Toward a Sustainable Agriculture Through Plant Biostimulants: From Experimental Data to Practical Applications
Abstract
:1. Biostimulants in Agriculture: Rationale
2. The Role of Non-Microbial and Microbial Biostimulants in Morpho-Anatomical, Biochemical and Physiological Traits of Crops
3. The Role of Non-Microbial and Microbial Biostimulants in Enhancing Nutrient Uptake and Efficiency
4. The Role of Non-Microbial and Microbial Biostimulants in Abiotic Stresses Tolerance/Resistance
5. The Role of Non-Microbial and Microbial Biostimulants in Improving Quality Traits
6. Conclusions and Looking Forward
Author Contributions
Funding
Conflicts of Interest
References
- Colla, G.; Rouphael, Y. Biostimulants in horticulture. Sci. Hortic. 2015, 196, 1–2. [Google Scholar] [CrossRef]
- Rouphael, Y.; Colla, G. Synergistic Biostimulatory Action: Designing the Next Generation of Plant Biostimulants for Sustainable Agriculture. Front. Plant Sci. 2018, 9, 9. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rouphael, Y.; Colla, G. Editorial: Biostimulants in Agriculture. Front. Plant Sci. 2020, 11, 40. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jägermeyr, J. Agriculture’s historic twin-challenge toward sustainable water use and food supply for all. Front. Sustain. Food Syst. 2020, 4, 35. [Google Scholar] [CrossRef]
- Fiorentino, N.; Ventorino, V.; Woo, S.L.; Pepe, O.; De Rosa, A.; Gioia, L.; Romano, I.; Lombardi, N.; Napolitano, M.; Colla, G.; et al. Trichoderma-Based Biostimulants Modulate Rhizosphere Microbial Populations and Improve N Uptake Efficiency, Yield, and Nutritional Quality of Leafy Vegetables. Front. Plant Sci. 2018, 9, 9. [Google Scholar] [CrossRef] [Green Version]
- Rouphael, Y.; Spíchal, L.; Panzarová, K.; Casa, R.; Colla, G. High-Throughput Plant Phenotyping for Developing Novel Biostimulants: From Lab to Field or From Field to Lab? Front. Plant Sci. 2018, 9, 1197. [Google Scholar] [CrossRef]
- E.U. Regulation of the European Parliament and of the Council Laying Down Rules on the Making Available on the Market of EU Fertilising Products and Amending Regulations (EC) No 1069/2009 and (EC) No 1107/2009 and Repealing Regulation (EC) No 2003/2003. 2019. Available online: https://eur-lex.europa.eu/legal-content/EN/TXT/?uri=OJ:L:2019:170:TOC (accessed on 10 September 2020).
- Battacharyya, D.; Babgohari, M.Z.; Rathor, P.; Prithiviraj, B. Seaweed extracts as biostimulants in horticulture. Sci. Hortic. 2015, 196, 39–48. [Google Scholar] [CrossRef]
- Canellas, L.P.; Olivares, F.L.; Aguiar, N.O.; Jones, D.L.; Nebbioso, A.; Mazzei, P.; Piccolo, A. Humic and fulvic acids as biostimulants in horticulture. Sci. Hortic. 2015, 196, 15–27. [Google Scholar] [CrossRef]
- López-Bucio, J.; Pelagio-Flores, R.; Herrera-Estrella, A. Trichoderma as biostimulant: Exploiting the multilevel properties of a plant beneficial fungus. Sci. Hortic. 2015, 196, 109–123. [Google Scholar] [CrossRef]
- Ruzzi, M.; Aroca, R. Plant growth-promoting rhizobacteria act as biostimulants in horticulture. Sci. Hortic. 2015, 196, 124–134. [Google Scholar] [CrossRef]
- Savvas, D.; Ntatsi, G. Biostimulant activity of silicon in horticulture. Sci. Hortic. 2015, 196, 66–81. [Google Scholar] [CrossRef]
- Colla, G.; Nardi, S.; Cardarelli, M.; Ertani, A.; Lucini, L.; Canaguier, R.; Rouphael, Y. Protein hydrolysates as biostimulants in horticulture. Sci. Hortic. 2015, 196, 28–38. [Google Scholar] [CrossRef]
- Colla, G.; Hoagland, L.; Ruzzi, M.; Cardarelli, M.; Bonini, P.; Canaguier, R.; Rouphael, Y. Biostimulant Action of Protein Hydrolysates: Unraveling Their Effects on Plant Physiology and Microbiome. Front. Plant Sci. 2017, 8, 2202. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rouphael, Y.; Franken, P.; Schneider, C.; Schwarz, D.; Giovannetti, M.; Agnolucci, M.; De Pascale, S.; Bonini, P.; Colla, G. Arbuscular mycorrhizal fungi act as biostimulants in horticultural crops. Sci. Hortic. 2015, 196, 91–108. [Google Scholar] [CrossRef]
- Chiaiese, P.; Corrado, G.; Colla, G.; Kyriacou, M.C.; Rouphael, Y. Renewable Sources of Plant Biostimulation: Microalgae as a Sustainable Means to Improve Crop Performance. Front. Plant Sci. 2018, 9, 9. [Google Scholar] [CrossRef] [Green Version]
- De Pascale, S.; Rouphael, Y.; Colla, G. Plant biostimulants: Innovative tool for enhancing plant nutrition in organic farming. Eur. J. Hortic. Sci. 2018, 82, 277–285. [Google Scholar] [CrossRef]
- Basile, B.; Rouphael, Y.; Colla, G.; Soppelsa, S.; Andreotti, C. Appraisal of emerging crop management opportunities in fruit trees, grapevines and berry crops facilitated by the application of biostimulants. Sci. Hortic. 2020, 267, 109330. [Google Scholar] [CrossRef]
- Rouphael, Y.; Kyriacou, M.C.; Petropoulos, S.A.; De Pascale, S.; Colla, G. Improving vegetable quality in controlled environments. Sci. Hortic. 2018, 234, 275–289. [Google Scholar] [CrossRef]
- Rouphael, Y.; Lucini, L.; Miras-Moreno, B.; Colla, G.; Bonini, P.; Cardarelli, M. Metabolomic Responses of Maize Shoots and Roots Elicited by Combinatorial Seed Treatments With Microbial and Non-microbial Biostimulants. Front. Microbiol. 2020, 11, 664. [Google Scholar] [CrossRef]
- Rouphael, Y.; Colla, G.; Graziani, G.; Ritieni, A.; Cardarelli, M.; De Pascale, S. Phenolic Composition, Antioxidant Activity and Mineral Profile in Two seed-Propagated Artichoke Cultivars as Affected by Microbial Inoculants And Planting Time. Food Chem. 2017, 234, 10–19. [Google Scholar] [CrossRef]
- Biostimulants Market by Active Ingredient (Humic Substances, Amino Acids, Seaweed Extracts, Microbial Amendments), Crop Type (Fruits & Vegetables, Cereals, Turf & Ornamentals), Application Method, Form, and Region—Global Forecast to 2025. Available online: https://www.marketsandmarkets.com/Market-Reports/biostimulant-market-1081.html?gclid=CjwKCAjw4_H6BRALEiwAvgfzq1LVX47L4C4O0v0leN5GfYGuk0xW2oF25JDZhWGs03E3I2rL1kEwGxoCnsAQAvD_BwE (accessed on 10 September 2020).
- Qiu, Y.; Amirkhani, M.; Mayton, H.; Chen, Z.; Taylor, A. Biostimulant Seed Coating Treatments to Improve Cover Crop Germination and Seedling Growth. Agronomy 2020, 10, 154. [Google Scholar] [CrossRef] [Green Version]
- Ben-Jabeur, M.; Kthiri, Z.; Harbaoui, K.; Belguesmi, K.; Serret, M.D.; Araus, J.; Hamada, W.; Jabeur, B. Seed Coating with Thyme Essential Oil or Paraburkholderia phytofirmans PsJN Strain: Conferring Septoria Leaf Blotch Resistance and Promotion of Yield and Grain Isotopic Composition in Wheat. Agronomy 2019, 9, 586. [Google Scholar] [CrossRef] [Green Version]
- D’Addabbo, T.; Laquale, S.; Perniola, M.; Candido, V.; Addabbo, D. Biostimulants for Plant Growth Promotion and Sustainable Management of Phytoparasitic Nematodes in Vegetable Crops. Agronomy 2019, 9, 616. [Google Scholar] [CrossRef] [Green Version]
- Allaga, H.; Bóka, B.; Poor, P.; Nagy, V.D.; Szűcs, A.; Stankovics, I.; Takó, M.; Manczinger, L.; Vágvölgyi, C.; Kredics, L.; et al. A Composite Bioinoculant Based on the Combined Application of Beneficial Bacteria and Fungi. Agronomy 2020, 10, 220. [Google Scholar] [CrossRef] [Green Version]
- Ertani, A.; Nardi, S.; Francioso, O.; Pizzeghello, D.; Tinti, A.; Schiavon, M. Metabolite-Targeted Analysis and Physiological Traits of Zea mays L. in Response to Application of a Leonardite-Humate and Lignosulfonate-Based Products for Their Evaluation as Potential Biostimulants. Agronomy 2019, 9, 445. [Google Scholar] [CrossRef] [Green Version]
- Kim, H.-J.; Ku, K.-M.; Choi, S.; Cardarelli, M. Vegetal-derived Biostimulant Enhances Adventitious Rooting in Cuttings of Basil, Tomato, and Chrysanthemum via Brassinosteroid-mediated Processes. Agronomy 2019, 9, 74. [Google Scholar] [CrossRef] [Green Version]
- Khan, S.; Yu, H.-J.; Li, Q.; Gao, Y.; Sallam, B.N.; Wang, H.; Liu, P.; Jiang, W. Exogenous Application of Amino Acids Improves the Growth and Yield of Lettuce by Enhancing Photosynthetic Assimilation and Nutrient Availability. Agronomy 2019, 9, 266. [Google Scholar] [CrossRef] [Green Version]
- McCoy, R.M.; Meyer, G.W.; Rhodes, D.; Murray, G.C.; Sors, T.G.; Widhalm, J.R. Exploratory Study on the Foliar Incorporation and Stability of Isotopically Labeled Amino Acids Applied to Turfgrass. Agronomy 2020, 10, 358. [Google Scholar] [CrossRef] [Green Version]
- Bákonyi, N.; Kisvarga, S.; Barna, D.; Tóth, I.O.; El-Ramady, H.; Abdalla, N.; Kovács, S.; Rozbach, M.; Fehér, C.; Elhawat, N.; et al. Chemical Traits of Fermented Alfalfa Brown Juice: Its Implications on Physiological, Biochemical, Anatomical, and Growth Parameters of Celosia. Agronomy 2020, 10, 247. [Google Scholar] [CrossRef] [Green Version]
- Kisvarga, S.; Barna, D.; Kovács, S.; Csatári, G.; Tóth, I.O.; Fári, M.; Makleit, P.; Veres, S.; Alshaal, T.; Bákonyi, N. Fermented Alfalfa Brown Juice Significantly Stimulates the Growth and Development of Sweet Basil (Ocimum basilicum L.) Plants. Agronomy 2020, 10, 657. [Google Scholar] [CrossRef]
- Niewiadomska, A.; Sulewska, H.; Wolna-Maruwka, A.; Ratajczak, K.; Waraczewska, Z.; Budka, A. The Influence of Bio-Stimulants and Foliar Fertilizers on Yield, Plant Features, and the Level of Soil Biochemical Activity in White Lupine (Lupinus albus L.) Cultivation. Agronomy 2020, 10, 150. [Google Scholar] [CrossRef] [Green Version]
- Carillo, P.; Ciarmiello, L.F.; Woodrow, P.; Corrado, G.; Chiaiese, P.; Rouphael, Y. Enhancing Sustainability by Improving Plant Salt Tolerance through Macro- and Micro-Algal Biostimulants. Biology 2020, 9, 253. [Google Scholar] [CrossRef] [PubMed]
- Kocira, S.; Szparaga, A.; Kuboń, M.; Czerwinska, E.; Piskier, T. Morphological and Biochemical Responses of Glycine max (L.) Merr. to the Use of Seaweed Extract. Agronomy 2019, 9, 93. [Google Scholar] [CrossRef] [Green Version]
- Kocira, A.; Lamorska, J.; Kornas, R.; Nowosad, N.; Tomaszewska, M.; Leszczyńska, D.; Kozłowicz, K.; Tabor, S. Changes in Biochemistry and Yield in Response to Biostimulants Applied in Bean (Phaseolus vulgaris L.). Agronomy 2020, 10, 189. [Google Scholar] [CrossRef] [Green Version]
- Wadas, W.; Dziugieł, T. Changes in Assimilation Area and Chlorophyll Content of Very Early Potato (Solanum tuberosum L.) Cultivars as Influenced by Biostimulants. Agronomy 2020, 10, 387. [Google Scholar] [CrossRef] [Green Version]
- Ashour, M.; El-Shafei, A.A.; Khairy, H.M.; Abd-Elkader, D.Y.; Mattar, M.; Alataway, A.; Hassan, S. Effect of Pterocladia capillacea Seaweed Extracts on Growth Parameters and Biochemical Constituents of Jew’s Mallow. Agronomy 2020, 10, 420. [Google Scholar] [CrossRef] [Green Version]
- Pohl, A.; Grabowska, A.; Kalisz, A.; Sękara, A. Biostimulant Application Enhances Fruit Setting in Eggplant—An Insight into the Biology of Flowering. Agronomy 2019, 9, 482. [Google Scholar] [CrossRef] [Green Version]
- Jo, H.; Tagele, S.B.; Pham, H.Q.; Kim, M.-C.; Choi, S.; Park, Y.-J.; Ibal, J.C.; Park, G.-S.; Shin, J.-H.; Kim, M.-J. Response of Soil Bacterial Community and Pepper Plant Growth to Application of Bacillus thuringiensis KNU-07. Agronomy 2020, 10, 551. [Google Scholar] [CrossRef]
- Carillo, P.; Colla, G.; Fusco, G.M.; Dell’Aversana, E.; El-Nakhel, C.; Giordano, M.; Pannico, A.; Cozzolino, E.; Mori, M.; Reynaud, H.; et al. Morphological and Physiological Responses Induced by Protein Hydrolysate-Based Biostimulant and Nitrogen Rates in Greenhouse Spinach. Agronomy 2019, 9, 450. [Google Scholar] [CrossRef] [Green Version]
- Di Mola, I.; Cozzolino, E.; Ottaiano, L.; Giordano, M.; Rouphael, Y.; Colla, G.; Mori, M. Effect of Vegetal- and Seaweed Extract-Based Biostimulants on Agronomical and Leaf Quality Traits of Plastic Tunnel-Grown Baby Lettuce under Four Regimes of Nitrogen Fertilization. Agronomy 2019, 9, 571. [Google Scholar] [CrossRef] [Green Version]
- Di Mola, I.; Cozzolino, E.; Ottaiano, L.; Nocerino, S.; Rouphael, Y.; Colla, G.; El-Nakhel, C.; Mori, M. Nitrogen use and uptake effciency and crop performance of baby spinach (Spinacia oleracea L.) and lamb’s lettuce (Valerianella locusta L.) grown under variable cub-optimal N regimes combined with plant-based biostimulant application. Agronomy 2020, 10, 278. [Google Scholar] [CrossRef] [Green Version]
- Rouphael, Y.; Carillo, P.; Colla, G.; Fiorentino, N.; Sabatino, L.; El-Nakhel, C.; Giordano, M.; Pannico, A.; Cirillo, V.; Shabani, E.; et al. Appraisal of Combined Applications of Trichoderma virens and a Biopolymer-Based Biostimulant on Lettuce Agronomical, Physiological, and Qualitative Properties under Variable N Regimes. Agronomy 2020, 10, 196. [Google Scholar] [CrossRef] [Green Version]
- Leoni, B.; Loconsole, D.; Cristiano, G.; De Lucia, B.; De Lucia, B. Comparison between Chemical Fertilization and Integrated Nutrient Management: Yield, Quality, N, and P Contents in Dendranthema grandiflorum (Ramat.) Kitam. Cultivars. Agronomy 2019, 9, 202. [Google Scholar] [CrossRef] [Green Version]
- Rouphael, Y.; Kyriacou, M.C.; Colla, G. Vegetable Grafting: A Toolbox for Securing Yield Stability under Multiple Stress Conditions. Front. Plant Sci. 2018, 8, 2255. [Google Scholar] [CrossRef] [Green Version]
- Bulgari, R.; Franzoni, G.; Ferrante, A. Biostimulants Application in Horticultural Crops under Abiotic Stress Conditions. Agronomy 2019, 9, 306. [Google Scholar] [CrossRef] [Green Version]
- Arnao, M.B.; Hernández-Ruiz, J. Melatonin as a Chemical Substance or as Phytomelatonin Rich-Extracts for Use as Plant Protector and/or Biostimulant in Accordance with EC Legislation. Agronomy 2019, 9, 570. [Google Scholar] [CrossRef] [Green Version]
- Elansary, H.O.; Mahmoud, E.A.; El-Ansary, D.O.; Mattar, M. Effects of Water Stress and Modern Biostimulants on Growth and Quality Characteristics of Mint. Agronomy 2019, 10, 6. [Google Scholar] [CrossRef] [Green Version]
- Barsanti, L.; Coltelli, P.; Gualtieri, P. Paramylon Treatment Improves Quality Profile and Drought Resistance in Solanum lycopersicum L. cv. Micro-Tom. Agronomy 2019, 9, 394. [Google Scholar] [CrossRef] [Green Version]
- Petropoulos, S.A.; Fernandes, Â; Plexida, S.; Chrysargyris, A.; Tzortzakis, N.; Barreira, J.C.M.; Barros, L.; Ferreira, I.C. Biostimulants Application Alleviates Water Stress Effects on Yield and Chemical Composition of Greenhouse Green Bean (Phaseolus vulgaris L.). Agronomy 2020, 10, 181. [Google Scholar] [CrossRef] [Green Version]
- Mannino, G.; Nerva, L.; Gritli, T.; Novero, M.; Fiorilli, V.; Bacem, M.; Bertea, C.M.; Lumini, E.; Chitarra, W.; Balestrini, R. Effects of di different microbial inocula on tomato tolerance to water deficit. Agronomy 2020, 10, 170. [Google Scholar] [CrossRef] [Green Version]
- Francesca, S.; Arena, C.; Mele, B.H.; Schettini, C.; Ambrosino, P.; Barone, A.; Rigano, M.M. The Use of a Plant-Based Biostimulant Improves Plant Performances and Fruit Quality in Tomato Plants Grown at Elevated Temperatures. Agronomy 2020, 10, 363. [Google Scholar] [CrossRef] [Green Version]
- Trevisan, S.; Manoli, A.; Quaggiotti, S. A Novel Biostimulant, Belonging to Protein Hydrolysates, Mitigates Abiotic Stress Effects on Maize Seedlings Grown in Hydroponics. Agronomy 2019, 9, 28. [Google Scholar] [CrossRef] [Green Version]
- Kyriacou, M.C.; Rouphael, Y. Towards a new definition of quality for fresh fruits and vegetables. Sci. Hortic. 2018, 234, 463–469. [Google Scholar] [CrossRef]
- Drobek, M.; Frąc, M.; Cybulska, J. Plant Biostimulants: Importance of the Quality and Yield of Horticultural Crops and the Improvement of Plant Tolerance to Abiotic Stress—A Review. Agronomy 2019, 9, 335. [Google Scholar] [CrossRef] [Green Version]
- Cozzolino, E.; Giordano, M.; Fiorentino, N.; El-Nakhel, C.; Pannico, A.; Di Mola, I.; Mori, M.; Kyriacou, M.C.; Colla, G.; Rouphael, Y. Appraisal of Biodegradable Mulching Films and Vegetal-Derived Biostimulant Application as Eco-Sustainable Practices for Enhancing Lettuce Crop Performance and Nutritive Value. Agronomy 2020, 10, 427. [Google Scholar] [CrossRef] [Green Version]
- Caruso, G.; Giordano, M.; Cozzolino, E.; Cuciniello, A.; Cenvinzo, V.; Bonini, P.; Colla, G.; Rouphael, Y. Yield and Nutritional Quality of Vesuvian Piennolo Tomato PDO as Affected by Farming System and Biostimulant Application. Agronomy 2019, 9, 505. [Google Scholar] [CrossRef] [Green Version]
- Soppelsa, S.; Kelderer, M.; Casera, C.; Bassi, M.; Robatscher, P.; Matteazzi, A.; Andreotti, C. Foliar Applications of Biostimulants Promote Growth, Yield and Fruit Quality of Strawberry Plants Grown under Nutrient Limitation. Agronomy 2019, 9, 483. [Google Scholar] [CrossRef] [Green Version]
- Gugała, M.; Sikorska, A.; Zarzecka, K.; Findura, P.; Malaga-Toboła, U.; Toboła, M. Chemical Composition of Winter Rape Seeds Depending on the Biostimulators Used. Agronomy 2019, 9, 716. [Google Scholar] [CrossRef] [Green Version]
- Chandrasekaran, M.; Chun, S.C.; Oh, J.-W.; Paramasivan, M.; Saini, R.K.; Sahayarayan, J.J. Bacillus subtilis CBR05 for Tomato (Solanum lycopersicum) Fruits in South Korea as a Novel Plant Probiotic Bacterium (PPB): Implications from Total Phenolics, Flavonoids, and Carotenoids Content for Fruit Quality. Agronomy 2019, 9, 838. [Google Scholar] [CrossRef] [Green Version]
- Caser, M.; Demasi, S.; Victorino, Í.M.M.; Donno, D.; Faccio, A.; Lumini, E.; Bianciotto, V.; Scariot, V. Arbuscular Mycorrhizal Fungi Modulate the Crop Performance and Metabolic Profile of Saffron in Soilless Cultivation. Agronomy 2019, 9, 232. [Google Scholar] [CrossRef] [Green Version]
- Caser, M.; Victorino, Í.M.M.; Demasi, S.; Berruti, A.; Donno, D.; Lumini, E.; Bianciotto, V.; Scariot, V. Saffron Cultivation in Marginal Alpine Environments: How AMF Inoculation Modulates Yield and Bioactive Compounds. Agronomy 2018, 9, 12. [Google Scholar] [CrossRef] [Green Version]
- Briglia, N.; Petrozza, A.; Hoeberichts, F.A.; Verhoef, N.; Povero, G. Investigating the Impact of Biostimulants on the Row Crops Corn and Soybean Using High-Efficiency Phenotyping and Next Generation Sequencing. Agronomy 2019, 9, 761. [Google Scholar] [CrossRef] [Green Version]
- Giovannini, L.; Palla, M.; Agnolucci, M.; Avio, L.; Sbrana, C.; Turrini, A.; Giovannetti, M. Arbuscular Mycorrhizal Fungi and Associated Microbiota as Plant Biostimulants: Research Strategies for the Selection of the Best Performing Inocula. Agronomy 2020, 10, 106. [Google Scholar] [CrossRef] [Green Version]
© 2020 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Rouphael, Y.; Colla, G. Toward a Sustainable Agriculture Through Plant Biostimulants: From Experimental Data to Practical Applications. Agronomy 2020, 10, 1461. https://doi.org/10.3390/agronomy10101461
Rouphael Y, Colla G. Toward a Sustainable Agriculture Through Plant Biostimulants: From Experimental Data to Practical Applications. Agronomy. 2020; 10(10):1461. https://doi.org/10.3390/agronomy10101461
Chicago/Turabian StyleRouphael, Youssef, and Giuseppe Colla. 2020. "Toward a Sustainable Agriculture Through Plant Biostimulants: From Experimental Data to Practical Applications" Agronomy 10, no. 10: 1461. https://doi.org/10.3390/agronomy10101461
APA StyleRouphael, Y., & Colla, G. (2020). Toward a Sustainable Agriculture Through Plant Biostimulants: From Experimental Data to Practical Applications. Agronomy, 10(10), 1461. https://doi.org/10.3390/agronomy10101461