Skip to main content
SpringerLink
Log in

Root morphological and molecular responses induced by microalgae extracts in sugar beet (Beta vulgaris L.)

  • Published:
Journal of Applied Phycology Aims and scope Submit manuscript

Abstract

The characterization of nutrient and biostimulant effects in crops is complex and needs rigorous evaluations. In this study, we evaluated morphological and molecular responses induced by microalgae (Chlorella vulgaris and Scenedesmus quadricauda) extracts in Beta vulgaris L. The two microalgae extracts were firstly characterized by CNS, Fourier transform infrared spectroscopic analysis (FT-IR), and carbon-13 nuclear magnetic resonance (13C NMR). Seedlings were grown in Hoagland’s solution under controlled conditions. After 5 days of growth, 2 mL L−1 (1 mg Corg L−1) and 4 mL L−1 (2 mg Corg L−1) of the two microalgae extracts were added to the Hoagland solution. Roots were sampled 36 h after treatments. Inductively coupled plasma spectrometry (ICP-OES) and nanofluidic real-time PCR (OpenArray system) were used for sample profiling. Fifty-three sugar beet genes putatively involved in sulfate starvation were tested in treated and untreated samples. Root morphological traits were measured by means of a scanner-based image analysis system. Multivariate statistical analysis revealed no significant changes in the ionomic profile of Hoagland’s solutions treated with the two microalgae extracts with respect to that of the untreated solution. At the molecular level, microalgae extract supplies upregulated many of the evaluated genes. Functional categorization revealed these genes to be related to various biological pathways and processes including primary and secondary metabolism and intracellular transport. At the morphological level, the treated seedlings showed significantly higher values for root traits related to soil exploration and nutrient uptake, such as total root length, fine root length (diameter < 0.5 mm), and number of root tips, than the untreated plants. These data indicate that microalgae extracts have biostimulant effects on the expression of root traits and genes related to nutrient acquisition in sugar beet.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Akhter M, Majumdar RD, Fortier-McGill B, Soong R, Liaghati-Mobarhan Y, Simpson M, Arhonditsis G, Schmidt S, Heumann H, Simpson AJ (2016) Identification of aquatically available carbon from algae through solution-state NMR of whole 13C-labelled cells. Anal Bioanal Chem 408:4357–4370

    Article  CAS  PubMed  Google Scholar 

  • Arnon DI, Hoagland DR (1940) Crop production in artificial culture solution and in soils with special reference to factors influencing yields and absorption of inorganic nutrients. Soil Sci 50:463–483

  • Baglieri A, Gennari M, Ioppolo A, Leinweber P, Nègre M (2012) Comparison between the humic acids characteristics of two andisols of different age by: FT-IR and 1 H-NMR spectroscopy and py-FIMS. Geochem Int 50:148–158

    Article  CAS  Google Scholar 

  • Baglieri A, Cadili V, Monterumici CM, Gennari M, Tabasso S, Montoneri E, Nardi S, Negre M (2014) Fertilization of bean plants with tomato plants hydrolysates. Effect on biomass production, chlorophyll content and N assimilation. Sci Hortic 176:194–199

    Article  CAS  Google Scholar 

  • Baglieri A, Sidella S, Barone V, Fragalà F, Silkina A, Nègre M, Gennari M (2016) Cultivating Chlorella vulgaris and Scenedesmus quadricauda microalgae to degrade inorganic compounds and pesticides in water. Environ Sci Pollut Res 23:18165–18174

    Article  CAS  Google Scholar 

  • Beijerinck MW (1890) Culturversuche mit Zoochlorellen, Lichenengonidien und anderen niederen Algen. Bot Ztg 48:1–23

    Google Scholar 

  • Biancardi E, McGrath JM, Panella LW, Lewellen RT, Stevanato P (2010) Sugar beet. In: Bradshaw J (ed) Handbook of plant breeding, Tuber and Root Crops, vol 4. Springer, New York, pp 173–219

    Google Scholar 

  • Billard V, Etienne P, Jannin L, Garnica M, Cruz F, Garcia-Mina JM, Yvin JC, Ourry A (2014) Two biostimulants derived from algae or humic acid induce similar responses in the mineral content and gene expression of winter oilseed rape (Brassica napus L.) J Plant Growth Regul 33:305–316

    Article  CAS  Google Scholar 

  • Borowitzka MA (2013) High-value products from microalgae—their development and commercialisation. J Appl Phycol 25:743–756

    Article  CAS  Google Scholar 

  • Boyer JS (1982) Plant productivity and environment. Science 218:443–448

    Article  CAS  PubMed  Google Scholar 

  • Bulgari R, Cocetta G, Trivellini A, Vernieri P, Ferrante A (2015) Biostimulants and crop responses: a review. Biol Agric Hortic 31:1–17

    Article  Google Scholar 

  • Bumbak F, Cook S, Zachleder V, Hauser S, Kovar K (2011) Best practices in heterotrophic high-cell-density microalgal processes: achievements, potential and possible limitations. Appl Microbiol Biotechnol 91:31

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen SK, Subler S, Edwards CA (2002) Effects of agricultural biostimulants on soil microbial activity and nitrogen dynamics. Appl Soil Ecol 19:249–260

    Article  Google Scholar 

  • Coppens J, Lindeboom R, Muys M, Coessens W, Alloul A, Meerbergen K, Lievens B, Clauwaert P, Boon N, Vlaeminck SE (2016) Nitrification and microalgae cultivation for two-stage biological nutrient valorization from source separated urine. Bioresour Technol 211:41–50

    Article  CAS  PubMed  Google Scholar 

  • Crofcheck C, Xinyi E, Shea A, Montross M, Crocker M, Andrews R (2012) Influence of media composition on the growth rate of Chlorella vulgaris and Scenedesmus acutus utilized for CO2 mitigation. J Biochem Technol 4:589–594

    Google Scholar 

  • Devi MP, Subhash GV, Mohan SV (2012) Heterotrophic cultivation of mixed microalgae for lipid accumulation and wastewater treatment during sequential growth and starvation phases: effect of nutrient supplementation. Renew Energy 43:276–283

    Article  Google Scholar 

  • Di Caprio F, Altimari P, Pagnanelli F (2015) Integrated biomass production and biodegradation of olive mill wastewater by cultivation of Scenedesmus sp. Algal Res 9:306–311

    Article  Google Scholar 

  • du Jardin P (2015) Plant biostimulants: definition, concept, main categories and regulation. Sci Hortic 196:3–14

    Article  Google Scholar 

  • Duygu DY, Udoh AU, Ozer TB, Akbulut A, Erkaya IA, Yildiz K, Guler D (2012) Fourier transform infrared (FTIR) spectroscopy for identification of Chlorella vulgaris Beijerinck 1890 and Scenedesmus obliquus (Turpin) Kützing 1833. Afr J Biotechnol 11:3817–3824

    CAS  Google Scholar 

  • Faheed FA, Abd-El Fattah Z (2008) Effect of Chlorella vulgaris as bio-fertilizer on growth parameters and metabolic aspects of lettuce plant. J Agric Soc Sci 4:165–169

    Google Scholar 

  • Ferreira KN, Iverson TM, Maghlaoui K, Barber J, Iwata S (2004) Architecture of the photosynthetic oxygen-evolving center. Science 303:1831–1838

    Article  CAS  PubMed  Google Scholar 

  • Fierro S, del Pilar S-SM, Copalcua C (2008) Nitrate and phosphate removal by chitosan immobilized Scenedesmus. Bioresour Technol 99:1274–1279

    Article  CAS  PubMed  Google Scholar 

  • Garcia-Gonzalez J, Sommerfeld M (2016) Biofertilizer and biostimulant properties of the microalga Acutodesmus dimorphus. J Appl Phycol 28:1051–1061

  • Huang CZ, Wang SL, Chen L, Lemieux C, Otis C, Turmel M, Liu XQ (1994) The Chlamydomonas chloroplast clpP gene contains translated large insertion sequences and is essential for cell growth. Mol Gen Genet 244:151–159

    Article  CAS  PubMed  Google Scholar 

  • Jones PD, Lister DH, Jaggard KW, Pidgeon JD (2003) Future climate impact on the productivity of sugar beet (Beta vulgaris L.) in Europe. Clim Chang 58:93–108

    Article  Google Scholar 

  • Köhler HR, Triebskorn R (2013) Wildlife ecotoxicology of pesticides: can we track effects to the population level and beyond? Science 341:759–765

    Article  PubMed  Google Scholar 

  • Lopez CVG, Garcia MDCC, Fernandez FGA, Bustos CS, Chisti Y, Sevilla JMF (2010) Protein measurements of microalgal and cynobacterial biomass. Biores Technol 101:7587–7591

  • Lucini L, Rouphael Y, Cardarelli M, Canaguier R, Kumar P, Colla G (2015) The effect of a plant-derived biostimulant on metabolic profiling and crop performance of lettuce grown under saline conditions. Sci Hortic 182:124–133

    Article  CAS  Google Scholar 

  • Makarevičienė V, Skorupskaitė V, Andrulevičiūtė V (2012) Biomass and oil production of green microalgae Scenedesmus sp. using different nutrients and growth. Environ Res Eng Manag 62:5–13

    Google Scholar 

  • Mann JE, Myers J (1968) On pigments, growth and photosynthesis of Phaedactylum tricornutum. J Phycol 4:349–355

    Article  CAS  PubMed  Google Scholar 

  • Metting B, Zimmerman WJ, Crouch IJ, van Staden J (1990) Agronomic uses of seaweed and microalgae. In: Akatsuka I (ed) Introduction to applied phycology. SPB Academic Publishing, The Hague, pp 269–307

    Google Scholar 

  • Miller RH (1990) Soil microbiological inputs for sustainable agricultural systems. In: Edwards CA, Lal R, Madden P, Miller RH, House G (eds) Sustainable agricultural systems. Soil and Water Conservation Society, Ankeny, pp 614–623

    Google Scholar 

  • Nabti E, Jha B, Hartmann A (2016) Impact of seaweeds on agricultural crop production as biofertilizer. Int J Environ Sci Technol 1–16

  • Norton TA, Melkonian M, Andersen RA (1996) Algal biodiversity. Phycologia 35:308–326

    Article  Google Scholar 

  • Olofsson M, Lamela T, Nilsson E, Bergé JP, Del Pino V, Uronen P, Legrand C (2012) Seasonal variation of lipids and fatty acids of the microalgae Nannochloropsis oculata grown in outdoor large-scale photobioreactors. Energies 5:1577–1592

    Article  CAS  Google Scholar 

  • Rocha GS, Pinto FHV, Melão MGG, Lombardi AT (2015) Growing Scenedesmus quadricauda in used culture media: is it viable? J Appl Phycol 27:171–178

    Article  Google Scholar 

  • Safi C, Ursu AV, Laroche C, Zebib B, Merah O, Pontalier PY, Vaca-Garcia C (2014) Aqueous extraction of proteins from microalgae: effect of different cell disruption methods. Algal Res 3:61–65

    Article  Google Scholar 

  • Sanudo-Wilhelmy SA, Gómez-Consarnau L, Suffridge C, Webb EA (2014) The role of B vitamins in marine biogeochemistry. Annu Rev Mar Sci 6:339–367

    Article  Google Scholar 

  • Shaaban MM (2001) Green microalgae water extract as foliar feeding to wheat plants. Pak J Biol Sci 4:628–632

    Article  Google Scholar 

  • Sigee DC, Dean A, Levado E, Tobin MJ (2002) Fourier-transform infrared spectroscopy of Pediastrum duplex: characterization of a micro-population isolated from a eutrophic lake. Eur J Phycol 37:19–26

    Article  Google Scholar 

  • Spolaore P, Joannis-Cassan C, Duran E, Isambert A (2006) Commercial applications of microalgae. J Biosci Bioeng 101:87–96

    Article  CAS  PubMed  Google Scholar 

  • Stanier RY, Kunisawa R, Mandel M, Cohen-Bazire G (1971) Purification and properties of unicellular blue-green algae (order Chroococcales). Bact Rev 35:171

    CAS  PubMed  PubMed Central  Google Scholar 

  • Stevanato P, Trebbi D, Saccomani M (2010) Root traits and yield in sugar beet: identification of AFLP markers associated with root elongation rate. Euphytica 173:289–298

    Article  Google Scholar 

  • Stevanato P, Trebbi D, Bertaggia M, Colombo M, Broccanello C, Concheri G, Saccomani M (2011) Root traits and competitiveness against weeds in sugar beet. Int Sugar J 113:497–501

    Google Scholar 

  • Stevanato P, Fedito P, Trebbi D, Cagnin M, Saccomani M, Cacco G (2015) Effect of sulfate availability on root traits and microRNA395 expression in sugar beet. Biol Plantarum 59:491–496

    Article  CAS  Google Scholar 

  • Vigani M, Parisi C, Rodríguez-Cerezo E, Barbosa MJ, Sijtsma L, Ploeg M, Enzing C (2015) Food and feed products from micro-algae: market opportunities and challenges for the EU. Trends Food Sci Technol 42:81–92

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Agriculture, Food and Environment, University of Catania, Via S. Sofia 98, 95125, Catania, Italy

    V. Barone & A. Baglieri

  2. Department of Agronomy, Food, Natural Resources, Animals and Environment, University of Padova, Viale Università, 16, 35020, Legnaro, PD, Italy

    Piergiorgio Stevanato, C. Broccanello, G. Bertoldo, M. Bertaggia, M. Cagnin, D. Pizzeghello, A. Squartini, S. Nardi & G. Concheri

  3. CREA, Genomic Research Centre, Via S. Protaso 302, 29017, Fiorenzuola d’Arda, PC, Italy

    V. M. C. Moliterni

  4. CREA, Research Centre for Industrial Crops, Via di Corticella 133, 40128, Bologna, Italy

    G. Mandolino

  5. CREA, Research Centre for Plant-Soil Relationships, Via Trieste 23, 34170, Gorizia, Italy

    F. Fornasier

Authors
  1. V. Barone
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. Baglieri
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Piergiorgio Stevanato
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. C. Broccanello
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. G. Bertoldo
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. M. Bertaggia
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. M. Cagnin
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. D. Pizzeghello
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. V. M. C. Moliterni
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. G. Mandolino
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. F. Fornasier
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. A. Squartini
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. S. Nardi
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. G. Concheri
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Piergiorgio Stevanato.

Electronic supplementary material

ESM 1

(XLSX 53 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Barone, V., Baglieri, A., Stevanato, P. et al. Root morphological and molecular responses induced by microalgae extracts in sugar beet (Beta vulgaris L.). J Appl Phycol 30, 1061–1071 (2018). https://doi.org/10.1007/s10811-017-1283-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-017-1283-3

Keywords

Search

Navigation