Abstract
Recent evidence suggests that seaweed extracts can protect plants against microbial disease by upregulating the host’s immune system. However, if this upregulation comes at a cost to host vegetative and reproductive growth it will make the use of seaweed extracts in crop disease protection less attractive. In a series of experiments, using Arabidopsis thaliana infected by white rust (Albugo sp.) and treated with crude extracts of Ulva lactuca and Saccharina latissima, we test the hypothesis that a growth-immunity trade-off exists. We include temporal samples of the two seaweed species because the composition of bioactive molecules in them is known to vary over the year. Our results confirm that extracts of both species have the potential to protect against disease, but that both the timing of seaweed sampling and extraction procedures can introduce considerable variation to this effect. Importantly, these seaweed treatments were also associated with reduced host vegetative mass, though treatment with S. latissima could compensate for this as it also stimulated increased seed mass. We conclude that the effects of crude seaweed extracts from U. lactuca and S. latissima on plant fitness are not immediately predictable, and benefits in terms of disease protection may come with costs.
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References
Aarssen LW, Clauss MJ (1992) Genotypic variation in fecundity allocation in Arabidopsis thaliana. J Ecol 80:109–114
Aarssen LW, Jordan CY (2001) Between-species patterns of covariation in plant size, seed size and fecundity in monocarpic herbs. Ecoscience 8:471–477
Abkhoo J, Sabbagh SK (2016) Control of Phytophthora melonis damping-off, induction of defense responses, and gene expression of cucumber treated with commercial extract from Ascophyllum nodosum. J Appl Phycol 28:1333–1342
Abouraïcha E, El Alaoui-Talibi Z, El Boutachfaiti R, Petit E, Courtois B, Courtois J, El Modafar C (2015) Induction of natural defense and protection against Penicillium expansum and Botrytis cinerea in apple fruit in response to bioelicitors isolated from green algae. Sci Hortic 181:121–128
Akiyama R, Aagren J (2012) Magnitude and timing of leaf damage affect seed production in a natural population of Arabidopsis thaliana (Brassicaceae). PLoS One 7:e30015
Ali N, Ramkissoon A, Ramsubhag A, Jayaraj J (2016) Ascophyllum extract application causes reduction of disease levels in field tomatoes grown in a tropical environment. Crop Prot 83:67–75
Blunden G, Challen SB, Woods DL (1968) Seaweed extracts as fertilisers. J Sci Food Agr 19:289–293
Bruhn A, Janicek T, Manns D, Nielsen MM, Balsby TJS, Meyer AS, Rasmussen MB, Hou X, Saake B, Göke C, Bjerre AB (2017) Crude fucoidan content in two North Atlantic kelp species, Saccharina latissima and Laminaria digitata - seasonal variation and impact of environmental factors. J Appl Phycol 29:3121–3137
Burketova L, Trda L, Ott PG, Valentova O (2015) Bio-based resistance inducers for sustainable plant protection against pathogens. Biotechnol Adv 33:994–1004
Cluzet S, Torregrosa C, Jacquet C, Lafitte C, Fournier J, Mercier L, Salamagne S, Briand X, Esquerre-Tugaye MT, Dumas B (2004) Gene expression profiling and protection of Medicago truncatula against a fungal infection in response to an elicitor from green algae Ulva spp. Plant Cell Environ 27:917–928
de Borba MC, de Freitas MB, Stadnik MJ (2019) Ulvan enhances seedling emergence and reduces Fusarium wilt severity in common bean (Phaseolus vulgaris L.). Crop Prot 118:66–71
de Borba MC, Velho AC, Maia-Grondard A, Baltenweck R, Magnin-Robert M, Randoux B, Holvoet M, Hilbert JL, Flahaut C, Reignault P, Hugueney P, Stadnik MJ, Siah A (2021) The algal polysaccharide ulvan induces resistance in wheat against Zymoseptoria tritici without major alteration of leaf metabolome. Front Plant Sci 12:703712
de Freitas MB, Ferreira LG, Hawerroth C, Duarte MER, Noseda MD, Stadnik MJ (2015) Ulvans induce resistance against plant pathogenic fungi independently of their sulfation degree. Carbohyd Polym 133:384–390
Delgado DZ, de Freitas MB, Stadnik MJ (2013) Effectiveness of saccharin and ulvan as resistance inducers against rust and angular leaf spot in bean plants (Phaseolus vulgaris). Crop Prot 47:67–73
Ding P, Ding Y (2020) Stories of salicylic acid: A plant defense hormone. Trends Plant Sci 25:549–565
Dookie M, Ali O, Ramsubhag A, Jayaraman J (2021) Flowering gene regulation in tomato plants treated with brown seaweed extracts. Sci Hortic 276:109715
El Modafar C, Elgadda M, El Boutachfaiti R, Abouraicha E, Zehhar N, Petit E, El Alaoui-Talibi Z, Courtois B, Courtois J (2012) Induction of natural defence accompanied by salicylic acid-dependant systemic acquired resistance in tomato seedlings in response to bioelicitors isolated from green algae. Sci Hortic 138:55–63
Esserti S, Smaili A, Makroum K, Belfaiza M, Rifai LA, Koussa T, Kasmi I, Faize M (2018) Priming of Nicotiana benthamiana antioxidant defences using brown seaweed extracts. J Phytopathol 166:86–94
Esserti S, Smaili A, Rifai LA, Koussa T, Makroum K, Belfaiza M, Kabil EM, Faize L, Burgos L, Alburquerque N, Faize M (2017) Protective effect of three brown seaweed extracts against fungal and bacterial diseases of tomato. J Appl Phycol 29:1081–1093
Farag SMA, Elhalag KMA, Hagag MH, Khairy ASM, Ibrahim HM, Saker MT, Messiha NAS (2017) Potato bacterial wilt suppression and plant health improvement after application of different antioxidants. J Phytopathol 165:522–537
Gauthier A, Trouvelot S, Kelloniemi J, Frettinger P, Wendehenne D, Daire X, Joubert JM, Ferrarini A, Delledonne M, Flors V, Poinssot B (2014) The sulfated laminarin triggers a stress transcriptome before priming the SA- and ROS-dependent defenses during grapevine's induced resistance against Plasmopara viticola. PloS One 9 (2):e88145
Gnan S, Marsh T, Kover PX (2017) Inflorescence photosynthetic contribution to fitness releases Arabidopsis thaliana plants from trade-off constraints on early flowering. PLoS One 12 (10):e0185835
Huot B, Yao J, Montgomery BL, He SY (2014) Growth-defense tradeoffs in plants: A balancing act to optimize fitness. Mol Plant 7:1267–1287
Jaulneau V, Lafitte C, Corio-Costet MF, Stadnik MJ, Salamagne S, Briand X, Esquerre-Tugaye MT, Dumas B (2011) An Ulva armoricana extract protects plants against three powdery mildew pathogens. Eur J Plant Pathol 131:393–401
Jayaraj J, Wan A, Rahman M, Punja ZK (2008) Seaweed extract reduces foliar fungal diseases on carrot. Crop Prot 27:1360–1366
Jayaraman 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
Jimenez E, Dorta F, Medina C, Ramirez A, Ramirez I, Pena-Cortes H (2011) Anti-phytopathogenic activities of macro-algae extracts. Mar Drugs 9:739–756
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 28:386–399
Kidgell JT, Magnusson M, de Nys R, Glasson CRK (2019) Ulvan: A systematic review of extraction, composition and function. Algal Res 39:101422
Laporte D, Vera J, Chandia NP, Zuniga EA, Matsuhiro B, Moenne A (2007) Structurally unrelated algal oligosaccharides differentially stimulate growth and defense against tobacco mosaic virus in tobacco plants. J Appl Phycol 19:79–88
Menard R, Alban S, de Ruffray P, Jamois F, Franz G, Fritig B, Yvin JC, Kauffmann S (2004) β-1,3 glucan sulfate, but not β-1,3 glucan, induces the salicylic acid signaling pathway in tobacco and Arabidopsis. Plant Cell 16:3020–3032
Menard R, de Ruffray P, Fritig B, Yvin JC, Kauffmann S (2005) Defense and resistance-inducing activities in tobacco of the sulfated β-1,3 glucan PS3 and its synergistic activities with the unsulfated molecule. Plant Cell Physiol 46:1964–1972
Ning YS, Liu WD, Wang GL (2017) Balancing immunity and yield in crop plants. Trends Plant Sci 22:1069–1079
Paulert R, Talamini V, Cassolato JEF, Duarte MER, Noseda MD, Smania A, Stadnik MJ (2009) Effects of sulfated polysaccharide and alcoholic extracts from green seaweed Ulva fasciata on anthracnose severity and growth of common bean (Phaseolus vulgaris L.). J Plant Dis Protect 116:263–270
Raghavendra VB, Lokesh S, Prakashl HS (2007) Dravya, a product of seaweed extract (Sargassum wightii), induces resistance in cotton against Xanthomonas campestris pv. malvacearum. Phytoparasitica 35:442–449
Sangha JS, Kandasamy S, Khan W, Bahia NS, Singh RP, Critchley AT, Prithiviraj B (2015) Lambda-carrageenan suppresses tomato chlorotic dwarf viroid (TCDVd) replication and symptom expression in tomatoes. Mar Drugs 13:2875–2889
Sangha JS, Ravichandran S, Prithiviraj K, Critchley AT, Prithiviraj B (2010) Sulfated macroalgal polysaccharides lambda-carrageenan and iota-carrageenan differentially alter Arabidopsis thaliana resistance to Sclerotinia sclerotiorum. Physiol Mol Plant Pathol 75:38–45
Schiener P, Black KD, Stanley MS, Green DH (2015) The seasonal variation in the chemical composition of the kelp species Laminaria digitata, Laminaria hyperborea, Saccharina latissima and Alaria esculenta. J Appl Phycol 27:363–373
Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675
Sharma HSS, Fleming C, Selby C, Rao JR, Martin T (2014) Plant biostimulants: a review on the processing of macroalgae and use of extracts for crop management to reduce abiotic and biotic stresses. J Appl Phycol 26:465–490
Shukla PS, Borza T, Critchley AT, Prithiviraj B (2021) Seaweed-based compounds and products for sustainable protection against plant pathogens. Mar Drugs 19 (2): 59
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: 655
Stengel DB, Connan S, Popper ZA (2011) Algal chemodiversity and bioactivity: Sources of natural variability and implications for commercial application. Biotechnol Adv 29:483–501
Stirk WA, Reinecke DL, van Staden J (2007) Seasonal variation in antifungal, antibacterial and acetylcholinesterase activity in seven South African seaweeds. J Appl Phycol 19:271–276
Subramanian S, Sangha JS, Gray BA, Singh RP, Hiltz D, Critchley AT, Prithiviraj B (2011) Extracts of the marine brown macroalga, Ascophyllum nodosum, induce jasmonic acid dependent systemic resistance in Arabidopsis thaliana against Pseudomonas syringae pv tomato DC3000 and Sclerotinia sclerotiorum. Eur J Plant Pathol 131:237–248
Team RC (2020) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/
Thines M, Choi YJ, Kemen E, Ploch S, Holub EB, Shin HD, Jones JDG (2009) A new species of Albugo parasitic to Arabidopsis thaliana reveals new evolutionary patterns in white blister rusts (Albuginaceae). Persoonia 22:123–128
van Butselaar T, Van den Ackerveken G (2020) Salicylic acid steers the growth-immunity tradeoff. Trends Plant Sci 25:566–576
van der Burgh AM, Joosten M (2019) Plant immunity: Thinking outside and inside the box. Trends Plant Sci 24:587–601
Zhang S, Mersha Z, Vallad GE, Huang CH (2016) Management of powdery mildew in squash by plant and alga extract biopesticides. Plant Pathol J 32:528–536
Zhang XQ, Thomsen M (2019) Biomolecular composition and revenue explained by interactions between extrinsic factors and endogenous rhythms of Saccharina latissima. Mar Drugs 17:107
Acknowledgements
Aarhus University Research Foundation provided financial support through a synergy grant to the project ‘From Seaweed waste to bio-stimulant’. We thank project participants Karen Koefoed Petersen, Annette Bruhn, Michael Bo Rasmussen, Benita Hyldgaard and Marianne Glasius for discussions of experimental design and results. We thank David Richardson for help on language and presentation.
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Support from a synergy grant from Aarhus University Research Foundation.
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Jensen, A., Jorgensen, T.H. Extracts of Saccharina latissima and Ulva lactuca affect the balance between growth and immunity in Arabidopsis thaliana. J Appl Phycol 34, 2201–2209 (2022). https://doi.org/10.1007/s10811-022-02761-8
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DOI: https://doi.org/10.1007/s10811-022-02761-8