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Effects of cytokinins on physiological and biochemical responses of the agar-producing red alga Gracilaria caudata (Gracilariales, Rhodophyta)

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Abstract

The red alga Gracilaria caudata J. Agardh (Gracilariales) is commercially exploited in Brazil as a source of raw material for agar production, and its cultivation is needed for sustainable biomass production to avoid overexploitation of natural populations. The objective of the present study was to evaluate the effects of aromatic and isoprenoid-derived cytokinins under two photon flux densities (PFDs) on growth rates, formation of lateral branches, pigment content (chlorophyll a and phycobiliproteins), and total soluble proteins in G. caudata. Aromatic cytokinins (benzylaminopurine, BA, and kinetin, K) and isoprenoid cytokinins (2-isopentenyladenine, 2iP, cis-zeatin, and trans-zeatin) were tested at 50 and 100 μmol photons m−2 s−1, temperature of 23 ± 1 °C, and light:dark cycle of 14:10 h. Cytokinins were added to the ASP 12-NTA synthetic medium (salinity 30 PSU, pH 8.0) in concentrations ranging from 0.0 to 50.0 μM. Growth rates of G. caudata were not affected by addition of isoprenoid and aromatic cytokinins. Zeatins (cis and trans forms) and BA at the concentrations of 0.5 and/or 5.0 μM stimulated the branch formation at 100 μmol photons m−2 s−1. In general, concentrations of isoprenoid cytokinins showed negative correlation with total soluble proteins and pigment contents at both PFDs. On the other hand, aromatic cytokinins did not affect protein contents, and K inhibited the pigment contents in both PFD levels. In conclusion, our results indicate that the isoprenoid and aromatic cytokinins and PFD levels did not affect the growth rates of G. caudata, but influence the branching and contents of pigments and total soluble proteins. Moreover, aromatic cytokinins and zeatins stimulated branch formation, which is a morphogenetic process useful for micropropagation of G. caudata, and could improve its cultivation in the Brazilian coast.

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References

  • Armisen R (1995) World-wide use and importance of Gracilaria. J Appl Phycol 7:231–243

    Article  Google Scholar 

  • Baweja P, Sahoo D (2009) Regeneration studies in Grateloupia filicina (J.V. Lamouroux) C. Agardh—an important carrageenophyte and edible seaweed. Algae 24:163–168

    Article  Google Scholar 

  • Benková E, Witters E, Dongen WV, Kolar J, Motyka V, Brzobohatý B, Onckelen HAV, Machácková (1999) Cytokinins in tobacco and wheat chloroplasts. Occurrence and changes due to light/dark treatment. Plant Physiol 121:245–252

    Article  PubMed  PubMed Central  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Bradley PM, Cheney DP (1990) Some effects of plant growth regulators on tissue cultures of the marine red alga Agardhiella subulata (Gigartinales, Rhodophyta). Hydrobiologia 204/205:353–360

    Article  Google Scholar 

  • Evans ML (1984) Functions of hormones at the cellular level of organization. In: Scott TK (ed) Encyclopedia of plant physiology, vol 10. New Series, Springer-Verlag, Berlin, pp 23–80

    Google Scholar 

  • Fosket DF (1994) Plant growth and development: a molecular approach. Academic, California, p 580

    Google Scholar 

  • Guiry MD, Guiry GM (2016) Algaebase. World-wide electronic publication, National University of Ireland, Galway, http://www.algaebase.org; searched on 02 May 2016.

  • Iwasaki H (1961) The life cycle of Porphyra tenera in vitro. Bio Bull 121:173–187

  • Jeffrey SW, Humphrey GF (1975) New spectrophotometric equations for determining clorophylls a, b, c 1 and c 2 in higher plants, algae and natural phytoplankton. Biochem Physiol Pflanz 167:191–194

    CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Kursar TA, Van Der Meer J, Alberte RS (1983) Light-harvesting system of red alga Gracilaria tikvahiae: I. Biochemical analyses of pigment mutations. Plant Physiol 73:353–360

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lawlor HJ, McComb JA, Borowitzka MA (1988) The development of filamentous and callus-like growth in tissue culture of Ecklonia radiata (Phaeophyta). In: Stadler T, Mollion J, Verdus MC, Karamanos Y, Morvan H, Christiaen D (eds) Algal Biotechnology. Elsevier Applied Science, Barking, pp 139–150

  • Mansilla A, Rodriguez JP, Souza JMC, Rosenfeld S, Ojeda J, Yokoya NS (2014) Growth responses to temperature, salinity and nutrient variations, and biomass variation and phenology of Ahnfeltia plicata (Rhodophyta, Ahnfeltiales), a commercially interesting agarophyte from the Magellanic Region, Chile. J Appl Phycol 26:1133–1139

    Article  CAS  Google Scholar 

  • Marinho-Soriano E, Moreira WSC, Carneiro MAA (2006) Some aspects of the growth of Gracilaria birdiae (Gracilariales, Rhodophyta) in an estuary in northeast Brasil. Aquac Int 14:327–336

    Article  Google Scholar 

  • Martins AP, Yokoya NS, Carvalho MAM, Plastino EM (2008) Effects of kinetin and nitrogen on growth rates, pigment and protein contents of wild and phycoerythrin-deficient strains of Hypnea musciformis (Rhodophyta). J Appl Phycol 20:767–773

    Article  CAS  Google Scholar 

  • McDonald MS (2003) Photobiology of higher plants. John Wiley and Sons, New York, p 368

    Google Scholar 

  • Mikani K, Mori IC, Matsuura T, Ikeda Y, Kojima M, Sakakibara H, Hirayama T (2015) Comprehensive quantification and genome survey reveal the presence of novel phytohormone action modes in red seaweeds. J Appl Phycol. doi:10.1007/s10811-015-0759-2

    Google Scholar 

  • Mok DW, Mok MC (2001) Cytokinin metabolism and action. Annu Rev Plant Physiol Plant Mol Biol 52:89–118

    Article  CAS  PubMed  Google Scholar 

  • Mooney PA, van Staden J (1986) Algae and cytokinins. J Plant Physiol 123:1–21

    Article  CAS  Google Scholar 

  • Oliveira EC (1998) The seaweed resources of Brazil. In: Critchley AT, Ohno M (eds) Seaweed resources of the world. Japan International Cooperation Agency, Yokosuka, pp 366–371

    Google Scholar 

  • Oliveira EC, Paula EJ, Plastino EM, Petti R (1995) Metodologias para o cultivo no axênico de macroalgas marinas in vitro. In: Alveal K, Ferrario ME, Oliveira EC, Sar E (eds) Manual de métodos ficológicos. Universidad de Concepción, Concepción, pp 429–455

    Google Scholar 

  • Ördög V, Stirk WA, Van Staden J, Novák O, Strnad M (2004) Endogenous cytokinins in three genera of microalgae from the Chlorophyta. J Phycol 40:88–95

    Article  Google Scholar 

  • Pedersén M (1973) Identification of a cytokinin, 6-(3 methyl-2-butenylamino) purine, in sea water and the effect of cytokinins on brown algae. Physiol Plant 28:101–105

    Article  Google Scholar 

  • Plastino EM, Oliveira EC (1997) Gracilaria caudata J. Agardh (Gracilariales, Rhodophyta)—restoring and old name for a common western Atlantic algae. Phycologia 36:225–232

    Article  Google Scholar 

  • Ramlov F, Plastino EM, Yokoya NS (2013) Growth, callus formation and plant regeneration in color morphs of Gracilaria domingensis (Gracilariales, Rhodophyta) cultured under different irradiance and plant growth regulators. Phycologia 52:508–516

    Article  CAS  Google Scholar 

  • Rebours C, Marinho-Soriano E, Zertuche-González JA, Hayashi L, Vásquez JÁ, Kradolfer P, Soriano G, Ugarte R, Abreu MH, Bay-Larsen I, Hovelsrud G, Rødven R, Robledo D (2014) Seaweeds: an opportunity for wealth and sustainable livelihood for coastal communities. J Appl Phycol 26:1939–1951

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sakakibara H (2006) Cytokinins: activity, biosynthesis, and translocation. Annu Rev Plant Biol 57:431–449

    Article  CAS  PubMed  Google Scholar 

  • Stirk WA, van Staden J (1997) Screening of some South African seaweeds for cytokinin-like activity. S Afr J Bot 63:161–164

    Article  Google Scholar 

  • Stirk WA, Van Staden J (2006) Seaweed products as biostimulants in agriculture. In Critchley AT, Ohno M, Largo DB (eds) World Seaweed Resources. ETI Information Services Ltd., Wokingham, (DVD)

  • Stirk WA, Novák O, Strnad M, Van Staden J (2003) Cytokinins in macroalgae. Plant Growth Regul 41:13–24

    Article  CAS  Google Scholar 

  • Stirk WA, Novák O, Hradecká V, Pénčík A, Rolčík J, Strnad M, Van Staden J (2009) Endogenous cytokinins, auxins and abscisic acid in Ulva fasciata (Chlorophyta) and Dictyota humifusa (Phaeophyta): towards understanding their biosynthesis and homeostasis. Eur J Phycol 44:231–240

    Article  CAS  Google Scholar 

  • Strnad M (1997) The aromatic cytokinins. Physiol Plant 101:674–688

    Article  CAS  Google Scholar 

  • Tarakhosvskaya ER, Maslov YI, Shishova MF (2007) Phytohormones in algae. Russ J Plant Physiol 54:163–170

    Article  Google Scholar 

  • Tian Q, Reed JW (2001) Molecular links between light and auxin signaling. J Plant Growth Regul 20:274–280

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Yokoya NS, Handro W (1996) Effects of auxins and cytokinins on tissue culture of Grateloupia dichotoma (Gigartinales, Rhodophyta). Hydrobiologia 326/327:393–400

    Article  Google Scholar 

  • Yokoya NS, Handro W (2002) Effects of plant growth regulators and culture medium on morphogenesis of Solieria filiformis (Rhodophyta) cultured in vitro. J Appl Phycol 14:97–102

    Article  CAS  Google Scholar 

  • Yokoya NS, Yoneshigue-Valentin Y (2011) Micropropagation as a tool for sustainable utilization and conservation of populations of Rhodophyta. Braz J Pharmacognosy 21:334–339

    Google Scholar 

  • Yokoya NS, Stirk WA, Van Staden J, Novák O, Turecková V, Pénčík A, Strnad M (2010) Endogenous cytokinins, auxins, and abscisic acid in red algae from Brazil. J Phycol 46:1198–1205

  • Yong YS, Yong WTL, Anton A (2013) Analysis of formulae for determination of seaweed growth rate. J Appl Phycol 25:1831–1834

    Article  Google Scholar 

Download references

Acknowledgments

The authors thank Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for fellowship to the first author and for research grants to NSY. This research was also supported by grant from Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES/AUXPE-CIMAR 1991/2014). The authors also thank Dr Andrea Tucci (Institute of Botany) for helping in statistical analyses. The present study is part of the Master dissertation presented by the first author to the Graduate Program in Plant Biodiversity and Environment, Institute of Botany, São Paulo, Brazil.

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Correspondence to Nair S. Yokoya.

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Souza, J.M.C., Yokoya, N.S. Effects of cytokinins on physiological and biochemical responses of the agar-producing red alga Gracilaria caudata (Gracilariales, Rhodophyta). J Appl Phycol 28, 3491–3499 (2016). https://doi.org/10.1007/s10811-016-0885-5

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