Skip to main content
Log in

Apical, sub-apical, and basal explants of industrially exploited marine red alga Gracilaria salicornia exhibited differential response to commercial seaweed-derived plant bio-stimulants

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

Abstract

The cultivation of the red algal genus Gracilaria is successful and accounts for a ca. 14% global share in farmed seaweed. Gracilaria salicornia has been used as feedstock for commercial production of galactans and plant bio-stimulant. The un-abated demand of raw material during last 5 years by domestic industries has fueled ca. 757% increase in biomass exploitation of this resource. As the farming methods heavily rely on clonal propagation of apical explants, it is imperative to check the viability of sub-apical and basal explant to increase the number of clones needed for farming operation. Here we ascertained the efficacy of two commercially available seaweed-derived plant bio-stimulants namely AMPEP and Sagarika under various concentrations and treatment times. One hundred percent survival was recorded with 0.1% AMPEP and 15-, 30-min exposure, 10% AMPEP and 15-, 30-, and 60-min exposure, while with Sagarika, it was observed in 0.01% and 60 min, 0.001% and 15, 30, and 60 min and 0.1% and 30, 60 min treatments of apical explants. The highest regeneration of 80.42 ± 12.01% was observed in apical explants at 1% AMPEP and 15-min exposure and the highest growth of 3.66 ± 0.32% day−1 was found in apical explants with 1% AMPEP and 60-min exposure. The proximate composition of apical explants treated with 0.1 g L−1 AMPEP and 60-min exposure was 25.10 ± 3.9% carbohydrate, 13.59 ± 4.8% protein, and 4.6 ± 1.1% lipid, while total phenol and free radical activity were 13.11 ± 1.65% and 37.93 ± 1.9%, respectively. Although apical explants clearly showed superiority for clonal propagation, use of sub-apical and basal explants can also be considered for commercial seedlings production in case of paucity of material to continue the operation. The sustainable production of seedlings would help in negating consequences of natural harvesting while ensuring continuous feedstock supply through cultivation.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1 
Fig. 2 
Fig. 3 

Similar content being viewed by others

Data availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  • Aguirre-Lipperheide M, Estrada-Rodriguez FJ, Evans LV (1995) Facts, problems and needs in seaweed tissue culture: an appraisal. J Phycol 31:677–688

    Article  Google Scholar 

  • Ali MKM, Critchley AT, Hurtado AQ (2020) Micropropagation and sea-based nursery growth of selected commercial Kappaphycus species in Penang, Malaysia. J Appl Phycol 32:1301–1309

    Article  CAS  Google Scholar 

  • Ali MKM, Sani MZB, Hi KK, Yasis SM, Keon KH, Critchley AT, Hurtado AQ (2018a) The comparative efficiency of a brown algal derived biostimulant extract (AMPEP), with and without supplemented PGRs: the induction of direct, axis shoots as applied to the propagation of vegetative seedlings for the successful mass cultivation of three commercial strains of Kappaphycus in Sabah, Malaysia. J Appl Phycol 30:1913–1919

    Article  CAS  Google Scholar 

  • Ali MKM, Yasir SM, Critchley AT, Hurtado AQ (2018b) Impacts of Ascophyllum marine plant extract powder (AMPEP) on the growth, incidence of the endophyte Neosiphonia apiculata and associated carrageenan quality of three commercial cultivars of Kappaphycus. J Appl Phycol 30:1185–1195

    Article  CAS  Google Scholar 

  • Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917

    Article  CAS  PubMed  Google Scholar 

  • Borlongan IAG, Tibubos KR, Yunque DAT, Hurtado AQ, Critchley AT (2011) Impact of AMPEP on the growth and occurrence of epiphytic Neosiphonia infestation on two varieties of commercially cultivated Kappaphycus alvarezii grown at different depths in the Philippines. J Appl Phycol 23:615–662

    Article  Google Scholar 

  • Calumpong HP, Maypa A, Magbanua M, Suarez P (1999) Biomass andagar assessment of three species of Gracilaria from the Negros Island, central Philippines. Hydrobiologia 398:173–182

    Article  Google Scholar 

  • Chen LCM, Taylor ARA (1978) Medullary tissue culture of the red alga Chondrus crispus. Can J Bot 56:883–886

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Dawange P, Jaiswar S (2020) Effects of Ascophyllum marine plant extract powder (AMPEP) on tissue growth, proximate, phenolic contents, and free radical scavenging activities in endemic red seaweed Gracilaria corticata var. cylindrica from India. J Appl Phycol 32:4127–4135

    Article  CAS  Google Scholar 

  • Dawes CJ, Lluisma AD, Trono CG (1993) Clonal propagation of Eucheuma denticulatum and Kappaphycus alvarezii for Philippine seaweed farms. Hydrobiologia 260:379–383

    Google Scholar 

  • Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356

    Article  CAS  Google Scholar 

  • Ertani A, Francioso O, Tinti A, Schiavon M, Pizzeghello D, Nardi S (2018) 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 9:428

  • FAO (2020) The State of World Fisheries and Aquaculture 2020. Sustainability in Action. FAO, Rome, pp 1–224

    Google Scholar 

  • Friedlander M (2008) Advances in cultivation of Gelidiales. J Appl Phycol 20:451–456

  • Friedlander M, Levy I (1995) Cultivation of Gracilaria in outdoor tanks and ponds. J Appl Phycol 7:315–324

    Article  Google Scholar 

  • Gamero-Vega G, Palacios-Palacios M, Quitral V (2020) Nutritional composition and bioactive compounds of red seaweed: a mini-review. J Food Nutr Res 8:431–440

    Article  CAS  Google Scholar 

  • Ganesan M, Thiruppathi S, Eswaran K, Reddy CRK, Jha B (2011) Development of an improved method of cultivation to obtain high biomass of red alga Gelidiella acerosa (Gelidiales, Rhodophyta) in the open sea. Biomass Bioenergy 35:2729–2736

    Article  Google Scholar 

  • Gloria C, Carlos M, Arturo C (2004) Micropropagation by explants of Gracilaria chilensis Bird, McLachlan and Oliveira. J Appl Phycol 16:203–213

    Article  Google Scholar 

  • Hurtado AQ, Critchley AT (2020) Time for applications of biostimulants in phyconomy. In: Torres DM, Kraan S, Dominguez H (eds) Seaweed extracts for enhanced cultivation of seaweeds (SEECS). Sustainable Seaweed Technologies. Elsevier, London. pp 103–127

  • Hurtado AQ, Joe M, Sanares RC, Fan D, Prithiviraj B, Critchley AT (2012) Investigation of the application of Acadian Marine Plant Extract Powder (AMPEP) to enhance the growth, phenolic content, free radical scavenging, and iron chelating activities of Kappaphycus Doty (Solieriaceae, Gigartinales, Rhodophyta). J Appl Phycol 24:601–611

    CAS  Google Scholar 

  • Hurtado AQ, Samonte GPB, Luhan MR, Guanzon N (1992) Gracilaria (Rhodophyta) farming in Panay, Western Visayas, Philippines. Aquaculture 105:233–240

    Article  Google Scholar 

  • Hurtado AQ, Yunque DA, Tibubos K, Critchley AT (2009) Use of Acadian marine plant extract powder from Ascophyllum nodosum in tissue culture of Kappaphycus varieties. J Appl Phycol 21:633–639

    Article  Google Scholar 

  • Kaladharan P, Johnson B, Abdul-Nazar AK, Boby-Ignatius, Chakraborty K, Gopalakrishnan A (2019) Perspective plan of ICAR-CMFRI for promoting seaweed agriculture in India. Mar Fish Inf Serv Tech Ext 17–22 Ser. No. 240

  • Khan 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 (review). J Plant Growth Regul 28:386–399

    Article  CAS  Google Scholar 

  • Kumar GRK, Reddy CRK, Jha B (2007) Callus induction and thallus regeneration from callus of phycocolloid yielding seaweeds from the Indian coast. J Appl Phycol 19:15–25

    Article  Google Scholar 

  • Lowry O, Rosebrough N, Farr A, Randall R (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275

    CAS  PubMed  Google Scholar 

  • Luhan MRJ, Mateo JP (2017) Clonal production of Kappaphycus alvarezii (Doty) Doty in vitro. J Appl Phycol 29:2339–2344

    Article  CAS  Google Scholar 

  • Mancuso S, Azzarello E, Mugnai S, Briand X (2006) Marine bioactive substances (IPA extract) improve foliar ion uptake and water stress tolerance in potted Vitis vinifera plants. Adv Hort Sci 20:156–161

    Google Scholar 

  • Mantri VA, Shah Y, Thiruppathi S (2020) Feasibility of farming the agarose-yielding red alga Gracilaria dura using tube-net cultivation in the open sea along the Gujarat coast of NW India. Appl Phycol 1:12–19

    Article  Google Scholar 

  • Mantri VA, Thakur MC, Kumar M, Reddy CRK, Jha B (2009) The carpospores culture of industrially important red alga Gracilaria dura (Gracilariales, Rhodophyta). Aquaculture 297:85–90

    Article  Google Scholar 

  • Mehta GK, Meena R, Prasad K, Ganesan M, Siddhanta AK (2010) Preparation of galactans from Gracilaria debilis and Gracilaria salicornia (Gracilariales, Rhodophyta) of Indian waters. J Appl Phycol 22:623–627

    Article  Google Scholar 

  • Nanda S, Kumar G, Hussain S (2021) Utilization of seaweed-based bio-stimulants in improving plant and soil health: current updates and future prospective. Int J Environ Sci Technol. https://doi.org/10.1007/s13762-021-03568-9

  • Oyieke HA (1994) The effect of phenotypic plasticity on agar from Gracilaria salicornia (J. Ag.) Dawson (Gracilariales, Rhodophyta) in Kenya. Bioresour Technol 49:267–271

    Article  CAS  Google Scholar 

  • Oza RM (1971) Effect of lAA on the growth of fragment of Gracilaria corticata. Seaweed Res Util 1:48–49

    Google Scholar 

  • Pierre G, Delattre C, Laroche C, Michaud P (2014) Galactans and its applications. In: Ramawat K, Mérillon JM (eds) Polysaccharides. Springer, Cham, pp 1–37

    Google Scholar 

  • Polne-Fuller M, Gibor A (1987) Callus and callus like growth in seaweeds: induction and Culture. Hydrobiologia 151/152:131–138

    Article  Google Scholar 

  • Porse H, Rudolph B (2017) The seaweed hydrocolloid industry: 2016 updates, requirements, and outlook. J Appl Phycol 29:2187–2200

    Google Scholar 

  • Rayirath P, Benkel B, Mark Hodges D et al (2009) Lipophilic components of the brown seaweed, Ascophyllum nodosum, enhance freezing tolerance in Arabidopsis thaliana. Planta 230:135–147

    Article  CAS  PubMed  Google Scholar 

  • Reddy CRK, Gupta MK, Mantri VA, Jha B (2008) Seaweed protoplasts: status, biotechnological perspectives and needs. J Appl Phycol 20:619–632

    Article  CAS  Google Scholar 

  • Reddy CRK, Kumar GRK, Siddhanta AK, Tewari A (2003) In vitro somatic embryogenesis and regeneration of somatic embryos from pigmented callus of Kappaphycus alvarezii (Doty) Doty (Rhodophyta, Gigartinales). J Phycol 39:610–616

    Article  CAS  Google Scholar 

  • Saga N, Uchida T, Sakai Y (1978) Clone Laminaria from single isolated cell. Bull Jap Soc Sci Fish 44:87

    Article  Google Scholar 

  • Salvador RC, Serrano AE (2005) Isolation of protoplasts from tissue fragments of Philippine cultivars of Kappaphycus alvarezii (Solieriaceae, Rhodophyta). J Appl Phycol 17:15–22

    Article  Google Scholar 

  • Saminathan KR, Ashok KS, Veeragurunathan V, Mantri VA  (2015) Seedling production in the industrially important agarophyte Gracilaria dura (Gracilariales, Rhodophyta). J Appl Phycol 27:1541–1548

    Article  CAS  Google Scholar 

  • Shah Y, Yadav A, Kumar MA, Kavale MG, Prasad K, Mantri VA (2021) ‘Proof of concept’ of how tube-net diameter affects growth and agar content in industrially important farmed red seaweed Gracilaria dura. J Appl Phycol 33:2349–2358

    Article  CAS  Google Scholar 

  • Singh RP, Muthy KNC, Jayaprakasha GK (2002) Studies on the antioxidant activity of pomegranate (Pinica granatum) peel and seed extracts using in vitro models. J Agric Food Chem 50:81–86

    Article  CAS  PubMed  Google Scholar 

  • Spann TM, Little HA (2011) Applications of a commercial extract of the brown seaweed Ascophyllum nodosum increases drought tolerance in container-grown ‘Hamlin’ sweet orange nursery trees. HortScience 46:577–582

    Article  Google Scholar 

  • Suto S (1959) Skeletonema No Tame No Jinkoubaiyoueki Suisan-Zouskoku 7:17–19 [in Japanese]

    Google Scholar 

  • Tabarsa M, Rezaei M, Ramezanpour Z, Waaland JR (2012) Chemical compositions of the marine algae Gracilaria salicornia (Rhodophyta) and Ulva lactuca (Chlorophyta) as a potential food source. J Sci Food Agric 92:2500–2506

    Article  CAS  PubMed  Google Scholar 

  • Titlyanov EA, Titlyanova TV, Kadel P, Luning K (2006a) New methods of obtaining plantlets and tetraspores from explants and cell aggregates of meristematic and submeristematic tissue of the red alga Palmaria palmata. J Exp Mar Biol Ecol 339:55–64

    Article  Google Scholar 

  • Titlyanov EA, Titlyanova TV, Kadel P, Luning K (2006b) Obtaining plantlets from apical meristem of the red alga Gelidium sp. J Appl Phycol 18:167–174

    Article  Google Scholar 

  • Trivedi K, Vijay Anand KG, Vaghela P, Ghosh A (2018) Differential growth, yield and biochemical responses of maize to the exogenous application of Kappaphycus alvarezii seaweed extract, at grain-filling stage under normal and drought conditions. Algal Res 35:236–244

    Article  Google Scholar 

  • Veeragurunathan V, Prasad K, Malarvizhi J, Singh N, Meena R, Mantri VA (2019) Gracilaria debilis cultivation, agar characterization and economics: bringing new species in the ambit of commercial farming in India. J Appl Phycol 31:2609–2621

    Article  Google Scholar 

  • Vignesh M, Kazi MA, Rathore MS, Kavale MG, Dineshkumar R, Mantri VA (2020) Artificial neural network modelling for seedling regeneration in Gracilaria dura (Rhodophyta) under different physiochemical conditions. Plant Cell Tiss Org 143:583–591

    Article  Google Scholar 

  • Wang W, Li H, Lin X, Zhang F, Fang B, Wang Z (2016) The effect of polar auxin transport on adventitious branches formation in Gracilaria lichenoides in vitro. Physiol Plantarum 158:356–365

    Article  CAS  Google Scholar 

  • Yeong HY, Phang SM, Reddy CRK, Khalid N (2014) Production of clonal planting materials from Gracilaria changii and Kappaphycus alvarezii through tissue culture and culture of G. changii explants in airlift photobioreactors. J Appl Phycol 26:729–746

    Article  CAS  Google Scholar 

  • Yokoya NS (2000) Apical callus formation and plant regeneration controlled by plant growth regulators on axenic culture of the red alga Gracilariopsis tenuifrons (Gracilariales, Rhodophyta). Phycol Res 48:133–142

    Article  CAS  Google Scholar 

  • Zhang X, Ervin EH (2004) Cytokinin-containing seaweed and humic acid extracts associated with creeping bentgrass leaf cytokinins and drought resistance. Crop Sci 44:1737–1745

    Article  CAS  Google Scholar 

  • Zhang X, Ervin EH (2008) Impact of seaweed extract-based cytokinins and zeatin riboside on creeping bentgrass heat tolerance. Crop Sci 48:364–370

    Article  Google Scholar 

  • Zuldin WH, Shapawi R (2015) Performance of red seaweed (Kappaphycus sp.) cultivated using tank culture system. J Fish Aquat Sci 10:1–12

    Google Scholar 

Download references

Acknowledgements

Authors thank Chris Sewall, Ocean Organics (USA) for providing the ‘Ascophyllum extract’ sample. We thank Alan Critchley for introducing us to this topic of research. Authors would like to take this opportunity to thank anonymous reviewer for meticulous comments on the first draft of the manuscript and handling editor for suggestions to improve the work. Thanks are also due to Director, CSIR-Central Salt and Marine Chemicals Research Institute, Bhavnagar for facilities. This communication has CSMCRI PRIS approval number 70/2021.

Funding

This study is funded by the Science and Engineering Research Board (SERB), New Delhi (EEQ/2018/000562) and Council of Scientific and Industrial Research under the mission mode project “Development of feasible and cost-effective technology for seedling production for commercially important seaweeds for sustainable cultivation.”

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Vaibhav A. Mantri.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 13.0 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jaiswar, S., Dawange, P.S., Thanth, C. et al. Apical, sub-apical, and basal explants of industrially exploited marine red alga Gracilaria salicornia exhibited differential response to commercial seaweed-derived plant bio-stimulants. J Appl Phycol 33, 3975–3985 (2021). https://doi.org/10.1007/s10811-021-02594-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-021-02594-x

Keywords

Navigation