed pretreatment in switchgrass.Crossref | GoogleScholarGoogle Scholar |
Wang H, Xu K, Ma Y, Liang Y, Zhang H, Chen L (2020a) Impact of ultrasonication on the aggregation structure and physicochemical characteristics of sweet potato starch. Ultrasonics Sonochemistry 63, 104868
| Impact of ultrasonication on the aggregation structure and physicochemical characteristics of sweet potato starch.Crossref | GoogleScholarGoogle Scholar |
Wang J, Bian Z, Wang S, Zhang L (2020b) Effects of ultrasonic waves, microwaves, and thermal stress treatment on the germination of Tartary buckwheat seeds. Journal of Food Process Engineering 43, e13494
| Effects of ultrasonic waves, microwaves, and thermal stress treatment on the germination of Tartary buckwheat seeds.Crossref | GoogleScholarGoogle Scholar |
Xia Q, Tao H, Li Y, Pan D, Cao J, Liu L, Zhou X, Barba FJ (2020) Characterizing physicochemical, nutritional and quality attributes of wholegrain Oryza sativa L. subjected to high intensity ultrasound-stimulated pre-germination. Food Control 108, 106827
| Characterizing physicochemical, nutritional and quality attributes of wholegrain Oryza sativa L. subjected to high intensity ultrasound-stimulated pre-germination.Crossref | GoogleScholarGoogle Scholar |
Yang H, Gao J, Yang A, Chen H (2015) The ultrasound-treated soybean seeds improve edibility and nutritional quality of soybean sprouts. Food Research International 77, 704–710.
| The ultrasound-treated soybean seeds improve edibility and nutritional quality of soybean sprouts.Crossref | GoogleScholarGoogle Scholar |
Zhang G, Bown AW (1997) The rapid determination of γ-aminobutyric acid. Phytochemistry 44, 1007–1009.
| The rapid determination of γ-aminobutyric acid.Crossref | GoogleScholarGoogle Scholar |
Zhang Y, Zhao T, Shen J, Wang X (2016) Study on effect of ultrasonic treatment on GABA accumulation and antioxidant capacity in germinated brown rice. Science and Technology of Food Industry 37, 130–133.
