Abstract
Abiotic stress, especially drought, is one of the principal constraints of crop productivity and is expected to worsen with climate change in the near future. This warrants the development of new technologies to decrease the impact of drought on crop productivity. Biostimulants made from seaweed extracts are one of the relatively new biological based inputs that can help mitigate the negative effects of abiotic stress on plants by enhancing growth, development, and stress tolerance. The current study evaluated the impact of Ascophyllum nodosum extract (SWE) on tomato plants grown under different levels of water stress. Greenhouse studies were conducted to assess the effect of foliar spray (0.5%) of the extract on stomatal conductance, photosynthesis, chlorophyll content, and biomass, for plants grown at moisture levels of 100%, 50%, and 25% of field capacity. A field study was also conducted with irrigation maintained at 100% and 25% (irrigation capacity). Additionally, the expression levels of marker genes associated with drought tolerance were evaluated using qPCR studies for Metacaspase 1 (LeMCA1), Non-specific lipid-transfer protein 2 (Itpg2), Late embryogenesis abundant protein (LEA) and Delta 1-pyrroline-5- carboxylate synthetase (P5CS) genes. Assays were also conducted on plants for osmolyte content including proline and glycine betaine. Furthermore, the activities of antioxidant defense enzymes were evaluated for superoxide dismutase (SOD), catalase (CAT), peroxidase (POX), ascorbate peroxidase (APX) and guaiacol peroxidase (GPX). The results of the greenhouse study indicated higher stomatal conductance, chlorophyll content, and Fv/Fm in stressed plants that were foliar sprayed with the A. nodosum extract. Seaweed extract-treated plants under water-stress conditions also had significantly greater shoot and root dry weights compared to control plants. The relative expression levels of the marker genes were also significantly increased in SWE sprayed plants compared to control plants along with increased antioxidant enzymes activities and osmolyte contents. The field experiments revealed that seaweed extract-treated plants had significantly higher plant height and total yield under reduced irrigation compared to control plants, although both parameters remained lower than those seen under full irrigation. This study has produced encouraging findings on the application of SWE in crop systems, indicating that it may have a positive role in mitigating the effects of drought stress.
Similar content being viewed by others
Data availability
The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.
References
Ahmed M, Ullah H, Attia A, Tisarum R, Cha-um S, Datta A (2022) Interactiveeffects of Ascophyllum nodosum seaweed extract and silicon on growth, fruit yield and quality, and water productivity of tomato under water stress. Silicon 15:2263–2278
Ali N, Farrell A, Ramsubhag A, Jayaraj J (2016) The effect of Ascophyllum nodosum extract on the growth, yield and fruit quality of tomato grown under tropical conditions. J Appl Phycol 28:1353–1362
Ali O, Ramsubhag A, Jayaraj J (2019) Biostimulatory activities of Ascophyllum nodosum extract in tomato and sweet pepper crops in a tropical environment. PLoS One 14:140–155
Ali O, Ramsubhag A, Jayaraj J (2021) Biostimulant properties of seaweed extracts in plants: implications towards sustainable crop production. Plants 10:531
Ali J, Jan I, Ullah H, Ahmed N, Alam M, Ullah R, El-Sharnouby M, Kesba H, Shukry M, Sayed S, Nawaz T (2022a) Influence of Ascophyllum nodosum extract foliar spray on the physiological and biochemical attributes of okra under drought stress. Plants 11:790
Ali O, Ramsubhag A, Jr DB, Ramnarine S, Jayaraj J (2022b) Transcriptomic changes induced by applications of a commercial extract of Ascophyllum nodosum on tomato plants. Sci Rep 12:8042
Almaroai YA, Eissa MA (2020) Role of marine algae extracts in water stress resistance of onion under semiarid conditions. J Soil Sci Plant Nutr 20:1092–1101
Ashraf M, Foolad MR (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 59:206–216
Baker NR (2008) Chlorophyll fluorescence: A probe of photosynthesis in vivo. Annu Rev Plant Biol 59:89–113
Bartels D, Sunkar R (2005) Drought and salt tolerance in plants. CRC Crit Rev Plant Sc 24:23–58
Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207
Beyer WF, Fridovich I (1987) Assaying for superoxide dismutase activity: Some large consequences of minor changes in conditions. Ann Biochem 161:559–566
Blunden G, Jenkins T, Liu YW (1996) Enhanced leaf chlorophyll levels in plants treated with seaweed extract. J Appl Phycol 8:535–543
Boutraa T, Sanders FE (2001) Influence of water stress on grain yield and vegetative growth of two cultivars of bean (Phaseolus vulgaris L.). J Agron Crop Sci 187:251–257
Bray EA (2002) Abscisic acid regulation of gene expression during water-deficit stress in the era of the Arabidopsis genome. Plant Cell Environ 25:153–161
Campobenedetto C, Agliassa C, Mannino G, Vigliante I, Contartese V, Secchi F, Bertea CM (2021) A biostimulant based on seaweed (Ascophyllum nodosum and Laminaria digitata) and yeast extracts mitigateswater stress effects on tomato (Solanum lycopersicum L.). Agriculture 11:557
Cocetta G, Landoni M, Pilu R, Repiso C, Nolasco J, Alajarin M, Ugena L, Levy CCB, Scatolino G, Villa D, Ferrante A (2022) Priming treatments with biostimulants to cope the short-term heat stress response: A transcriptomic profile evaluation. Plants 11:1130
Conrath U, Beckers GJM, Flors V, García-Agustín P, Jakab G, Mauch F, Newman MA, Pieterse CMJ, Poinssot B, Pozo MJ, Pugin A, Schaffrath U, Ton J, Wendehenne D, Zimmerli L, Mauch-Mani B (2006) Priming: Getting ready for battle. Mol Plant Microbe Interact 19:1062–1071
Daryanto S, Wang L, Jacinthe PA (2017) Global synthesis of drought effects on cereal, legume, tuber and root crops production: A review. Agric Water Manag 179:18–33
De Saeger J, Van Praet S, Vereecke D, Park J, Jacques S, Han T, Depuydt S (2020) Toward the molecular understanding of the action mechanism of Ascophyllum nodosum extracts on plants. J Appl Phycol 32:573–597
Dogan M, Tipirdamaz R, Demir Y (2010) Effective salt criteria in callus-cultured tomato genotypes. Z Naturforsch C 65C:613–661
Foley SA, Mulloy B, Tuohy MG (2011) An unfractionated fucoidan from Ascophyllum nodosum: Extraction, characterization, and apoptotic effects in vitro. J Nat Prod 74:1851–1861
Foyer CH, Halliwell B (1976) The presence of glutathione and glutathione reductase in chloroplasts: A proposed role in ascorbic acid metabolism. Planta 133:21–25
Frioni T, VanderWeide J, Palliotti A, Tombesi S, Poni S, Sabbatini P (2021) Foliar vs. soil application of Ascophyllum nodosum extracts to improve grapevine water stress tolerance. Sci Hortic (Amsterdam) 277:109807
Fujita Y, Fujita M, Satoh R, Maruyama K, Parvez MM, Seki M, Hiratsu K, Ohme-Takagi M, Shinozaki K, Yamaguchi-Shinozaki K (2005) AREB1 is a transcription activator of novel ABRE-dependent ABA signaling that enhances drought stress tolerance in Arabidopsis. Plant Cell 17:3470–3488
Furuki T, Sakurai M (2016) Group 3 LEA protein model peptides protect enzymes against desiccation stress. Biochim Biophys Acta - Proteins Proteomics 1864:1237–1243
Gangadhar BH, Sajeesh K, Venkatesh J, Baskar V, Abhinandan K, Yu JW, Prasad R, Mishra RK (2016) Enhanced tolerance of transgenic potato plants over-expressing non-specific lipid transfer protein-1 (StnsLTP1) against multiple abiotic stresses. Front Plant Sci 7:1228
Goñi O, Quille P, O’Connell S (2018) Ascophyllum nodosum extract biostimulants and their role in enhancing tolerance to drought stress in tomato plants. Plant Physiol Biochem 126:63–73
Goyal K, Walton LJ, Tunnacliffe A (2005) LEA proteins prevent protein aggregation due to water stress. Biochem J 388:151–157
Grieve CM, Grattan SR (1983) Rapid assay for determination of water soluble quaternary ammonium compounds. Plant Soil 70:303–307
Guillén S, Casas A, Terrazas T, Vega E, Martínez-Palacios A (2013) Differential survival and growth of wild and cultivated seedlings of columnar cacti: Consequences of domestication. Am J Bot 100:2364–2379
Gupta A, Rico-Medina A, Caño-Delgado AI (2020) The physiology of plant responses to drought. Science 368:266–269
Hosseinifard M, Stefaniak S, Javid MG, Soltani E, Wojtyla Ł, Garnczarska M (2022) Contribution of exogenous proline to abiotic stresses tolerance in plants: A review. Int J Mol Sci 23:5186
Huh SU (2022) Evolutionary diversity and function of metacaspases in plants: Similar to but not caspases. Int J Mol Sci 23:4588
Islam MT, Arioli T, Cahill DM (2021) Seaweed extract-stimulated priming in Arabidopsis thaliana and Solanum lycopersicum. Plants 10:2476
Jayaraj J, Wan A, Rahman M, Punja ZK (2008) Seaweed extract reduces foliar fungal diseases on carrot. Crop Prot 27:1360–1366
Jayaraj J, Norrie J, Punja ZK (2011) Commercial extract from the brown seaweed Ascophyllum nodosum reduces fungal diseases in greenhouse cucumber. J Appl Phycol 23:353–361
Jithesh MN, Wally OSD, Manfield I, Critchley AT, Hiltz D, Prithiviraj B (2012) Analysis of seaweed extract-induced transcriptome leads to identification of a negative regulator of salt tolerance in Arabidopsis. HortScience 47:704–709
Kar M, Feierabend J (1984) Metabolism of activated oxygen in detached wheat and rye leaves and its relevance to the initiation of senescence. Planta 160:385–391
Karabal E, Yücel M, Öktem HA (2003) Antioxidant responses of tolerant and sensitive barley cultivars to boron toxicity. Plant Sci 164:925–933
Khan W, Rayirath UP, Subramanian S, Jithesh MN, Rayorath P, Hodges DM, Critchley AT, Craigie JS, Norrie J, Prithiviraj B (2009) Seaweed extracts as biostimulants of plant growth and development. J Plant Growth Regul 45:112–134
Kovacs D, Agoston B, Tompa P (2008) Disordered plant LEA proteins as molecular chaperones. Plant Signal Behav 3:710–713
Kumari S, Sehrawat KD, Phogat D, Sehrawat AR, Chaudhary R, Sushkova SN, Voloshina MS, Rajput VD, Shmaraeva AN, Marc RA, Shende SS (2023) Ascophyllum nodosum (L.) Le Jolis, a pivotal biostimulant toward sustainable agriculture: A comprehensive review. Agriculture 13:1179
Lephatsi MM, Meyer V, Piater LA, Dubery IA, Tugizimana F (2021) Plant responses to abiotic stresses and rhizobacterial biostimulants: Metabolomics and epigenetics perspectives. Metabolites 11:457
Lim J, Lim CW, Lee SC (2018) The pepper late embryogenesis abundant protein, cadil1, positively regulates drought tolerance and aba signaling. Front Plant Sci 9:1301
Liu G, Xu H, Zhang L, Zheng Y (2011) Fe binding properties of two soybean (Glycine max L.) LEA4 proteins associated with antioxidant activity. Plant Cell Physiol 52:994–1002
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408
Lu C, Li Y, Chen A, Li L, Zuo J, Tian H, Luo Y, Zhu B (2010) LeERF1 improves tolerance to drought stress in tomato (Lycopersicon esculentum) and activates downstream stress-responsive genes. Afr J Biotechnol 9:6294–6300
Ma Y, Freitas H, Dias MC (2022) Strategies and prospects for biostimulants to alleviate abiotic stress in plants. Front Plant Sci 13:1024243
Mansori M, Chernane H, Latique S, Benaliat A, Hsissou D, El Kaoua M (2015) Seaweed extract effect on water deficit and antioxidative mechanisms in bean plants (Phaseolus vulgaris L.). J Appl Phycol 27:1689–1698
McNeil SD, Nuccio ML, Hanson AD (1999) Betaines and related osmoprotectants. Targets for metabolic engineering of stress resistance. Plant Physiol 67:45–56
Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681
Nakashima K, Yamaguchi-Shinozaki K, Shinozaki K (2014) The transcriptional regulatory network in the drought response and its crosstalk in abiotic stress responses including drought, cold, and heat. Front Plant Sci 5:170
Nankishore A, Farrell AD (2016) The response of contrasting tomato genotypes to combined heat and drought stress. J Plant Physiol 202:75–82
Ni F-T, Chu L-Y, Shao H-B, Liu Z-H (2009) Gene expression and regulation of higher plants under soil water stress. Curr Genomics 10:269–280
Oguz MC, Aycan M, Oguz E, Poyraz I, Yildiz M (2022) Drought stress tolerance in plants: interplay of molecular, biochemical and physiological responses in important development stages. Physiologia 2:180–197
Patel JS, Selvaraj V, More P, Bahmani R, Borza T, Prithiviraj B (2023) A plant biostimulant from Ascophyllum nodosum potentiates plant growth promotion and stress protection activity of Pseudomonas protegens CHA0. Plants 12:1208
Rai N, Rai SP, Sarma BK (2021) Prospects for abiotic stress tolerance in crops utilizing phyto- and bio-stimulants. Front Sustain Food Syst 5:754853
Rasul F, Gupta S, Olas JJ, Gechev T, Sujeeth N, Mueller-Roeber B (2021) Priming with a seaweed extract strongly improves drought tolerance in Arabidopsis. Int J Mol Sci 22:1469
Seleiman MF, Al-Suhaibani N, Ali N, Akmal M, Alotaibi M, Refay Y, Dindaroglu T, Abdul-Wajid HH, Battaglia ML (2021) Drought stress impacts on plants and different approaches to alleviate its adverse effects. Plants 10:259
Shukla PS, Mantin EG, Adil M, Bajpai S, Critchley AT, Prithiviraj B (2019) Ascophyllum nodosum-based biostimulants: Sustainable applications in agriculture for the stimulation of plant growth, stress tolerance, and disease management. Front Plant Sci 10:401–415
Smirnoff N (2005) Ascorbate, tocopherol and carotenoids: metabolism, pathway engineering and functions. In: Smirnoff N (ed) Antioxidants and reactive oxygen species in plants. Blackwell Publishing, Oxford, pp 53–86
Smith M (2000) The application of climatic data for planning and management of sustainable rainfed and irrigated crop production. Agric For Meteorol 103:99–108
Tolleter D, Hincha DK, Macherel D (2010) A mitochondrial late embryogenesis abundant protein stabilizes model membranes in the dry state. Biochim Biophys Acta - Biomembr 1798:1926–1933
Tombesi S, Frioni T, Sabbatini P, Poni S, Palliotti A (2021) Ascophyllum nodosum extract improves leaf thermoregulation by reducing stomatal sensitivity to VPD in Vitis vinifera L. J Appl Phycol 33:1293–1304
Van Doorn WG, Woltering EJ (2004) Senescence and programmed cell death: Substance or semantics? J Exp Bot 55:2147–2153
Van Oosten MJ, Pepe O, De Pascale S, Silletti S, Maggio A (2017) The role of biostimulants and bioeffectors as alleviators of abiotic stress in crop plants. Chem Biol Technol Agric 4:5
Wang W, Vinocur B, Altman A (2003) Plant responses to drought, salinity and extreme temperatures: Towards genetic engineering for stress tolerance. Planta 218:1–14
Yoshida T, Fujita Y, Sayama H, Kidokoro S, Maruyama K, Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K (2010) AREB1, AREB2, and ABF3 are master transcription factors that cooperatively regulate ABRE-dependent ABA signaling involved in drought stress tolerance and require ABA for full activation. Plant J 61:672–685
Zheng L, Dang Z, Li H, Zhang H, Wu S, Wang Y (2014) Isolation and characterization of a Δ1-pyrroline-5-carboxylate synthetase (NtP5CS) from Nitraria tangutorum Bobr. and functional comparison with its Arabidopsis homologue. Mol Biol Rep 41:563–572
Zhou R, Yu X, Ottosen CO, Rosenqvist E, Zhao L, Wang Y, Yu W, Zhao T, Wu Z (2017) Drought stress had a predominant effect over heat stress on three tomato cultivars subjected to combined stress. BMC Plant Biol 17:24
Zhu J, Tremblay N, Liang Y (2012) Comparing SPAD and atLEAF values for chlorophyll assessment in crop species. Can J Soil Sci 92
Acknowledgements
The authors would like to thank Mr. Alfred Kondayya for facilitating the field experiment.
Funding
No funding was received for conducting this study.
Author information
Authors and Affiliations
Contributions
Omar Ali: Conducting greenhouse, field, and molecular experiments, Data collection, Statistical analysis, Writing-Original manuscript draft, Carrying out corrections.
Adesh Ramsubhag: Data Validation, Research supervision, Reviewing and Editing of the manuscript.
Aidan D. Farrell: Greenhouse experimentation, Data collection and analysis, Reviewing and Editing of the manuscript.
Jayaraj Jayaraman: Conceptualization, Funding, Research supervision, Data Validation, Reviewing and Editing and Correction of the manuscript.
All authors reviewed the manuscript.
Corresponding author
Ethics declarations
Competing interests
The authors declare that they have no competing interests.
Additional information
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Ali, O., Farrell, A.D., Ramsubhag, A. et al. Beneficial effects of an Ascophyllum nodosum extract on tomato (Solanum lycopersicum L.) during water stress. J Appl Phycol 36, 385–397 (2024). https://doi.org/10.1007/s10811-023-03156-z
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10811-023-03156-z