Abstract
We evaluated the role of Kelpak® on growth, nutritional content, phytohormones, and phenolic acids in the angiosperm Ceratotheca triloba (Bernh.) Hook.f. grown under macronutrient-deficient conditions. Seeds were germinated in the greenhouse and established seedlings were treated with 50% Hoagland’s solution (50% HS) or nutrient-deficient solutions lacking one of the following: nitrogen (-N), phosphorus (-P), potassium (-K), which were either treated with or without Kelpak® (control). After 4 months of growth, macronutrient deficiency severely reduced growth and nutritional composition in plants. Nevertheless, the detrimental effects of insufficient macronutrient supply on growth were ameliorated with the application of Kelpak®, with a fourfold (-N), threefold (-P), and twofold (-K) increase in leaf and root fresh weight. Mineral and carbohydrate levels increased in plants deprived of N and P when Kelpak® was applied in the different soils. Macronutrient stress (N, P, K) increased phytohormone production in C. triloba more than in 50% HS-treated plants. The phytohormone content in macronutrient-deficient leaves was further enhanced with the application of Kelpak®. On the contrary, application of Kelpak® suppressed the production of phenolic acids in 50% HS, -N, and -K-treated plants when compared to the control treatments. The interaction between macronutrient deficiency and Kelpak® application played an important role in the regulation of phytohormone and phenolic acid concentration in C. triloba. The current findings demonstrated the potential of Kelpak® as an efficient biostimulant that enhances nutrient uptake for improved growth and biochemicals in C. triloba under macronutrient stress condition.
Similar content being viewed by others
References
Akula R, Ravishankar GA (2011) Influence of abiotic stress signals on secondary metabolites in plants. Plant Signal Behav 6:1720–1731
Amtmann A, Hammond JP, Armengaud P, White PJ (2005) Nutrient sensing and signalling in plants: potassium and phosphorus. Adv Bot Res 43:209–257
Aremu AO, Stirk WA, Kulkarni MG, Tarkowská D, Turečková V, Gruz J, Šubrtová M, Pěnčík A, Novák O, Doležal K, Strnad M, Van Staden J (2015) Evidence of phytohormones and phenolic acids variability in garden-waste-derived vermicompost leachate, a well-known plant growth stimulant. Plant Growth Regul 75:483–492
Aremu AO, Plačková L, Gruz J, Bíba O, Novák O, Stirk WA, Doležal K, Van Staden J (2016) Seaweed-derived biostimulant (Kelpak®) influences endogenous cytokinins and bioactive compounds in hydroponically grown Eucomis autumnalis. J Plant Growth Regul 35:151–162
Arthur GD, Aremu AO, Kulkarni MG, Van Staden J (2012) Vermicompost leachate alleviates deficiency of phosphorus and potassium in tomato seedlings. HortScience 47:1304–1307
Beckett RP, Mathegka ADM, Van Staden J (1994) Effect of seaweed concentrate on yield of nutrient-stressed tepary bean (Phaseolus acutifolius Gray). J Appl Phycol 6:429–430
Brewitz E, Larsson C-M, Larsson M (1995) Influence of nitrate supply on concentrations and translocation of abscisic acid in barley (Hordeum vulgare). Physiol Plant 95:499–506
Bulgari R, Cocetta G, Trivellini A, Vernieri P, Ferrante A (2014) Biostimulants and crop responses: a review. Biol Agric Hortic 31:1–17
Cakmak I (2002) Plant nutrition research: priorities to meet human needs for food in sustainable ways. Plant Soil 247:3–24
Calvo P, Nelson L, Kloepper JW (2014) Agricultural uses of plant biostimulants. Plant Soil 383:3–41
Chaoui HI, Zibilske LM, Ohno T (2003) Effects of earthworm casts and compost on soil microbial activity and plant nutrient availability. Soil Biol Biochem 35:295–302
Colla G, Rouphael Y, Canaguier R, Svecova E, Cardarelli M (2014) Biostimulant action of a plant-derived protein hydrolysate produced through enzymatic hydrolysis. Front Plant Sci 5
Colling J, Stander MA, Makunga NP (2010) Nitrogen supply and abiotic stress influence canavanine synthesis and the productivity of in vitro regenerated Sutherlandia frutescens microshoots. J Plant Physiol 167:1521–1524
Davies WJ, Kudoyarova G, Hartung W (2005) Long-distance ABA signaling and its relation to other signaling pathways in the detection of soil drying and the mediation of the plant’s response to drought. J Plant Growth Regul 24:285–295
Ertani A, Schiavon M, Altissimo A, Franceschi C, Nardi S (2011) Phenol-containing organic substances stimulate phenylpropanoid metabolism in Zea mays. J Plant Nutr Soil Sci 174:496–503
European Biostimulants Industry Council (2012) Promoting the biostimulant industry and the role of plant biostimulants in making agriculture more sustainable. http://www.biostimulants.eu/. Accessed 15 June 2018
Floková K, Tarkowská D, Miersch O, Strnad M, Wasternack C, Novák O (2014) UHPLC-MS/MS based target profiling of stress-induced phytohormones. Phytochemistry 105:147–157
Gremigni P, Hamblin J, Harris D, Cowling WA (2003) The interaction of phosphorus and potassium with seed alkaloid concentrations, yield and mineral content in narrow-leafed lupin (Lupinus angustifolius L.). Plant Soil 253:413–427
Gruhn P, Goletti F, Yudelman M (2000) Integrated nutrient management, soil fertility, and sustainable agriculture: current issues and future challenges. International Food Policy Research Institute, Washington, D.C.
Grúz J, Novák O, Strnad M (2008) Rapid analysis of phenolic acids in beverages by UPLC-MS/MS. Food Chem 111:789–794
Hamza B, Suggars A (2001) Biostimulants: myths and realities. TurfGrass Trends 8:6–10
Hare PD, Cress WA, van Staden J (1997) The involvement of cytokinins in plant responses to environmental stress. Plant Growth Regul 23:79–103
Hou X, Jones BT (2000) Inductively coupled plasma/optical emission spectrometry. In: Meyers RA (ed) Encyclopedia of analytical chemistry. Wiley, Chichester
Kiba T, Kudo T, Kojima M, Sakakibara H (2011) Hormonal control of nitrogen acquisition: roles of auxin, abscisic acid, and cytokinin. J Exp Bot 62:1399–1409
Liebman M, Davis AS (2000) Integration of soil, crop and weed management in low-external-input farming systems. Weed Res 40:27–47
Liu M, Hu F, Chen X, Huang Q, Jiao J, Zhang B, Li H (2009) Organic amendments with reduced chemical fertilizer promote soil microbial development and nutrient availability in a subtropical paddy field: the influence of quantity, type and application time of organic amendments. Appl Soil Ecol 42:166–175
Masondo NA, Finnie JF, Van Staden J (2016a) Nutritional and pharmacological potential of the genus Ceratotheca – an underutilized leafy vegetable of Africa. J Ethnopharmacol 178:209–221
Masondo NA, Kulkarni MG, Rengasamy KRR, Pendota SC, Finnie JF, Van Staden J (2016b) Effect of vermicompost leachate in Ceratotheca triloba under nutrient deficiency. Acta Physiol Plant 38:236
Masondo NA, Kulkarni MG, Finnie JF, Van Staden J (2018) Influence of biostimulants-seed-priming on Ceratotheca triloba germination and seedling growth under low temperatures, low osmotic potential and salinity stress. Ecotoxicol Environ Saf 147:43–48
Mattila P, Hellström J (2007) Phenolic acids in potatoes, vegetables, and some of their products. J Food Compos Anal 20:152–160
Nacry P, Canivenc G, Muller B, Azmi A, Van Onckelen H, Rossignol M, Doumas P (2005) A role for auxin redistribution in the responses of the root system architecture to phosphate starvation in Arabidopsis. Plant Physiol 138:2061–2074
Niu YF, Chai RS, Jin GL, Wang H, Tang CX, Zhang YS (2013) Responses of root architecture development to low phosphorus availability: a review. Ann Bot 112:391–408
Novák O, Hauserová E, Amakorová P, Doležal K, Strnad M (2008) Cytokinin profiling in plant tissues using ultra-performance liquid chromatography-electrospray tandem mass spectrometry. Phytochemistry 69:2214–2224
Odhav B, Beekrum S, Akula U, Baijnath H (2007) Preliminary assessment of nutritional value of traditional leafy vegetables in KwaZulu-Natal, South Africa. J Food Compos Anal 20:430–435
Papenfus H, Kulkarni M, Stirk W, Finnie J, Van Staden J (2013) Effect of a commercial seaweed extract (Kelpak®) and polyamines on nutrient-deprived (N, P and K) okra seedlings. Sci Hortic 151:142–146
Peleg Z, Blumwald E (2011) Hormone balance and abiotic stress tolerance in crop plants. Curr Opin Plant Biol 14:290–295
Peuke AD, Jeschke WD, Hartung W (1994) The uptake and flow of C, N and ions between roots and shoots in Ricinus communis L. III. Long-distance transport of abscisic acid depending on nitrogen nutrition and salt stress. J Exp Bot 45:741–747
Peuke AD, Jeschke WD, Hartung W (2002) Flows of elements, ions and abscisic acid in Ricinus communis and site of nitrate reduction under potassium limitation. J Exp Bot 53:241–250
Plačková L, Hrdlička J, Smýkalová I, Cvečková M, Novák O, Griga M, Doležal K (2015) Cytokinin profiling of long-term in vitro pea (Pisum sativum L.) shoot cultures. Plant Growth Regul 77:125–132
Rafiee H, Naghdi Badi H, Mehrafarin A, Qaderi A, Zarinpanjeh N, Sekara A, Zand E (2016) Application of plant biostimulants as new approach to improve the biological responses of medicinal plants-a critical review. J Med Plants 3:6–39
Rathore SS, Chaudhary DR, Boricha GN, Ghosh A, Bhatt BP, Zodape ST, Patolia JS (2009) Effect of seaweed extract on the growth, yield and nutrient uptake of soybean (Glycine max) under rainfed conditions. S Afr J Bot 75:351–355
Roberts SK, Snowman BN (2000) The effects of ABA on channel-mediated K+ transport across higher plant roots. J Exp Bot 51:1585–1594
Rouphael Y, Giordano M, Cardarelli M, Cozzolino E, Mori M, Kyriacou M, Bonini P, Colla G (2018) Plant and seaweed-based extracts increase yield but differentially modulate nutritional quality of greenhouse spinach through biostimulant action. Agronomy 8:126. https://doi.org/10.3390/agronomy8070126
Saa S, Olivos-Del Rio A, Castro S, Brown PH (2015) Foliar application of microbial and plant based biostimulants increases growth and potassium uptake in almond (Prunus dulcis [Mill.] D. A. Webb). Front Plant Sci 6:87
Sadasivam S, Manickam A (1996) Biochemical methods, 3rd edn. New Age International, New Delhi
Schmelz EA, Alborn HT, Engelberth J, Tumlinson JH (2003) Nitrogen deficiency increases volicitin-induced volatile emission, jasmonic acid accumulation, and ethylene sensitivity in maize. Plant Physiol 133:295–306
Schraut D, Heilmeier H, Hartung W (2005) Radial transport of water and abscisic acid (ABA) in roots of Zea mays under conditions of nutrient deficiency. J Exp Bot 56:879–886
Stirk WA, Arthur GD, Lourens AF, Novák O, Strnad M, Van Staden J (2004) Changes in cytokinin and auxin concentrations in seaweed concentrates when stored at an elevated temperature. J Appl Phycol 16:31–39
Stirk WA, Tarkowská D, Turečová V, Strnad M, Van Staden J (2014) Abscisic acid, gibberellins and brassinosteroids in Kelpak®, a commercial seaweed extract made from Ecklonia maxima. J Appl Phycol 26:561–567
Street RA, Kulkarni MG, Stirk WA, Southway C, Van Staden J (2008) Variation in heavy metals and microelements in South African medicinal plants obtained from street markets. Food Addit Contam Part A Chem Anal Control Expo Risk Assess 25:953–960
Theunissen J, Ndakidemi PA, Laubscher CP (2010) Potential of vermicompost produced from plant waste on the growth and nutrient status in vegetable production. Int J Phys Sci 5:1964–1973
Tilman D (1999) Global environmental impacts of agricultural expansion: the need for sustainable and efficient practices. Proc Natl Acad Sci 96:5995–6000
Wang Y, Li B, Du M, Eneji AE, Wang B, Duan L, Li Z, Tian X (2012) Mechanism of phytohormone involvement in feedback regulation of cotton leaf senescence induced by potassium deficiency. J Exp Bot 63:5887–5901
Wierzbowska J, Cwalina-Ambroziak B, Bowszys T, Glosek-Sobieraj M, Mackiewicz-Walec E (2015) Content of microelements in tubers of potato treated with biostimulators. Pol J Natur Sci 30:225–234
Wittenmayer L, Merbach W (2005) Plant responses to drought and phosphorus deficiency: contribution of phytohormones in root-related processes. J Plant Nutr Soil Sci 168:531–540
Zhang H, Rong H, Pilbeam D (2007) Signalling mechanisms underlying the morphological responses of the root system to nitrogen in Arabidopsis thaliana. J Exp Bot 58:2329–2338
Acknowledgments
Stellenbosch University (NAM) and North West University (AOA) are acknowledged for provision of access to resources utilized during the preparation of the manuscript.
Funding
We received financial support from the National Research Foundation (NRF, Grant UID: 89290), Graça Machel (Canon Collins), and the University of KwaZulu-Natal (Pietermaritzburg), South Africa. Financial assistance also was received from The Ministry of Education, Youth and Sport of the Czech Republic via ERDF project “Plants as a tool for sustainable global development” (No. CZ.02.1.01/0.0/0.0/16_019/0000827), the Internal Grant Agency of Palacký University (IGA_PrF_2019_018), and the Czech Science Foundation (Grant 17-06613S).
Author information
Authors and Affiliations
Contributions
NAM conceived the research idea, designed the experiments, conducted greenhouse experiments, and quantified the stress-related phytohormones. AOA, MGK, ON, JG, and KD advised on relevant experimental design and experiments performed. JG, KD, and MS provided equipment used for quantification of phenolic acids and phytohormones. AOA, IP, LP, and MŠ assisted with the quantification of phytohormones. AOA provided technical assistance in the interpretation of the phytohormone and phenolic acid data. NAM prepared the manuscript while all authors edited and approved the final version. JVS and JFF coordinated and supervised the project.
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
Masondo, N.A., Aremu, A.O., Kulkarni, M.G. et al. Elucidating the role of Kelpak® on the growth, phytohormone composition, and phenolic acids in macronutrient-stressed Ceratotheca triloba. J Appl Phycol 31, 2687–2697 (2019). https://doi.org/10.1007/s10811-019-01759-z
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10811-019-01759-z