Next Article in Journal
Exploring the Mediating Role of Knowledge Sharing between Informal Business Networks and Organizational Performance: An Insight into SMEs Internationalization in CEE
Next Article in Special Issue
Characterization of Thymus vulgaris subsp. vulgaris Community by Using a Multidisciplinary Approach: A Case Study from Central Italy
Previous Article in Journal
Natural Treatment Systems and Importance of Social Cost Benefit Analysis in Developing Countries: A Critical Review
Previous Article in Special Issue
Multi-Temporal Evaluation of Quantitative and Phenological Vegetation Dynamics Using Sentinel-2 Images in North Horr (Kenya)
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Sustainability
Volume 14
Issue 7
10.3390/su14073914
sustainability-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Screening on the Presence of Plant Growth Regulators in High Biomass Forming Seaweeds from the Ionian Sea (Mediterranean Sea)

by
Damiano Spagnuolo
1,†,
Valentino Russo
2,†,
Antonio Manghisi
1,
Antonio Di Martino
3,
Marina Morabito
1,*,
Giuseppa Genovese
1 and
Patrizia Trifilò
1
1
Department of Chemical, Biological, Pharmaceutical and Environmental Sciences, University of Messina, Salita Sperone 31, 98166 Messina, Italy
2
South Agro srl, Str. Torre Tresca 2/A, 70124 Bari, Italy
3
Research School of Chemistry & Applied Biomedical Sciences, Tomsk Polytechnic University, Lenin Avenue 43, 63400 Tomsk, Russia
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Sustainability 2022, 14(7), 3914; https://0-doi-org.brum.beds.ac.uk/10.3390/su14073914
Submission received: 9 February 2022 / Revised: 19 March 2022 / Accepted: 23 March 2022 / Published: 25 March 2022
(This article belongs to the Special Issue Green: The Best Way for a Sustainable Planet. How Agriculture, Architecture, Biology, Chemistry, Engineering, Food and Forestry Can Help the Survival of the Earth through Plants)
Versions Notes

Abstract

:
The use of seaweed as plant biostimulants is a solution for sustainable agriculture. The present study aims to quantify and compare the presence of plant growth regulators (PGRs) in four genetically labeled macroalgae growing in the Ionian Sea. Species were selected because they produce abundant biomass, disturbing ecological equilibrium and anthropic activities. We measured the content of gibberellic acid (GA3), kinetin (KN), indoleacetic acid (IAA), abscisic acid (ABA) and indole butyric acid (IBA). The method applied was modified from the literature to obtain simultaneously different PGRs from seaweed biomass in a shorter period of time. Among results, it is notable that Hypnea corona Huisman et Petrocelli (Rhodophyta) showed higher GA3 concentration, while in Spyridia filamentosa (Wulfen) Harvey (Rhodophyta), higher KN, IBA, IAA and ABA contents were recorded. The latter species displayed an interesting profile of PGRs, with an IAA value comparable with that reported in Ascophyllum nodosum (Linnaeus) Le Jolis (Ochrophyta), which is currently used as a source of plant biostimulants in agriculture. Macroalgae thrive abundantly in nutrient-rich environments, such as anthropized coastal areas affecting human economic activities. Consequently, environmental agencies are forced to dredge algal thalli and discard them as waste. Any use of unwanted biomass as an economic product is highly desirable in the perspective of ecosustainable development.

1. Introduction

Increasing drought events, as a consequence of climate change, are causing on a global scale relevant loss in crop yield [1]. Water availability strongly affects plant productivity [2]. Nevertheless, as a likely effect of climate change, an increase in the frequency of extreme events, such as heatwaves, flooding, hurricanes, etc., negatively impacts plant resilience ability, exposing vegetation to higher crop disease and, as a consequence, exacerbating yield reductions [3,4]. Based on alarming forcasts on global warming [5], improving, as much as possible, the resistance and resilience ability as well as the yield of crop plants in such “new” growth conditions is a priority. This challenging task is further needed to meet food demand due to population growth [6]. Optimal mineral nutrition increases plant resilience to different biotic and abiotic stresses, as well as food quality [7]. Nevertheless, chemical fertilization causes high economic and ecological costs [8]. The common practice of improving crop productivity and/or food quality, by using synthetic plant growth regulators (PGRs) in addition increasing management costs, could be toxic for plants and animals, including humans [9,10,11].
Plant biostimulants are products that respond to the requirement for agriculture products that are less dependent on synthetic chemicals and at the same time able to provide greater yields and mitigate the effects of climate change, stimulating plant nutrition processes, the tolerance to abiotic stress and crop quality [12,13,14].
On this view, the use of seaweed is actually a solution for sustainable agriculture because it combines the need to use low-cost but good fertilizers (i.e., it contains minerals) with a source of plant biostimulants. Furthermore, it has the added value of providing a solution to the disposal of unwanted seaweed biomass, which may occur especially in eutrophic environments [15,16,17].
Seaweeds have been used as an organic fertilizer since ancient times [18]. However, since the 1960s, the seaweed industry has received renewed interest because of an increasing number of studies demonstrating the positive effects of using seaweed extracts on crop productivity and food quality [19].
Seaweeds are mainly applied in organic agriculture due to their biodegradable, non-toxic, non-polluting and non-hazardous effects relative to human and animals [20]. In this regard, extracts obtained by macroalgae represent 30% of the market of plant biostimulants in 2013, 40% of which is absorbed by the European market [21]. Early studies aimed to identify mineral content of seaweed extracts [22,23]. By contrast, in the most recent years, greater attention has been given to PGR contents and other organic compounds frequently present in these natural plant biostimulants.
Macroalgae produce huge biomass in nutrient rich environments, which often are dredged and discarded as waste that do not affect human activities. Such biomass could be a promising source of PGRs in the perspective of eco-sustainable development.
A high and increasing number of studies on the physiological roles of phytohormones in terrestrial plants improve our understanding of their effects and interactions on plant growth and productivity. Conversely, the same knowledge is lacking for seaweeds [24]. This gap may negatively impact the advantages of using seaweed extracts on crops. On this view, verifying and quantifying the presence of plant biostimulant products in the algae are prerequisites to any project related to their physiological involvement.
The present study aims to quantify and compare the presence of some PGRs in four different macroalgae growing in the Ionian Sea (Taranto, Italy), i.e., two Rhodophyta (Spyridia filamentosa (Wulfen) Harvey and Hypnea corona Huisman et Petrocelli) and two Chlorophyta (Chaetomorpha linum (O.F. Müller) Kützing and Ulva lacinulata (Kützing) Wittrock). The four algal species were selected because they produce abundant biomass in the collection site, disturbing both ecological equilibrium and anthropic economic activities.
In detail, we measured the content of gibberellic acid (GA3), kinetin (KN) indoleacetic acid (IAA), abscisic acid (ABA) and indole butyric acid (IBA) as the main representatives of PGRs as a screening prerequisite for further tests to evaluate their agronomic effects.

2. Materials and Methods

2.1. Collection of Algae

Samples of Spyridia filamentosa (Wulfen) Harvey, Hypnea corona Huisman et Petrocelli (Rhodophyta), Chaetomorpha linum (O.F. Müller) Kützing and Ulva lacinulata (Kützing) Wittrock (Chlorophyta) were collected from Taranto (Italy, Ionian Sea) (Table 1).
Species names and phylum attributions are in accordance with algaebase.org [25]. All species used in the present investigation have isomorphic life cycles, with alternating gametophytic and sporophytic phases, which thrive in mixed populations and are distinguishable only by fine reproductive aspects by trained experts. In the perspective of potential economic exploitation, we decided to use natural populations and to process mixed haploid and diploid batches.
After collection, samples were immediately washed with seawater to remove possible debris, adhering sand particles and epiphytes and then transported to the laboratory in plastic bags at low temperatures and washed with tap water to remove surface salt. From each sample, a portion was dried in silica gel and stored at −20 °C for DNA barcoding identification, and the remaining portions were dried for 72 h in an oven at 65 °C. Then, the samples were powdered by an electric grinder stored in plastic bags at 4 °C until they were analyzed.
DNA barcoding identification was performed according to protocols described in Miladi et al. [26] and Manghisi et al. [27]. Selected barcodes were COI-5P for Rhodophyta, tufA for U. lacinulata and LSU D2/D3 for C. linum [28]. DNA sequencing reactions were performed by an external company (Macrogen Europe, Amsterdam, The Netherlands). Forward and reverse sequence reads were assembled with the software ChromasPro (v. 1.41, Technelysium Pty Ltd., South Brisbane, QLD, Australia), and species attributions were performed by the identification engine in BOLD Systems (www.boldsystems.org, accessed on 6 January 2022) and the BLAST tool at the National Center for Biotechnology Information (Bethesda, MD, USA, blast.ncbi.nlm.nih.gov/Blast.cgi, accessed on 6 January 2022).

2.2. Preparation of Standard Solutions

Standard substances (purity > 98%) of gibberellic acid (GA3), indoleacetic acid (IAA), abscisic acid (ABA) and indole butyric acid (IBA) were purchased from OlChemIm s.r.o. (Olomouc, Czech Republic). Kinetin (KN) was purchased from Sigma Aldrich (St. Louis, MO, USA). Analytical HPLC-grade methanol (MeOH) and glacial acetic acid were obtained from Merck (Darmstadt, Germany). Distilled water was deionized in an Elga Veolia Purelab ultra-pure water system (High Wycombe, UK).
The standard compounds were dissolved in MeOH:H2O (50:50 v/v) at a stock concentration of 1000 µg/mL and stored at 4 °C. Working standard solutions were obtained by diluting them with MeOH: H2O (50:50 v/v) prior to use. All solvents were ultrasonified for 30 min (Sonica, Soltec, Japan) before use.

2.3. Sample Preparation

An aliquot (0.5 g) of each powdered sample was infused in a 4 mL MeOH:H2O solution (80:20 v/v) with 1 mmol/L of citric acid as the antioxidant. Solutions were sonicated for 15 min and placed in infusion for 3 days at 4 °C. The samples were transferred in 15 mL vials and centrifuged at 7000 rpm for 30 min at 4 °C. Then, the supernatants were collected and 1 mL of MeOH was added. After 1 h, the samples were centrifuged for an additional 15 min at 7000 rpm at 4 °C, filtered with 0.2 μm in diameter syringe filter and diluted with ultra-pure water (1:5). No purification steps were performed to speed up the protocol.

2.4. HPLC Set-Up

Chromatographic runs were carried out on a Beckman Coulter 126 binary pumps HPLC system with the detector Beckman Coulter 166 UV/VIS system (Brea, CA, USA). Karat 32 ver. 8.0 software was employed for instrument control and data acquisition. Data analyses were accomplished by in-house Octave script. Starlab scientific (Xi’an, China) XChroma universal-C18 column (5 μm, 120 Å, 4.6 × 250 mm) was used as the separation channel.
The mobile phase was composed of MeOH:H2O (70:30, v/v), both acidified with acetic acid 0.5%, and the flow rate was 1.0 mL/min. The UV/Vis detector was set to 280 nm. The injection volume was 20 μL for each analysis using IDEX corp. Rheodyne 7125 valve (Lake Forest, CA, USA). All samples were analyzed in 3 repetitions. The results are presented as mean ± standard deviation.

2.5. Method Validation

The HPLC method was validated by the evaluation of the variation of retention times and peak area for analytes, performing calibration curves, limit of detection (LOD), limit of quantification (LOQ) and accuracy.
The analytical performances and the calibration curve are summarized in Table 2. The limit of detection (LOD), obtained by evaluation of signal to noise ratio, ranges between 5 µg/mL for GA3 and 0.2 µg/mL for KN, IAA and ABA. The calibration curves showed a linear trend, and the reliability of measurements were confirmed by intra- and inter-day analysis, and the standard deviations are less than 2%. The retention time of the standards was 4.6, 5.3, 7.5, 9.2 and 12.3 min for GA3, KN, IAA, ABA and IBA, respectively.
The standard solutions were found to be stable for months and stored at −25 °C; any variations on the value of response function were observed in the chromatogram recorded.

3. Results and Discussion

Seaweeds are known to produce plant growth regulators (PGRs), similarly to land plants [29]. Their effects include the response to various developmental and physiological processes and provide support to overcome abiotic and biotic stresses [30]. Recently, the attention of researchers pointed to the detection and quantification of different PGRs in seaweeds with the aim of agronomic applications [30].
The method applied in the present work was modified from Gupta et al. [31] in order to obtain simultaneously different PGRs from seaweed biomass but in a shorter period time. The separation of PGRs was performed by simplifying the extraction process, with a complete run performed in 18 min. The most significant modification was the lack of purification of the extracts in order to make the protocol faster and cheaper in the framework of applicative exploitation.
Overall, the Rhodophyta species analyzed in the present work showed a higher content of PGRs than the analyzed Chlorophyta (Table 3, HPLC chromatograms in 1
Supplementary Materials). These data, however, cannot be drawn as a general conclusion that Rhodophyta as a whole have a higher content of PGRs than Chlorophyta, as the present results regard a limited taxonomic span. More research is needed to achieve a general framework.
In detail, Hypnea corona Huisman et Petrocelli showed higher GA3 concentration, while in Spyridia filamentosa (Wulfen) Harvey, higher KN, IBA, IAA and ABA contents were recorded. The latter species displayed an interesting profile of PGRs, with an IAA value comparable with that reported in Ascophyllum nodosum (Linnaeus) Le Jolis (Ochrophyta) [32], which is currently used as a source of plant biostimulants in agriculture [33,34,35,36].
In Chaetomorpha linum (O.F. Müller) Kützing, no IAA, IBA and ABA were present. Ulva lacinulata (Kützing) Wittrock showed a concentration of KN and ABA similar to H. corona but lower than S. filamentosa and no GA3 content.
The presence of PGRs in seaweeds has been already reported in several studies [31,37,38]. However, the occurrence and the roles of these molecules on seaweeds physiology are still not clear [39,40,41].
Nevertheless, the literature data strongly suggest that PGRs in seaweeds are not a mere result of some metabolic processes but may have specific physiological relevance on their growth as a response to environmental stimuli [37]. In accordance, it has been shown that changes in PGR concentration occur in response to abiotic stress in different seaweed species [38,39,42]. Moreover, different studies highlighted similar roles of PGRs in terrestrial plants versus seaweeds species. As an example, IAA affects the embryo development of Brassica juncea (Linnaeus) Czernajew (Magnoliophyta) as well as of Fucus distichus Linnaeus (Ochrophyta) germlings [43,44]. Similarly to terrestrial plants, ethylene promoted chlorophyll degradation in Ulva intestinalis Linnaeus [45] and affected the maturation of reproductive structures in Pterocladiella capillacea (S.G. Gmelin) Bornet (Rhodophyta) [46]. ABA, a phytohormone generally associated to several stress responses in terrestrial plants [47,48], is involved in the coping oxidative stress of intertidal seaweed species [49]. Stirk et al. [50] recorded higher ABA content in Ulva lactuca Linnaeus (as Ulva fasciata Delile) versus Dictyota humifusa Hörnig, Schnetter et Coppejans (Ochrophyta), likely as a result of a stronger environmental stress. Brassinosteroided-mediated ABA synthesis occurred in response to thermal stress in brassicacean Chorispora bungeana Fischer et C.A. Mey (Magnoliophyta) as well as in green alga Chlorella vulgaris Beijerinck (Chlorophyta) [51,52]. Furthermore, in terrestrial plants and frequently but not exclusively in response to biotic and abiotic stresses, ABA plays a key role in different developmental processes, including seed germination, root and shoot development and photosynthesis inhibition [53,54,55,56,57,58]. Likewise, ABA impacted plant growth in Laminaria J.V. Lamouroux spp. (Ochrophyta), inhibited the growth of sporophyte, but it stimulated sorus formation in Saccharina japonica (Areschoug) C.E. Lane, C. Mayes, Druehl et G.W. Saunders (as Laminaria japonica Areschoug) and constrained the photosynthesis of Fucus vesiculosus Linnaeus embryos [59,60,61].

4. Conclusions

In the present study, PGRs were recorded in four macroalgal species belonging to Rhodophyta and Chlorophyta. Their physiological role was not investigated, which was out of the scope of our research. However, it could be speculated that PGRs in algae affect their growth and response to environmental factors, similarly to terrestrial plants in accordance with the literature (see above). Even if understanding the physiological functions of PGRs in algae is very interesting for fundamental physiological research, it is not essential for seaweed industrial exploitation, including the use of algal biomass as a source of plant biostimulants in the framework of sustainable agriculture. Further studies are needed to evaluate the effective applications of algal PGRs in agriculture, testing both protocols to produce algal plant biostimulants and application strategies on the growth of agronomic species in the field.
The novelty of the present research relies not only in reporting the presence of PGRs in algae as a whole but also on suggesting the use of unwanted biomasses and testing them for the presence of PGRs for the purpose of their exploitation in agriculture. Moreover, due to the large genetic and consequently metabolic diversity of macroalgae, the aim is to investigate more taxa as a source of PGRs from diverse geographical sites and add useful data in the knowledge of algal physiology.
Macroalgal identification at the species level is a complex task, which need the involvement of skilled taxonomists. In the perspective of industrial exploitation, we recommended that genetic labeling should be used. The official DNA barcode is a prompt and effective tool, which proved to be useful in applied research, e.g., [62,63,64].
Macroalgae thrive abundantly in nutrient rich environments, such as anthropized coastal areas. Such biomass affects human economic activities, disturbing navigation, aquaculture and tourism, as examples. As a consequence, environmental agencies are forced to dredge algal thalli and discard them as a waste. Any use of unwanted biomass as an economic product is highly desirable in the perspective of eco-sustainable development.

Supplementary Materials

The following supporting information can be downloaded at: https://0-www-mdpi-com.brum.beds.ac.uk/article/10.3390/su14073914/s1, Figure S1: Hypnea corona Huisman et Petrocelli, HPLC chromatogram. Minutes reported in decimal divisions; Figure S2: Spyridia filamentosa (Wulfen) Harvey, HPLC chromatogram. Minutes reported in decimal divisions; Figure S3: Chaetomorpha linum (O.F. Müller) Kützing, HPLC chromatogram. Minutes reported in decimal divisions; Figure S4: Ulva lacinulata (Kützing) Wittrock, HPLC chromatogram. Minutes reported in decimal divisions.

Author Contributions

Conceptualization, D.S., V.R. and P.T.; methodology, D.S., V.R., A.M. and A.D.M.; writing—original draft preparation, D.S., V.R., A.M. and A.D.M.; writing—review and editing, M.M., G.G. and P.T.; funding acquisition, V.R., M.M., G.G. and P.T. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by South Agro srl (Ordinary Operating Funds 2020), FFABR2017-UniMe (Italian Ministry of University and Research), to M.M. and P.T., FFABR2019-UniMe (Italian Ministry of University and Research) to G.G.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Lesk, C.; Rowhani, P.; Ramankutty, N. Influence of Extreme Weather Disasters on Global Crop Production. Nature 2016, 529, 84–87. [Google Scholar] [CrossRef] [PubMed]
  2. Mancosu, N.; Snyder, R.; Kyriakakis, G.; Spano, D. Water Scarcity and Future Challenges for Food Production. Water 2015, 7, 975–992. [Google Scholar] [CrossRef]
  3. Vogel, E.; Donat, M.G.; Alexander, L.V.; Meinshausen, M.; Ray, D.K.; Karoly, D.; Meinshausen, N.; Frieler, K. The Effects of Climate Extremes on Global Agricultural Yields. Environ. Res. Lett. 2019, 14, 054010. [Google Scholar] [CrossRef]
  4. del Río, S.; Canas, R.; Cano, E.; Cano-Ortiz, A.; Musarella, C.; Pinto-Gomes, C.; Penas, A. Modelling the Impacts of Climate Change on Habitat Suitability and Vulnerability in Deciduous Forests in Spain. Ecol. Indic. 2021, 131, 108202. [Google Scholar] [CrossRef]
  5. Masson-Delmotte, V.; Zhai, P.; Pörtner, H.-O.; Roberts, D.; Skea, J.; Shukla, P.R.; Pirani, A.; Moufouma-Okia, W.; Péan, C.; Pidcock, R.; et al. (Eds.) An IPCC Special Report on the Impacts of Global Warming of 1.5 °C above Pre-Industrial Levels and Related Global Greenhouse Gas Emission Pathways, in the Context of Strengthening the Global Response to the Threat of Climate Change, Sustainable Development, and Efforts to Eradicate Poverty; IPCC: Geneva, Switzerland, 2019. [Google Scholar]
  6. Godfray, H.C.J.; Beddington, J.R.; Crute, I.R.; Haddad, L.; Lawrence, D.; Muir, J.F.; Pretty, J.; Robinson, S.; Thomas, S.M.; Toulmin, C. Food Security: The Challenge of Feeding 9 Billion People. Science 2010, 327, 812–818. [Google Scholar] [CrossRef] [Green Version]
  7. Sarwar, M.; Saleem, M.F.; Ullah, N.; Ali, S.; Rizwan, M.; Shahid, M.R.; Alyemeni, M.N.; Alamri, S.A.; Ahmad, P. Role of Mineral Nutrition in Alleviation of Heat Stress in Cotton Plants Grown in Glasshouse and Field Conditions. Sci. Rep. 2019, 9, 13022. [Google Scholar] [CrossRef] [Green Version]
  8. European Commission. Fertilisers in the EU Prices, Trade and Use; European Commission: Brussels, Belgium, 2019. [Google Scholar]
  9. Hąc-Wydro, K.; Flasiński, M. The Studies on the Toxicity Mechanism of Environmentally Hazardous Natural (IAA) and Synthetic (NAA) Auxin—The Experiments on Model Arabidopsis thaliana and Rat Liver Plasma Membranes. Colloids Surf. B 2015, 130, 53–60. [Google Scholar] [CrossRef]
  10. Kocaman, A.Y.; Güven, B. In Vitro Genotoxicity Assessment of the Synthetic Plant Growth Regulator, 1-Naphthaleneacetamide. Cytotechnology 2016, 68, 947–956. [Google Scholar] [CrossRef] [Green Version]
  11. Narasimhan, M.; Gallei, M.; Tan, S.; Johnson, A.; Verstraeten, I.; Li, L.; Rodriguez, L.; Han, H.; Himschoot, E.; Wang, R.; et al. Corrigendum to: Systematic Analysis of Specific and Nonspecific Auxin Effects on Endocytosis and Trafficking. Plant Physiol. 2021, 187, 1027. [Google Scholar] [CrossRef]
  12. du Jardin, P. Plant Biostimulants: Definition, Concept, Main Categories and Regulation. Sci. Hortic. 2015, 196, 3–14. [Google Scholar] [CrossRef] [Green Version]
  13. Piñar Fuentes, J.C.; Leiva, F.; Cano-Ortiz, A.; Musarella, C.M.; Quinto-Canas, R.; Pinto-Gomes, C.J.; Cano, E. Impact of Grass Cover Management with Herbicides on Biodiversity, Soil Cover and Humidity in Olive Groves in the Southern Iberian. Agronomy 2021, 11, 412. [Google Scholar] [CrossRef]
  14. Cano-Ortiz, A.; Musarella, C.M.; Piñar Fuentes, J.C.; Pinto Gomes, C.J.; Quinto-Canas, R.; del Río, S.; Cano, E. Indicative Value of the Dominant Plant Species for a Rapid Evaluation of the Nutritional Value of Soils. Agronomy 2020, 11, 1. [Google Scholar] [CrossRef]
  15. Spagnuolo, D.; Prisa, D. Evaluation of Growth Parameters on Carpobrotus edulis, Kalanchoe daigremontiana and Kalanchoe tubiflora in Relation to Different Seaweed Liquid Fertilizer (SLF) as a Biostimulant. Int. J. Curr. Microbiol. App. Sci. 2021, 10, 67–76. [Google Scholar] [CrossRef]
  16. Hassan, S.M.; Ashour, M.; Soliman, A.A.F.; Hassanien, H.A.; Alsanie, W.F.; Gaber, A.; Elshobary, M.E. The Potential of a New Commercial Seaweed Extract in Stimulating Morpho-Agronomic and Bioactive Properties of Eruca vesicaria (L.) Cav. Sustainability 2021, 13, 4485. [Google Scholar] [CrossRef]
  17. Ali, O.; Ramsubhag, A.; Jayaraman, J. Biostimulant Properties of Seaweed Extracts in Plants: Implications towards Sustainable Crop Production. Plants 2021, 10, 531. [Google Scholar] [CrossRef]
  18. Pereira, L.; Bahcevandziev, K.; Joshi, N.H. Seaweeds as Plant Fertilizer, Agricultural Biostimulants and Animal Fodder; CRC Press: Boca Raton, FL, USA, 2020; ISBN 978-1-138-59706-8. [Google Scholar]
  19. Blunden, G.; Challen, S.B.; Woods, D.L. Seaweed Extracts as Fertilisers. J. Sci. Food Agric. 1968, 19, 289–293. [Google Scholar] [CrossRef]
  20. Ghosh, A.; Vijay Anand, K.G.; Seth, A. Life Cycle Impact Assessment of Seaweed Based Biostimulant Production from Onshore Cultivated Kappaphycus alvarezii (Doty) Doty Ex Silva—Is It Environmentally Sustainable? Algal Res. 2015, 12, 513–521. [Google Scholar] [CrossRef]
  21. EBIC European Biostimulant Industry Council. 2013. Available online: http://www.biostimulants.eu (accessed on 2 February 2022).
  22. Soares, C.; Švarc-Gajić, J.; Oliva-Teles, M.T.; Pinto, E.; Nastić, N.; Savić, S.; Almeida, A.; Delerue-Matos, C. Mineral Composition of Subcritical Water Extracts of Saccorhiza polyschides, a Brown Seaweed Used as Fertilizer in the North of Portugal. J. Mar. Sci. Eng. 2020, 8, 244. [Google Scholar] [CrossRef] [Green Version]
  23. Ertani, A.; Francioso, O.; Tinti, A.; Schiavon, M.; Pizzeghello, D.; Nardi, S. Evaluation of Seaweed Extracts From Laminaria and Ascophyllum nodosum spp. as Biostimulants in Zea mays L. Using a Combination of Chemical, Biochemical and Morphological Approaches. Front. Plant Sci. 2018, 9, 428. [Google Scholar] [CrossRef]
  24. Mori, I.C.; Ikeda, Y.; Matsuura, T.; Hirayama, T.; Mikami, K. Phytohormones in Red Seaweeds: A Technical Review of Methods for Analysis and a Consideration of Genomic Data. Bot. Mar. 2017, 60, 153–170. [Google Scholar] [CrossRef]
  25. Guiry, M.D.; Guiry, G.M. AlgaeBase. World-Wide Electronic Publication, National University of Ireland, Galway. Available online: https://www.algaebase.org (accessed on 8 March 2022).
  26. Miladi, R.; Manghisi, A.; Armeli Minicante, S.; Genovese, G.; Abdelkafi, S.; Morabito, M. A DNA Barcoding Survey of Ulva (Chlorophyta) in Tunisia and Italy Reveals the Presence of the Overlooked Alien U. ohnoi. Cryptogam. Algol. 2018, 39, 85–107. [Google Scholar] [CrossRef]
  27. Manghisi, A.; Miladi, R.; Minicante, S.A.; Genovese, G.; Gall, L.L.; Abdelkafi, S.; Saunders, G.W.; Morabito, M. DNA Barcoding Sheds Light on Novel Records in the Tunisian Red Algal Flora. Cryptogam. Algol. 2019, 40, 5. [Google Scholar] [CrossRef]
  28. Saunders, G.W.; McDevit, D.C. Methods for DNA Barcoding Photosynthetic Protists Emphasizing the Macroalgae and Diatoms. In DNA Barcodes; Methods in Molecular BiologyTM; Kress, W.J., Erickson, D.L., Eds.; Humana Press: Totowa, NJ, USA, 2012; Volume 858, pp. 207–222. ISBN 978-1-61779-590-9. [Google Scholar]
  29. Davies, P. Plant Hormones: Physiology, Biochemistry and Molecular Biology; Springer: Dordrecht, The Netherlands, 2013; ISBN 978-94-011-0473-9. [Google Scholar]
  30. Verma, V.; Ravindran, P.; Kumar, P.P. Plant Hormone-Mediated Regulation of Stress Responses. BMC Plant Biol 2016, 16, 86. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  31. Gupta, V.; Kumar, M.; Brahmbhatt, H.; Reddy, C.R.K.; Seth, A.; Jha, B. Simultaneous Determination of Different Endogenetic Plant Growth Regulators in Common Green Seaweeds Using Dispersive Liquid–Liquid Microextraction Method. Plant Physiol. Bioch. 2011, 49, 1259–1263. [Google Scholar] [CrossRef] [PubMed]
  32. Sanderson, K.J.; Jameson, P.E.; Zabkiewicz, J.A. Auxin in a Seaweed Extract: Identification and Quantitation of Indole-3-Acetic Acid by Gas Chromatography-Mass Spectrometry. J. Plant Physiol. 1987, 129, 363–367. [Google Scholar] [CrossRef]
  33. Mattner, S.W.; Milinkovic, M.; Arioli, T. Increased Growth Response of Strawberry Roots to a Commercial Extract from Durvillaea potatorum and Ascophyllum nodosum. J. Appl. Phyco. 2018, 30, 2943–2951. [Google Scholar] [CrossRef] [Green Version]
  34. Fan, D.; Hodges, D.M.; Critchley, A.T.; Prithiviraj, B. A Commercial Extract of Brown Macroalga (Ascophyllum nodosum) Affects Yield and the Nutritional Quality of Spinach In Vitro. Commun. Soil Sci. Plan. 2013, 44, 1873–1884. [Google Scholar] [CrossRef]
  35. Shukla, P.S.; Borza, T.; Critchley, A.T.; Prithiviraj, B. Seaweed-Based Compounds and Products for Sustainable Protection against Plant Pathogens. Mar. Drugs 2021, 19, 59. [Google Scholar] [CrossRef]
  36. EL Boukhari, M.E.M.; Barakate, M.; Bouhia, Y.; Lyamlouli, K. Trends in Seaweed Extract Based Biostimulants: Manufacturing Process and Beneficial Effect on Soil-Plant Systems. Plants 2020, 9, 359. [Google Scholar] [CrossRef] [Green Version]
  37. Shoubaky, G.A.E.; Salem, E.A. Effect of Abiotic Stress on Endogenous Phytohormones Profile in Some Seaweeds. IJPPR 2016, 8, 11. [Google Scholar]
  38. Yalçın, S.; Okudan, E.Ş.; Karakaş, Ö.; Önem, A.N. Determination of Major Phytohormones in Fourteen Different Seaweeds Utilizing SPE–LC–MS/MS. J. Chromatogr. Sci. 2020, 58, 98–108. [Google Scholar] [CrossRef] [PubMed]
  39. Tarakhovskaya, E.R.; Maslov, Y.I.; Shishova, M.F. Phytohormones in Algae. Russ. J. Plant Physiol. 2007, 54, 163–170. [Google Scholar] [CrossRef]
  40. Khan, W.; Rayirath, U.P.; Subramanian, S.; Jithesh, M.N.; Rayorath, P.; Hodges, D.M.; Critchley, A.T.; Craigie, J.S.; Norrie, J.; Prithiviraj, B. Seaweed Extracts as Biostimulants of Plant Growth and Development. J. Plant Growth Regul. 2009, 28, 386–399. [Google Scholar] [CrossRef]
  41. Stirk, W.A.; Van Staden, J. Plant Growth Regulators in Seaweeds. In Advances in Botanical Research; Elsevier: Amsterdam, The Netherlands, 2014; Volume 71, pp. 125–159. ISBN 978-0-12-408062-1. [Google Scholar]
  42. Benítez García, I.; Dueñas Ledezma, A.K.; Martínez Montaño, E.; Salazar Leyva, J.A.; Carrera, E.; Osuna Ruiz, I. Identification and Quantification of Plant Growth Regulators and Antioxidant Compounds in Aqueous Extracts of Padina durvillaei and Ulva lactuca. Agronomy 2020, 10, 866. [Google Scholar] [CrossRef]
  43. Hadfi, K.; Speth, V.; Neuhaus, G. Auxin-Induced Developmental Patterns in Brassica juncea Embryos. Development 1998, 125, 879–887. [Google Scholar] [CrossRef]
  44. Basu, S.; Sun, H.; Brian, L.; Quatrano, R.L.; Muday, G.K. Early Embryo Development in Fucus distichus Is Auxin Sensitive. Plant Physiol. 2002, 130, 292–302. [Google Scholar] [CrossRef] [Green Version]
  45. Plettner, I.; Steinke, M.; Malin, G. Ethene (Ethylene) Production in the Marine Macroalga Ulva (Enteromorpha) intestinalis L. (Chlorophyta, Ulvophyceae): Effect of Light-Stress and Co-Production with Dimethyl Sulphide. Plant Cell. Environ. 2005, 28, 1136–1145. [Google Scholar] [CrossRef]
  46. Garcia-Jimenez, P.; Montero-Fernández, M.; Robaina, R.R. Analysis of Ethylene-Induced Gene Regulation during Carposporogenesis in the Red Seaweed Grateloupia imbricata (Rhodophyta). J. Phycol. 2018, 54, 681–689. [Google Scholar] [CrossRef]
  47. Raghavendra, A.S.; Gonugunta, V.K.; Christmann, A.; Grill, E. ABA Perception and Signalling. Trends Plant Sci. 2010, 15, 395–401. [Google Scholar] [CrossRef]
  48. Yoshida, T.; Mogami, J.; Yamaguchi-Shinozaki, K. ABA-Dependent and ABA-Independent Signaling in Response to Osmotic Stress in Plants. Curr. Opin. Plant Biol. 2014, 21, 133–139. [Google Scholar] [CrossRef]
  49. Guajardo, E.; Correa, J.A.; Contreras-Porcia, L. Role of Abscisic Acid (ABA) in Activating Antioxidant Tolerance Responses to Desiccation Stress in Intertidal Seaweed Species. Planta 2016, 243, 767–781. [Google Scholar] [CrossRef] [PubMed]
  50. Stirk, W.A.; Novák, O.; Hradecká, V.; Pĕnčík, A.; Rolčík, J.; Strnad, M.; Van Staden, J. Endogenous Cytokinins, Auxins and Abscisic Acid in Ulva fasciata (Chlorophyta) and Dictyota humifusa (Phaeophyta): Towards Understanding Their Biosynthesis and Homoeostasis. Eur. J. Phycol. 2009, 44, 231–240. [Google Scholar] [CrossRef] [Green Version]
  51. Bajguz, A.; Hayat, S. Effects of Brassinosteroids on the Plant Responses to Environmental Stresses. Plant Physiol. Bioch. 2009, 47, 1–8. [Google Scholar] [CrossRef] [PubMed]
  52. Liu, Y.; Jiang, H.; Zhao, Z.; An, L. Abscisic Acid Is Involved in Brassinosteroids-Induced Chilling Tolerance in the Suspension Cultured Cells from Chorispora bungeana. J. Plant Physiol. 2011, 168, 853–862. [Google Scholar] [CrossRef] [PubMed]
  53. Terashima, I.; Noguchi, K.; Itoh-Nemoto, T.; Park, Y.-M.; Kuhn, A.; Tanaka, K. The Cause of PSI Photoinhibition at Low Temperatures in Leaves of Cucumis sativus, a Chilling-Sensitive Plant. Physiol. Plant. 1998, 103, 295–303. [Google Scholar] [CrossRef]
  54. Sharp, R.E.; LeNoble, M.E. ABA, Ethylene and the Control of Shoot and Root Growth under Water Stress. J. Exp. Bot. 2002, 53, 33–37. [Google Scholar] [CrossRef]
  55. Finkelstein, R. Abscisic Acid Synthesis and Response. Arab. Book 2013, 11, e0166. [Google Scholar] [CrossRef] [Green Version]
  56. Chen, C.; Twito, S.; Miller, G. New Cross Talk between ROS, ABA and Auxin Controlling Seed Maturation and Germination Unraveled in APX6 Deficient Arabidopsis Seeds. Plant Signal. Behav. 2014, 9, e976489. [Google Scholar] [CrossRef] [Green Version]
  57. Luo, X.; Chen, Z.; Gao, J.; Gong, Z. Abscisic Acid Inhibits Root Growth in Arabidopsis through Ethylene Biosynthesis. Plant J. 2014, 79, 44–55. [Google Scholar] [CrossRef]
  58. Wang, Q.; Wang, L.; Chandrasekaran, U.; Luo, X.; Zheng, C.; Shu, K. ABA Biosynthesis and Signaling Cascades Under Hypoxia Stress. Front. Plant Sci. 2021, 12, 661228. [Google Scholar] [CrossRef]
  59. Schaffelke, B. Abscisic Acid in Sporophytes of Three Laminaria Species (Phaeophyta). J. Plant Physiol. 1995, 146, 453–458. [Google Scholar] [CrossRef]
  60. Nimura, K.; Mizuta, H. Inducible Effects of Abscisic Acid on Sporophyte Discs from Laminaria japonica Areschoug (Laminariales, Phaeophyceae). J. Appl. Phycol. 2002, 14, 159–163. [Google Scholar] [CrossRef]
  61. Tarakhovskaya, E.R.; Kang, E.J.; Kim, K.Y.; Garbary, D.J. Influence of Phytohormones on Morphology and Chlorophyll a Fluorescence Parameters in Embryos of Fucus vesiculosus L. (Phaeophyceae). Russ. J. Plant Physiol. 2013, 60, 176–183. [Google Scholar] [CrossRef]
  62. Armeli Minicante, S.; Michelet, S.; Bruno, F.; Castelli, G.; Vitale, F.; Sfriso, A.; Morabito, M.; Genovese, G. Bioactivity of Phycocolloids against the Mediterranean Protozoan Leishmania infantum: An Inceptive Study. Sustainability 2016, 8, 1131. [Google Scholar] [CrossRef] [Green Version]
  63. Zammuto, V.; Rizzo, M.G.; Spanò, A.; Spagnuolo, D.; Di Martino, A.; Morabito, M.; Manghisi, A.; Genovese, G.; Guglielmino, S.; Calabrese, G.; et al. Effects of crude polysaccharides from marine macroalgae on the adhesion and biofilm formation of Pseudomonas aeruginosa and Staphylococcus aureus. Algal Res. 2022, 63, 102646. [Google Scholar] [CrossRef]
  64. Zammuto, V.; Rizzo, M.G.; Spanò, A.; Genovese, G.; Morabito, M.; Spagnuolo, D.; Capparucci, F.; Gervasi, C.; Smeriglio, A.; Trombetta, D.; et al. In vitro evaluation of antibiofilm activity of crude extracts from macroalgae against pathogens relevant in aquaculture. Aquaculture 2022, 549, 737729. [Google Scholar] [CrossRef]
Table
Table 1. List of the algal samples used in this study.
Table 1. List of the algal samples used in this study.
SpeciesVoucher ID
RhodophytaHypnea corona Huisman et PetrocelliPhL705
Spyridia filamentosa (Wulfen) HarveyPhL706
ChlorophytaChaetomorpha linum (O.F. Müller) KützingPhL707
Ulvalacinulata (Kützing) WittrockPhL708
Table
Table 2. Analytical performance data for major endogenetic plant growth regulators. R2: correlation coefficient. LOD: limit of detection.
Table 2. Analytical performance data for major endogenetic plant growth regulators. R2: correlation coefficient. LOD: limit of detection.
AnalyteRange (µg/mL)EquationsR2LOD (µg/mL)Degree of Freedom
GA310–1000y = 0.0433x + 0.00130.989656
KN0.1–10y = 3.9094x − 0.00080.99370.26
IAA0.1–10y = 0.5829x + 0.00060.99670.26
ABA0.1–10y = 1.8133x − 0.00040.99850.26
IBA0.1–10y = 0.4685x + 0.00070.99651.86
Table
Table 3. Gibberellic acid (GA3), kinetin (KN) indoleacetic acid (IAA), abscisic acid (ABA) and indole butyric acid (IBA) contents as estimated by HPLC-UV in extracts of the four investigated seaweed extracts. Values are presented as means of three measurements with standard deviations. LOD: limit of detection. LOQ: limit of quantification.
Table 3. Gibberellic acid (GA3), kinetin (KN) indoleacetic acid (IAA), abscisic acid (ABA) and indole butyric acid (IBA) contents as estimated by HPLC-UV in extracts of the four investigated seaweed extracts. Values are presented as means of three measurements with standard deviations. LOD: limit of detection. LOQ: limit of quantification.
SpeciesGA3
(µg/mL)		KN (µg/mL)IAA (µg/mL)ABA (µg/mL)IBA (µg/mL)
Hypneacorona Huisman et Petrocelli1038.00 ± 2.000.57 ± 0.076.70 ± 0.301.10 ± 0.40LOQ
Spryridia filamentosa (Wulfen) Harvey6.30 ± 0.101.70 ± 0.2063.60 ± 0.508.40 ± 0.9017.90 ± 0.00
Chaetomorpha linum (O.F. Müller) Kützing5.40 ± 0.400.31 ± 0.05LOD0LOQ
Ulvalacinulata (Kützing) Wittrock00.48 ± 0.062.30 ± 0.100.72 ± 0.02LOQ
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Spagnuolo, D.; Russo, V.; Manghisi, A.; Di Martino, A.; Morabito, M.; Genovese, G.; Trifilò, P. Screening on the Presence of Plant Growth Regulators in High Biomass Forming Seaweeds from the Ionian Sea (Mediterranean Sea). Sustainability 2022, 14, 3914. https://0-doi-org.brum.beds.ac.uk/10.3390/su14073914

AMA Style

Spagnuolo D, Russo V, Manghisi A, Di Martino A, Morabito M, Genovese G, Trifilò P. Screening on the Presence of Plant Growth Regulators in High Biomass Forming Seaweeds from the Ionian Sea (Mediterranean Sea). Sustainability. 2022; 14(7):3914. https://0-doi-org.brum.beds.ac.uk/10.3390/su14073914

Chicago/Turabian Style

Spagnuolo, Damiano, Valentino Russo, Antonio Manghisi, Antonio Di Martino, Marina Morabito, Giuseppa Genovese, and Patrizia Trifilò. 2022. "Screening on the Presence of Plant Growth Regulators in High Biomass Forming Seaweeds from the Ionian Sea (Mediterranean Sea)" Sustainability 14, no. 7: 3914. https://0-doi-org.brum.beds.ac.uk/10.3390/su14073914

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop