Differential Production of Phenolics, Lipids, Carbohydrates and Proteins in Stressed and Unstressed Aquatic Plants, Azolla filiculoides and Azolla pinnata

Simple Summary Crops are the primary feedstock for the production of food/feed and energy, and our dependency on them has been increasing over the last decade. Climate change, reduced land for active agriculture, increased population, reduced amount of clean water, and high costs of chemical fertilizers and energy make modern agriculture unsustainable. Demands are rising for the next generation of cheap and sustainable feedstock, which could be productive under existing conditions. Aquatic plants, such as the free-floating species duckweed and Azolla, have started attracting attention because of their unique features, presenting advantages over terrestrial plants. Terrestrial plants grow on the land or need to be on dry land to survive. On the other hand, aquatic plants have the ability to thrive in ponds under controlled conditions using wastewaters as a source of nutrients. Over the last decade, Azolla species became an attractive feedstock for livestock because of their accumulation of valuable products, phenolic compounds, proteins, lipids, and carbohydrates. Stress-triggered changes in these nutritional components could have a significant impact on the nutritional value of Azolla, which is used as a sustainable food supplement for livestock, poultry, and fish industries. This paper aims to assess the effects of environmental and nutrient stresses on the biosynthesis of valuable metabolites in Azolla. Abstract The metabolic plasticity of shikimate and phenylpropanoid pathways redirects carbon flow to different sink products in order to protect sessile plants from environmental stresses. This study assessed the biochemical responses of two Azolla species, A. filiculoides and A. pinnata, to the combined effects of environmental and nutritional stresses experienced while growing outdoors under Australian summer conditions. These stresses triggered a more than 2-fold increase in the production of total phenols and their representatives, anthocyanins (up to 18-fold), flavonoids (up to 4.7-fold), and condensed tannins (up to 2.7-fold), which led to intense red coloration of the leaves. These changes were also associated with an increase in the concentration of carbohydrates and a decrease in concentrations of lipids and total proteins. Changes in lipid biosynthesis did not cause significant changes in concentrations of palmitoleic acid (C16:0), linolenic acid (C18:3), and linoleic acid (C18:2), the fatty acid signatures of Azolla species. However, a reduction in protein production triggered changes in biosynthesis of alanine, arginine, leucine, tyrosine, threonine, valine, and methionine amino acids. Stress-triggered changes in key nutritional components, phenolics, lipids, proteins, and carbohydrates could have a significant impact on the nutritional value of both Azolla species, which are widely used as a sustainable food supplement for livestock, poultry, and fish industries.

[1]  K. Karimi,et al.  Integrated biorefinery of aquatic fern Azolla filiculoides for enhanced extraction of phenolics, protein, and lipid and methane production from the residues , 2020 .

[2]  R. D. de Vos,et al.  Azolla ferns testify: seed plants and ferns share a common ancestor for leucoanthocyanidin reductase enzymes , 2020, The New phytologist.

[3]  H. Hasan,et al.  Dual function of Lemna minor and Azolla pinnata as phytoremediator for Palm Oil Mill Effluent and as feedstock. , 2020, Chemosphere.

[4]  Takayuki Tohge,et al.  Diversity of anthocyanin and proanthocyanin biosynthesis in land plants. , 2020, Current opinion in plant biology.

[5]  G. Spangenberg,et al.  Aquatic Plants, Landoltia punctata, and Azolla filiculoides as Bio-Converters of Wastewater to Biofuel , 2020, Plants.

[6]  Zhong-Guang Li,et al.  Signaling Role of Glutamate in Plants , 2020, Frontiers in Plant Science.

[7]  W. Huijgen,et al.  Aquatic weeds as novel protein sources: Alkaline extraction of tannin-rich Azolla , 2019, Biotechnology reports.

[8]  Hafiz Ansar Rasul Suleria,et al.  Proanthocyanidins: A comprehensive review. , 2019, Biomedicine & pharmacotherapy = Biomedecine & pharmacotherapie.

[9]  T. Isah.  Stress and defense responses in plant secondary metabolites production , 2019, Biological Research.

[10]  A. Hudson,et al.  The Synthesis and Role of β-Alanine in Plants , 2019, Front. Plant Sci..

[11]  A. Lüscher,et al.  Benefits of Condensed Tannins in Forage Legumes Fed to Ruminants: Importance of Structure, Concentration, and Diet Composition , 2019, Crop Science.

[12]  L. Shu,et al.  Water Scarcity and Ways to Reduce the Impact: Management Strategies and Technologies for Zero Liquid Discharge and Future Smart Cities , 2019 .

[13]  M. R. M. Júnior,et al.  Health Benefits of Flavonoids , 2019, Bioactive Compounds.

[14]  A. Mouradov,et al.  Microalgae as Bio-Converters of Wastewater into Biofuel and Food , 2018, Water Scarcity and Ways to Reduce the Impact.

[15]  S. Smeekens,et al.  Growing Azolla to produce sustainable protein feed: the effect of differing species and CO2 concentrations on biomass productivity and chemical composition , 2018, Journal of the science of food and agriculture.

[16]  F. Perez-Vizcaino,et al.  Research trends in flavonoids and health. , 2018, Archives of biochemistry and biophysics.

[17]  S. Rochfort,et al.  Lipid production in aquatic plant Azolla at vegetative and reproductive stages and in response to abiotic stress. , 2018, Plant physiology and biochemistry : PPB.

[18]  Liangjiang Wang,et al.  STRESS INDUCED FACTOR 2, a Leucine-Rich Repeat Kinase Regulates Basal Plant Pathogen Defense1[OPEN] , 2018, Plant Physiology.

[19]  U. Pérez-López,et al.  Concentration of phenolic compounds is increased in lettuce grown under high light intensity and elevated CO2. , 2018, Plant physiology and biochemistry : PPB.

[20]  Ana L. Pereira.  The Unique Symbiotic System between a Fern and a Cyanobacterium, Azolla-Anabaena azollae: Their Potential as Biofertilizer, Feed, and Remediation , 2017, Symbiosis.

[21]  P. Brouwer.  Turning the aquatic weed Azolla into a sustainable crop , 2017 .

[22]  B. Lal,et al.  Applications of microalgal biofilms for wastewater treatment and bioenergy production , 2017, Biotechnology for Biofuels.

[23]  A. Fernie,et al.  Leveraging Natural Variance towards Enhanced Understanding of Phytochemical Sunscreens. , 2017, Trends in plant science.

[24]  Hai Zhao,et al.  High flavonoid accompanied with high starch accumulation triggered by nutrient starvation in bioenergy crop duckweed (Landoltia punctata) , 2017, BMC Genomics.

[25]  F. Carrapiço.  The Azolla–Anabaena–Bacteria Association: A Case of Symbiotic Abduction? , 2017 .

[26]  B. Podpora,et al.  Spent brewer's yeast extracts as a new component of functional food , 2016 .

[27]  Anitha Kc,et al.  NUTRITIVE EVALUATION OF AZOLLA AS LIVESTOCK FEED , 2016 .

[28]  T. Bhaskar,et al.  Aquatic plant Azolla as the universal feedstock for biofuel production , 2016, Biotechnology for Biofuels.

[29]  Michael Clark,et al.  The environmental impacts of food production , 2016 .

[30]  Such,et al.  Health benefits of anthocyanins , 2016 .

[31]  P. Lærke,et al.  Comparing annual and perennial crops for bioenergy production – influence on nitrate leaching and energy balance , 2015 .

[32]  D. Funck,et al.  Physiological implications of arginine metabolism in plants , 2015, Front. Plant Sci..

[33]  J. Garnier,et al.  Relationships for estimating N2 fixation in legumes: incidence for N balance of legume‐based cropping systems in Europe , 2015 .

[34]  Krishna K. Kadali,et al.  Fungal-assisted algal flocculation: application in wastewater treatment and biofuel production , 2015, Biotechnology for Biofuels.

[35]  G. Spangenberg,et al.  Flavonoids: a metabolic network mediating plants adaptation to their real estate , 2014, Front. Plant Sci..

[36]  József Popp,et al.  The effect of bioenergy expansion: Food, energy, and environment , 2014 .

[37]  Krishna K. Kadali,et al.  Dual application of duckweed and azolla plants for wastewater treatment and renewable fuels and petrochemicals production , 2014, Biotechnology for Biofuels.

[38]  M. Jafari,et al.  Investigation the Effect of Different Levels of Azolla ( Azolla pinnata ) on Performance and Carcass Characteristics of Cobb Broiler Chicks , 2014 .

[39]  R. Chandran,et al.  Nutritional Composition and Antioxidant Properties of Cucumis dipsaceus Ehrenb. ex Spach Leaf , 2013, TheScientificWorldJournal.

[40]  Pingfang Yang,et al.  Manipulation of arginase expression modulates abiotic stress tolerance in Arabidopsis: effect on arginine metabolism and ROS accumulation , 2013, Journal of experimental botany.

[41]  B. Umesh,et al.  Effect of partial replacement of Azolla for concentrate supplement on lactating crossbred cows. , 2013 .

[42]  S. Jeyakumar,et al.  Azolla supplementation: feed cost benefit in duck ration in Andaman Islands. , 2013 .

[43]  R. Chowdhury,et al.  ISOLATION AND STRUCTURAL ELUCIDATION OF FLAVONOIDS FROM AQUATIC FERN AZOLLA MICROPHYLLA AND EVALUATION OF FREE RADICAL SCAVENGING ACTIVITY , 2013 .

[44]  S. Cristescu,et al.  Stress responses of duckweed (Lemna minor L.) and water velvet (Azolla filiculoides Lam.) to anionic surfactant sodium-dodecyl-sulphate (SDS). , 2012, Aquatic toxicology.

[45]  G. Spangenberg,et al.  Biosynthesis of Proanthocyanidins in White Clover Flowers: Cross Talk within the Flavonoid Pathway1[W][OA] , 2011, Plant Physiology.

[46]  R. Barbehenn,et al.  Tannins in plant-herbivore interactions. , 2011, Phytochemistry.

[47]  G. Reichart,et al.  The omnipresent water fern Azolla caroliniana does not contain lignin , 2011 .

[48]  G. Spangenberg,et al.  A high-resolution method for the localization of proanthocyanidins in plant tissues , 2011, Plant Methods.

[49]  A. Alarcón,et al.  Short-Term Effects of Arsenate-Induced Toxicity on Growth, Chlorophyll and Carotenoid Contents, and Total Content of Phenolic Compounds of Azolla filiculoides , 2011 .

[50]  Navid R. Moheimani,et al.  Sustainable biofuels from algae , 2013, Mitigation and Adaptation Strategies for Global Change.

[51]  Vitaly Citovsky,et al.  The roles of plant phenolics in defence and communication during Agrobacterium and Rhizobium infection. , 2010, Molecular plant pathology.

[52]  Je-Gun Joung,et al.  Interdependence of threonine, methionine and isoleucine metabolism in plants: accumulation and transcriptional regulation under abiotic stress , 2010, Amino Acids.

[53]  J. Bindelle,et al.  Nutritional value and intake of aquatic ferns (Azolla filiculoides Lam. and Salvinia molesta Mitchell.) in sows , 2010 .

[54]  A. Alarcón,et al.  Copper effects on photosynthetic activity and membrane leakage of Azolla filiculoides and A. caroliniana. , 2010 .

[55]  B. J. Prabina,et al.  Dried Azolla as a nutritionally rich cost effective and immuno-modulatory feed supplement for broilers. , 2010 .

[56]  F. Carrapiço,et al.  Azolla-Anabaena's behaviour in urban wastewater and artificial media--influence of combined nitrogen. , 2009, Water research.

[57]  Daniel Tomé,et al.  Converting Nitrogen into Protein—Beyond 6.25 and Jones' Factors , 2008, Critical reviews in food science and nutrition.

[58]  T. Lumpkin,et al.  Azolla: Botany, physiology, and use as a green manure , 1980, Economic Botany.

[59]  K. Sithara,et al.  Formulation of low -cost feed using azolla as a protein supplement and its influence on feed utilization in fishes , 2008 .

[60]  F. Carrapiço,et al.  Histochemistry of simple hairs from the foliar cavities of Azolla filiculoides , 2007 .

[61]  Z. Xiong,et al.  Cadmium‐induced changes in pigments, total phenolics, and phenylalanine ammonia‐lyase activity in fronds of Azolla imbricata , 2006, Environmental toxicology.

[62]  E. Iyayi,et al.  Chemical Composition and the Feeding Value of Azolla (Azolla pinnata) Meal for Egg-Type Chicks , 2006 .

[63]  N. Ishikura.  3-Desoxyanthocyanin and other phenolics in the water fernAzolla , 1982, The botanical magazine = Shokubutsu-gaku-zasshi.

[64]  O. Pulz,et al.  Valuable products from biotechnology of microalgae , 2004, Applied Microbiology and Biotechnology.

[65]  E. Barbarino,et al.  Distribution of intracellular nitrogen in marine microalgae: Calculation of new nitrogen-to-protein conversion factors , 2004 .

[66]  E. Olguín,et al.  Annual productivity of Spirulina (Arthrospira) and nutrient removal in a pig wastewater recycling process under tropical conditions , 2003, Journal of Applied Phycology.

[67]  F. Carrapiço,et al.  Biomass characterization ofAzolla filiculoidesgrown in natural ecosystems and wastewater , 1999, Hydrobiologia.

[68]  I. Watanabe,et al.  Improving nitrogen-fixing systems and integrating them into sustainable rice farming , 1992, Plant and Soil.

[69]  A. Moretti,et al.  Influence of light and pH on growth and nitrogenase activity on temperate-grown Azolla , 1988, Biology and Fertility of Soils.

[70]  H. Makkar.  Quantification of Tannins in Tree and Shrub Foliage , 2003, Springer Netherlands.

[71]  B. Coulman,et al.  Expression of Anthocyanins and Proanthocyanidins after Transformation of Alfalfa with Maize Lc12 , 2003, Plant Physiology.

[72]  B. Roy,et al.  Azolla (Azolla pinnata) as a Feed Ingredient in Broiler Ration , 2002 .

[73]  M. Tsuchiya,et al.  Feeding deterrence of Azolla in relation to deoxyanthocyanin and fatty acid composition , 2002 .

[74]  Y. Sakihama,et al.  Synergistic effect of deoxyanthocyanins from symbiotic fern Azolla spp. on hrmA gene induction in the cyanobacterium Nostoc punctiforme. , 2002, Molecular plant-microbe interactions : MPMI.

[75]  L. Romero,et al.  Resistance to cold and heat stress: accumulation of phenolic compounds in tomato and watermelon plants. , 2001, Plant science : an international journal of experimental plant biology.

[76]  C. Hove,et al.  The Azolla: Anabaena Symbiosis , 2022, Biology and Environment: Proceedings of the Royal Irish Academy.

[77]  Mengcheng Tang,et al.  The determination of flavonoid contents in mulberry and their scavenging effects on superoxide radicals , 1999 .

[78]  J. Chory,et al.  Genetic interactions between phytochrome A, phytochrome B, and cryptochrome 1 during Arabidopsis development. , 1998, Plant physiology.

[79]  T. N. Barry,et al.  Effect of condensed tannins in Lotus corniculatus upon lactation performance in ewes , 1996, The Journal of Agricultural Science.

[80]  P. Larkin,et al.  The DMACA–HCl Protocol and the Threshold Proanthocyanidin Content for Bloat Safety in Forage Legumes , 1996 .

[81]  I. Simpson,et al.  Parameters Affecting Residue Nitrogen Mineralization in Flooded Soils , 1994 .

[82]  T. Preston,et al.  Azolla filiculoides as partial replacement for traditional protein supplements in diets for growing-fattening pigs based on sugar cane juice. , 1990 .

[83]  R. U. Schenk,et al.  Medium and techniques for induction and growth of monocotyledonous and dicotyledonous plant cell cultures , 1972 .