Growth performance and biochemical profile of Azolla pinnata and Azolla caroliniana grown under greenhouse conditions
Keywords:Azolla, chlorophyll, fatty acids, phenolics, essential amino acids
- Azolla is a floating fern that is usually found in paddy water, streams, and pools, in symbiosis with the nitrogen-fixing cyanobacterium Anabaena azollae in the dorsal lobe cavity of the leaves.
- We determined that in greenhouse A. pinnata grows faster than A. caroliniana and its photosynthetic efficiency is more effective. In addition, palmitic acid, oleic acid and lignoceric acid were found to be predominant in A. pinnata and A. caroliniana.
- A. pinnata and A. caroliniana contain significant levels of essential amino acids and essential fatty acids and these characteristics make them economically important for human nutrition and the aquaculture sector.
Abstract: This study aimed to evaluate the growth performance, pigment content changes, essential amino acids (EAAs), fatty acids (FAs), and proximate composition of Azolla pinnata and Azolla caroliniana grown in a greenhouse. Plants were grown in nitrogen-free Hoagland’s solution at 28±2°C/21±2°C, day/night temperature and 60-70% humidity and examined on the 3rd, 5th, 10th and 15th days. The mean percentage of plant growth and relative growth rate for A. pinnata were 119% and 0.148 gg-1day-1, respectively, while for A. caroliniana these values were 94% and 0.120 gg-1day-1, respectively. Compared to day 3, the amount of total chlorophyll obtained on day 15 decreased significantly (p<0.05) for A. pinnata while the total phenolic and flavonoid contents increased significantly (p<0.05) from the 3rd to the 15th day. However, the total phenolic and flavonoid contents did not differ (p>0.0.5) in A. caroliniana. The crude protein, lipid, cellulose, ash values and the amounts of EAAs were higher in A. pinnata than A. caroliniana. Palmitic acid, oleic acid, and lignoceric acid were found to be predominant in A. pinnata and A. caroliniana. From the plant growth and pigment contents, we concluded that A. pinnata grew faster than A. caroliniana and its photosynthetic efficiency was more effective.
Received: January 31, 2019; Revised: March 22, 2019; Accepted: April 25, 2019; Published online: May 10, 2019
How to cite this article: Kösesakal T, Yıldız M. Growth performance and biochemical profile of Azolla pinnata and Azolla caroliniana grown under greenhouse conditions. Arch Biol Sci. 2019;71(3):475-82.
Costa ML, Santos MC, Carrapico F, Pereira AL. Azolla-Anabaena's behaviour in urban wastewater and artificial media – Influence of combined nitrogen. Water Res. 2009;43:3743-50.
Yadav RK, Abraham G, Singh YV, Singh PK. Advancements in the utilization of Azolla-anabaena system in relation to sustainable agricultural practices. Proc Indian Natn Sci Acad. 2014;80:301.
Gangadhar B, Sridhar N, Saurabh S, Raghavendra CH, Hemaprasanth KP, Raghunath MR, Jayasankar P. Effect of Azolla-incorporated diets on the growth and survival of Labeo fimbriatus during fry-to-fingerling rearing. Cogent Food Agric. 2015;1:1055539.
Yao Y, Zhang M, Tian Y, Zhao M, Zhang B, Zeng K, Zhao M, Yin B. Urea deep placement in combination with Azolla for reducing nitrogen loss and improving fertilizer nitrogen recovery in rice field. Field Crops Res. 2018a;218:141-9.
Bocchi S, Malgioglio A. Azolla-Anabaena as a biofertilizer for rice paddy fields in the Po Valley, a temperate rice area in Northern Italy. Int J Agron. 2010;2010:152158.
Yao Y, Zhang M, Tian Y, Zhao M, Zeng K, Zhang B, Zhao M, Yin B. Azolla biofertilizer for improving low nitrogen use efficiency in an intensive rice cropping system. Field Crops Res. 2018b;216:158-64.
Carrapiço F. Azolla as a superorganism. Its implication in symbiotic studies. In: Seckbach J, Grube M, editors. Symbioses and stress: joint ventures in biology. Dordrecht: Springer; 2010. p. 225-41.
Subedi P, Shrestha J. Improving soil fertility through Azolla application in low land rice: A review. Azarian J Agric. 2015;2(2):35-9.
Gouri MD, Sanganal JS, Gopinath CR, Kalibavi1 CM. Importance of Azolla as a sustainable feed for livestock and poultry – A Review. Agric Review. 2012;33(2):93-103.
Brouwer P, Brautigam A, Kulahoglu C, Tazelaar AO, Kurz S, Nierop KG, van der Werf A, Weber AP, Schluepmann H. Azolla domestication towards a biobased economy? New Phytol. 2014;202:1069-82.
Miranda AF, Biswas B, Ramkumar N, Singh R, Kumar J, James A, Roddick F, Lal B, Subudhi S, Bhaskar T, Mouradov A. Aquatic plant Azolla as the universal feedstock for biofuel production. Biotechnol Biofuels. 2016;9:221.
Kollah B, Patra AK, Mohanty SR. Aquatic microphylla Azolla: a perspective paradigm for sustainable agriculture, environment and global climate change. Environ Sci Pollut Res Int. 2016;23:4358-69.
Muradov N, Taha M, Miranda AF, Kadali K, Gujar A, Rochfort S, Stevenson T, Ball AS, Mouradov A. Dual application of duckweed and Azolla plants for wastewater treatment and renewable fuels and petrochemicals production. Biotechnol Biofuels. 2014;7:30.
Roberts AE, Boylen CW, Nierzwicki-Bauer SA. Effects of lead accumulation on the Azolla caroliniana-Anabaena association. Ecotoxicol Environ Saf. 2014;102:100-4.
Kosesakal T. Effects of seasonal changes on pigment composition of Azolla filiculoides Lam. Am Fern J. 2014;104(2):58-66.
Kosesakal T. Assessment of the biodegradation capacity of Azolla on polycyclic aromatic hydrocarbons in crude oil. Global NEST J. 2018;20(3):27-32
Gomes MP, de Brito JCM, Carvalho Carneiro MML, Ribeiro da Cunha MR, Garcia QS, Figueredo CC. Responses of the nitrogen-fixing aquatic fern Azolla to water contaminated with ciprofloxacin: Impacts on biofertilization. Environ Pollut. 2018;232:293-9.
Kosesakal T, Unal M, Kulen O, Memon A, Yuksel B. Phytoremediation of petroleum hydrocarbons by using a freshwater fern species Azolla filiculoides Lam. Int J Phytoremediation. 2016;18:467-76.
Jampeetong A, Brix H. Effects of NH4+ concentration on growth, morphology, and NH4+ uptake kinetics of Salvinia natans. Ecol Eng. 2009;35:695-702.
Lichtenthaler HK, Wellburn AR. Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochem Soc Trans. 1983;11:591-2.
Zhang D, Quantick PC. Effects of chitosan coating on enzymatic browning and decay during postharvest storage of litchi (Litchi chinensis Sonn.) fruit. Postharvest Biol Tecnol. 1997;12:195-202.
AOAC. Official methods of analysis of AOAC International. 16th ed. Arlington, VA, USA: AOAC International; 1995.
AOAC. Official methods of analysis of AOAC International. 17th ed. Maryland, USA: AOAC International; 2000.
Antoine FR, Wei CI, Littell RC, Marshall MR. HPLC method for analysis of free amino acids in fish using o-phthaldialdehyde precolumn derivatization. J Agr Food Chem. 1999;47(12):5100-7.
Ichihara K, Shibahara A, Yamamoto K, Nakayama T. An improved method for rapid analysis of the fatty acids of glycerolipids. Lipids. 1996;31(5):535-9.
Pereira AL, Monteiro B, Azevedo J, Campos A, Osorio H, Vasconcelos V. Effects of the naturally-occurring contaminant microcystins on the Azolla filiculoides-Anabaena azollae symbiosis. Ecotoxicol Environ Saf. 2015;118:11-20.
Kannaiyan S. Effect of Benlate and Rhizoctonia interactions on the growth, chlorophyll contents and nitrogen fixation in three species of Azolla. S Afr J Bot. 1992;58:292-5.
Abraham G. Antioxidant enzyme status in Azolla microphylla in relation to salinity and possibilities of environmental monitoring. Thin Solid Films. 2010;519:1240-3.
Arora A, Saxena S. Cultivation of Azolla microphylla biomass on secondary-treated Delhi municipal effluents. Biomass Bioenergy. 2005;29:60-4.
Li YY, Lü XT, Wang ZW, Zhou C, Han XG. Linking relative growth rate to biomass allocation: the responses of a grass (Leymus chinensis) to nitrogen addition. Phyton Int J Exp Bot. 2014;83:283-9.
Mostafa EM, Tammam AA. The oxidative stress caused by NaCl in Azolla caroliniana is mitigated by nitrate. J Plant Interact. 2011;7:356-66.
Vafaei F, Khataee AR, Movafeghi A, Salehi Lisar SY, Zarei M. Bioremoval of an azo dye by Azolla filiculoides: Study of growth, photosynthetic pigments and antioxidant enzymes status. Int Biodeterior Biodegradation. 2012;75:194-200.
Rai AK, Rai V. Effect of NaCl on growth, nitrate uptake and reduction and nitrogenase activity of Azolla pinnata/Anabaena azollae. Plant Sci. 2003;164:61-9.
Close DC, Davidson NJ, Davies NW. Seasonal fluctuations in pigment chemistry of co-occurring plant hemi-parasites of distinct form and function. Environ Exp Bot. 2006;58:41-6.
Sun T, Yuan H, Cao H, Yazdani M, Tadmor Y, Li L. Carotenoid metabolism in plants: The role of plastids. Mol Plant. 2018;11:58-74.
Savicka M, Petjukevičs A, Batjuka A, Škute N. Impact of moderate heat stress on the biochemical and physiological responses of the invasive waterweed Elodea canadensis (Michx. 1803). Arch Biol Sci. 2018;70(3):551-7.
Dai LP, Xiong ZT, Huang Y, Li MJ. Cadmium-induced changes in pigments, total phenolics, and phenylalanine ammonia-lyase activity in fronds of Azolla imbricata. Environ Toxicol. 2006;21:505-12.
Candan N, Tarhan L. Relationship among chlorophyll-carotenoid content, antioxidant enzyme activities and lipid peroxidation levels by Mg2+ deficiency in the Mentha pulegium leaves. Plant Physiol Biochem. 2003;41:35-40.
Dixon RA, Paiva NL. Stress-induced phenylpropanoid metabolism. Plant Cell. 1995;7(7):1085.
Zhang X, Liu CJ. Multifaceted regulations of gateway enzyme phenylalanine ammonia-lyase in the biosynthesis of phenylpropanoids. Mol Plant. 2015;8:17-27.
Forni C, Braglia R, Harren FJ, Cristescu SM. Stress responses of duckweed (Lemna minor L.) and water velvet (Azolla filiculoides Lam.) to anionic surfactant sodium-dodecyl-sulphate (SDS). Aquat Toxicol. 2012;110-111:107-13.
Noor Nawaz AS, Syed J, Dileep N, Rakesh KN, Prashith Kekuda TR. Antioxidant activity of Azolla pinnata and Azolla rubra –A comparative study. Sch Acad J Biosci. 2014;2(10):719-23.
Leterme P, Londoño AM, Muñoz JE, Súarez J, Bedoya CA, Souffrant WB, Buldgen A. Nutritional value of aquatic ferns (Azolla filiculoides Lam. and Salvinia molesta Mitchell) in pigs. Anim Feed Sci Technol. 2009;149:135-48.
Datta SN. Culture of Azolla and its efficacy in diet of Labeo rohita. Aquaculture. 2011;310:376-9.
van Kempen MML, Smolders AJP, Bögemann GM, Lamers LLM, Visser EJW, Roelofs JGM. Responses of the Azolla filiculoides Stras.–Anabaena azollae Lam. association to elevated sodium chloride concentrations: Amino acids as indicators for salt stress and tipping point. Aquat Bot. 2013;106:20-8.
Paoletti C, Bocci F, Lercker G, Capella P, Materassi R. Lipid composition of Azolla caroliniana biomass and its seasonal variation. Phytochemistry. 1987;26:1045-7.
Cohen MF, Meziane T, Tsuchiya M, Yamasaki H. Feeding deterrence of Azolla in relation to deoxyanthocyanin and fatty acid composition. Aquat Bot. 2002;74 (2):181-7.
Brouwer P, van der Werf A, Schluepmann H, Reichart G-J, Nierop KGJ. Lipid yield and composition of Azolla filiculoides and the implications for biodiesel production. BioEnergy Res. 2016;9(1):369-77.
Miranda AF, Liu Z, Rochfort S, Mouradov A. Lipid production in aquatic plant Azolla at vegetative and reproductive stages and in response to abiotic stress. Plant Physiol Biochem. 2018;124:117-25.
Matoša Kočar M, Sudarić A, Sudar R, Duvnjak T, Zdunić Z. Screening of early maturing soybean genotypes for production of high quality edible oil. Zemdirbyste-Agric. 2018;105(1):55-62.