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Biofertilization with Macrocystis pyrifera algae extracts combined with PGPR-enhanced growth in Lactuca sativa seedlings

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Abstract

To improve crop yields the application of fertilizers to provide nutrients to soils is recommended. An alternative option to substitute nutritional supplements of chemical origin is the use of biofertilizers. This study evaluated the effectiveness of a biofertilizer of natural origin, Macrocystis pyrifera algal extracts and its combination with the plant growth–promoting bacterium Azospirillum brasilense, on the germination and establishment of lettuce seedlings (Lactuca sativa) under two different water irrigation treatments. Results demonstrated that germination energy and germination power improved upon inoculation of lettuce seeds with the seaweed extract. After 7 days of culture, seedlings showed increased root growth which would help to ensure their establishment. The application of bacteria and algae individually or in combination exerted a positive effect on lettuce plant growth compared with controls (without applications). In addition, treatments with the brown seaweed extract favoured seedlings adaptation to an unfavourable environment (water deficit) by increasing their root mass and protecting them from the negative effects imposed by stress. These results suggest that the use of M. pyrifera extract to improve plant growth and to provide stress protection may be considered an interesting tool for agricultural purposes. Nevertheless, when A. brasilense (whose plant growth–promoting properties are largely known) is combined with the brown seaweed extract, a new biofertilizing formula is obtained and proposed for future seed inoculation technology, based on the promising effects observed in this work.

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References

  • Aloni R, Aloni E, Langhans M, Ullrich CI (2006) Role of cytokinin and auxin in shaping root architecture: regulating vascular differentiation, lateral root initiation, root apical dominance and root gravitropism. Ann Bot 97:883–893

    CAS  PubMed  PubMed Central  Google Scholar 

  • Amara U, Khalid R, Hayat R (2015) Soil bacteria and phytohormones for sustainable crop production. In: Maheshwari D. (Ed) Bacterial metabolites in sustainable agroecosystem. Sustainable Development and Biodiversity, Springer, Dordrecht, pp 87–103

  • Arioli T, Mattner SW, Winberg PC (2015) Applications of seaweed extracts in Australian agriculture: past, present and future. J Appl Phycol 27:2007–2015

    PubMed  PubMed Central  Google Scholar 

  • Ayarza-León JL (2014) Los alginatos: 20000 usos de las algas submarinas. PUPC 28:19–23

    Google Scholar 

  • Bartoli G, Casalongué C, Simontacchi M, Marquez-Garcia B, Foyer C (2013) Interactions between hormone and redox signalling pathways in the control of growth and cross tolerance to stress. Environ Exp Bot 94:73–88

    CAS  Google Scholar 

  • Bashan Y, De-Bashan LE (2010) How the plant growth-promoting bacterium Azospirillum promotes plant growth-a critical assessment. In: Sparks DL (ed) Advances in agronomy. Academic Press. Elsevier, London, pp 77–136

  • Bogaert KA, Blommaert L, Ljung K, Beeckman T, De Clerck O (2019) Auxin function in the brown alga Dictyota dichotoma. Plant Physiol 179:280–299

  • Briceño-Domínguez D, Hernandez-Carmona G, Moyo M, Stirk W, Van Staden J (2014) Plant growth promoting activity of seaweed liquid extracts produced from Macrocystis pyrifera under different pH and temperature conditions. J Appl Phycol 26:2203–2210

    Google Scholar 

  • Brumos J, Robles LM, Yun J, Vu TC, Jackson S, Alonso JM, Stepanova AN (2018) Local auxin biosynthesis is a key regulator of plant development. Dev Cell 47:306–318

    CAS  PubMed  Google Scholar 

  • Buschmann AH, Prescott S, Potin P, Faugeron S, Vasquez JA, Camus C, Varela DA (2014) The status of kelp exploitation and marine agronomy, with emphasis on Macrocystis pyrifera, in Chile. In: Bourgougnon N (ed) Advances in botanical research. Academic Press Elsevier, London, pp 161–188

    Google Scholar 

  • Carral C, Vicente C (2015) Vademécum de Productos Fitosanitarios y Nutricionales 2015. Ediciones Agrotécnicas SL, Madrid

    Google Scholar 

  • Cassán F, Perrig D, Sgroy V, Masciarelli O, Penna C, Luna V (2009) Azospirillum brasilense Az39 and Bradyrhizobium japonicum E 109 promote seed germination and early seedling growth, independently or co-inoculated in maize (Zea mays L.) and soybean (Glycine max L.). Eur J Soil Biol 45:28–35

    Google Scholar 

  • Cassán F, Perrig D, Sgroy V, Luna V (2011) Basic and technological aspects of phytohormone production by microorganisms: Azospirillum sp. as a model of plant growth promoting rhizobacteria. In: Maheshwari DK (ed) Bacteria in agrobiology: plant nutrient management. Springer, Berlin, pp 141–182

    Google Scholar 

  • Cassán F, Vanderleyden J, Spaepen S (2014) Physiological and agronomical aspects of phytohormone production by model plant-growth-promoting rhizobacteria (PGPR) belonging to the genus Azospirillum. J Plant Growth Regul 33:440–459

  • Chagnon M, Kreutzweiser D, Mitchell EA, Morrissey CA, Noome DA, Van der Sluijs JP (2015) Risks of large-scale use of systemic insecticides to ecosystem functioning and services. Environ Sci Pollut Res 22:119–134

    CAS  Google Scholar 

  • Craigie JS (2011) Seaweed extract stimuli in plant science and agriculture. J Appl Phycol 23:371–393

    CAS  Google Scholar 

  • Cruzate GA, Casas R (2012) Extracción y balance de nutrientes en los suelos agrícolas de la Argentina. Informaciones agronómicas de Hispanoamérica 6:7–14

    Google Scholar 

  • De Liñan CC (2015) EcoVad 2015: Productos e insumos para agricultura orgánica. Ediciones Agrotecnicas Sl, p 140

  • Di Rienzo JA, Casanoves F, Balzarini MG, Gonzalez L, Tablada M, Robledo CW (2016) InfoStat. Grupo InfoStat, FCA, Universidad Nacional de Córdoba, Argentina. http://www.infostat.com.ar/ searched on 10 November 2019

  • Dıaz-Zorita M, Grove J (2006) Wheat grain response to nitrogen fertilization and field inoculation with a liquid formulation of Azospirillum brasilense. ASA-CSSA-SSSA Abstracts of International Annual Meetings, Indianapolis, USA. 12–16 November 2006

  • Díaz-Zorita M, Grove JH, Murdock L, Herbeck J, Perfect E (2004) Soil structural disturbance effects on crop yields and soil properties in a no-till production system. Agron J 96:1651–1659

    Google Scholar 

  • Díaz-Zorita M, Fernández-Canigia MV (2009) Field performance of a liquid formulation of Azospirillum brasilense on dryland wheat productivity. Eur J Soil Biol 45:3–11

  • Draget KI, Smidsrød O, Skjåk-Bræk G (2002) Alginates from algae. In: Steinbüchel, A.; De Baets, S.; Vandamme, E. (Eds.) Biopolymers Vol. 6, Polysaccharides II: Polysaccharides from Eukaryotes. Wiley-VCH, Weinheim, pp 215–224

  • Eyras MC, Sar EA (2003) Arribazones estivales en Puerto Madryn, Argentina, como materiales para la obtención de compost. Bol Soc Arg Bot 38:105–111

  • Eyras MC, Defosse GE, Dellatorre F (2008) Seaweed compost as an amendment for horticultural soils in Patagonia, Argentina. Compost Sci Utilization 16:119–124

  • Ferratto J, Grasso R, Longo A, Ortiz Mackinson M, Mondino C (2009) Censo 2008 del Cinturón Hortícola de Rosario. INTA Publicaciones Miscelánea 46:15

    Google Scholar 

  • Godfray HCJ, Beddington JR, Crute IR, Haddad L, Lawrence D, Muir JF, Toulmin C (2010) Food security: the challenge of feeding 9 billion people. Science 327:812–818

    CAS  PubMed  Google Scholar 

  • Gupta V, Kumar M, Brahmbhatt H, Reddy CRK, Seth A, Jha B (2011) Simultaneous determination of different endogenetic plant growth regulators in common green seaweeds using dispersive liquid–liquid microextraction method. Plant Physiol Biochem 49:1259–1263

  • Hallmann CA, Foppen RP, van Turnhout CA, de Kroon H, Jongejans E (2014) Declines in insectivorous birds are associated with high neonicotinoid concentrations. Nature 511:341–343

    CAS  PubMed  Google Scholar 

  • Helman Y, Burdman S, Okon Y (2012) Plant growth promotion by rhizosphere bacteria through direct effects. In: Rosenberg E, Gophna U (eds) Beneficial microorganisms in multicellular life forms. Springer, Berlin, pp 89–103

  • Hernández MI, Chailloux M (2001) La nutrición mineral y la biofertilización en el cultivo del tomate (Lycopersicon esculentum Mill). Temas de Ciencia y Tecnología 15:11–27

    Google Scholar 

  • ISTA, Rules (2016) International seed testing association. ISTA Germination Sec. Chapter 19, UK, pp. 19–41

  • Kahn 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 27:270–279

    Google Scholar 

  • Kastner T, Rivas MJI, Koch W, Nonhebel S (2012) Global changes in diets and the consequences for land requirements for food. Proc Natl Acad Sci U S A 109:6868–6872

    CAS  PubMed  PubMed Central  Google Scholar 

  • Khan W, Rayirath UP, Subramanian S, Jithesh MN, Rayorath P, Hodges DM, Prithiviraj B (2009) Seaweed extracts as biostimulants of plant growth and development. J Plant Growth Regul 28:386–399

  • Krasensky J, Jonak C (2012) Drought, salt, and temperature stress induced metabolic rearrangements and regulatory networks. J Exp Bot 63:1593–1608

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kiseleva AA, Tarachovskaya ER, Shishova MF (2012) Biosynthesis of phytohormones in algae. Russ J Plant Physiol 59:595–610

  • Kurepa J, Shull TE, Smalle JA (2019) Antagonistic activity of auxin and cytokinin in shoot and root organs. Plant Direct 3:e00121

    PubMed  PubMed Central  Google Scholar 

  • Kumar K, Sirasale A, Das D (2013) Use of image analysis tool for the development of light distribution pattern inside the photobioreactor for the algal cultivation. Bioresour Technol 143:88–95

  • Laplaze L, Benkova E, Casimiro I, Maes L, Vanneste S, Swarup R, Offringa R (2007) Cytokinins act directly on lateral root founder cells to inhibit root initiation. Plant Cell 19:3889–3900

    CAS  PubMed  PubMed Central  Google Scholar 

  • Leung DW, Bewley JD (1981) Red-light- and gibberellic-acid-enhanced α-galactosidase activity in germinating lettuce seeds, cv. Grand Rapids: control by the axis. Planta 152:436–441

    CAS  PubMed  Google Scholar 

  • López DBS, Hoyos AMG, Perdomo FAR, Buitrago RRB (2014) Efecto de rizobacterias promotoras de crecimiento vegetal solubilizadoras de fosfato en Lactuca sativa cultivar White Boston. Rev Colomb Biotecnol 16:122–128

    Google Scholar 

  • Mérigout P (2006) Étude du métabolisme de la plante en réponse à l'apport de différents fertilisants et adjuvants culturaux. Influence des phytohormones sur le métabolisme azoté (Doctoral dissertation)

  • 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

    CAS  PubMed  Google Scholar 

  • Perrig D, Boiero ML, Masciarelli OA, Penna C, Ruiz OA, Cassán FD, Luna MV (2007) Plant-growth-promoting compounds produced by two agronomically important strains of Azospirillum brasilense, and implications for inoculant formulation. Appl Microbiol Biot 75:1143–1150

    CAS  Google Scholar 

  • Reddy P, Urban S (2008) Linear and cyclic C18 terpenoids from the southern Australian marine brown alga Cystophora moniliformis. J Nat Prod 71:1441–1446

    CAS  PubMed  Google Scholar 

  • Salinas P (2010) Efecto del ácido salicílico sobre la tolerancia a estrés hídrico en lechuga (Lactuca sativa L.) bajo condiciones de invernadero. MSc Thesis, Querétaro, Mexico 1–51 pp.

  • Sanaa A, Boulila A, Boussaid M, Fadhel NB (2013) Alginic acid and derivatives, new polymers from the endangered Pancratium maritimum L. Ind Crop Prod 44:290–293

    CAS  Google Scholar 

  • Sarabia-Ochoa ME, Avila-Díaz I, Carlos-Gómez A, Salgado-Garciglia R (2010) Callus growth and plant regeneration in Laelia speciosa (Orchidaceae). Lankesteriana Int J Orchidology 10:13–18

    Google Scholar 

  • Sharma SHS, 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

    CAS  Google Scholar 

  • Shukla PS, Shotton K, Norman E, Neily W, Critchley AT, Prithiviraj B (2018) Seaweed extract improve drought tolerance of soybean by regulating stress-response genes. AoB Plants 10(1):plx051

  • Stirk WA, Novák O, Strnad M, Van Staden J (2003) Cytokinins in macroalgae. Plant Growth Reg 41:13–12

    CAS  Google Scholar 

  • Stirk WA, Arthur GD, Lourens AF, Novak 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

    CAS  Google Scholar 

  • Stirk WA, Ördög V, Novák O, Rolčík J, Strnad M, Bálint P (2013) Auxin and cytokinin relationships in 24 microalgal strains. J Phycol 49:459–467

    CAS  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Tarakhovskaya ER, Maslov Yu I, Shishova MF (2007) Phytohormones in algae. Russ J Plant Physiol 4:163–170

    Google Scholar 

  • Ünlükara A, Cemek B, Karaman S, Erşahin S (2008) Response of lettuce (Lactuca sativa var. crispa) to salinity of irrigation water. NZ J Crop Hort Sci 36:265–273

  • Vishal B, Kumar PP (2018) Regulation of seed germination and abiotic stresses by gibberellins and abscisic acid. Front Plant Sci 9:838

  • Yang W, Li X, Li Z, Tong C, Feng L (2015) Understanding low-lipid algae hydrothermal liquefaction characteristics and pathways through hydrothermal liquefaction of algal major components: Crude polysaccharides, crude proteins and their binary mixtures. Bioresour Technol 196:99–108

  • Yabur R, Bashan Y, Hernández-Carmona G (2007) Alginate from the macroalgae Sargassum sinicola as a novel source for microbial immobilization material in wastewater treatment and plant growth promotion. J Appl Phycol 19:43–53

    CAS  Google Scholar 

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Funding

This study was supported by the National Research Council of Argentina (CONICET) to J.I and National Agency for Scientific and Technological Promotion (PICT - START UP) Res. N° 1408/12 to V. L.

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Correspondence to Iparraguirre Julia or Luna Virginia.

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Julia, I., Oscar, M., Analía, L. et al. Biofertilization with Macrocystis pyrifera algae extracts combined with PGPR-enhanced growth in Lactuca sativa seedlings. J Appl Phycol 32, 4361–4371 (2020). https://doi.org/10.1007/s10811-020-02202-4

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