Reviews In Food And Agriculture (RFNA) 2(1) (2021) 04-08

Reviews In Food And Agriculture (RFNA)

ISSN: 2735-0312 (Online)

REVIEW ARTICLE

AN OVERVIEW OF AZOLLA IN RICE PRODUCTION: A REVIEW

Tribhuvan University, Institute of Agriculture and Animal Science, Prithu Technical College, Deukhuri, Dang, Nepal.
*Corresponding author email: kripaadhikary9@gmail.com

This is an open access article distributed under the Creative Commons Attribution License CC BY 4.0, which permits unrestricted use, distribution, and
reproduction in any medium, provided the original work is properly cited.

ARTICLE DETAILS ABSTRACT

Article History: Azolla is a free-floating water fern which in symbiotic association with cyanobacterium Anabaena azollaefixes
the atmospheric nitrogen. Nitrogen fixing ability of cyanobacterialsymbiont varies between 30 and 60 kg N
Received 10 October 2020
Accepted 12 November 2020
ha−1 which designates Azolla as an important biological nitrogen source for rice ecosystem. Inoculation of
Available online 04 December 2020 Azolla is an alternative and sustainable source of nitrogen to increase the rice productivity and it also can
decrease the use of synthetic fertilizer. A number of past researches prove that Azolla has been used as
apotential biofertilizer for rice production. Azolla is either incorporated in the soil before rice transplanting
or grown as a dual crop along with rice. The objective of this paper is to provide a brief account of importance
as well as developments in the utilization of Azolla-Anabaena system in agriculture, mainly rice production.

KEYWORDS
Azolla, nitrogen,Anabaena azollae,rice crop.

1. INTRODUCTION by rice is very low as 10% and never exceeds 50% (Vlek and Byrnes,
1986). Loss from urea ranges from 11 to 54% when it is broadcasted in
Bio-fertilizers are formulations of beneficial microorganisms that help the rice field after transplantation (Schnier, 1995).Thus,Azollabiofertification
growth of plants by increasing the quantity and availability of nutrients could be a good approach to increase the nitrogen use efficiency (NUE) in
through their biological activities (El-Hawary and El-Kholy, 2019). They rice fields (Yao et al., 2018).
are the preparations containing living cells or latent cells of efficient
strains of microorganisms that help crop plants for the uptake of nutrients Azollais a heterosporouspteridophyte that lives in a place having plenty of
by their interactions in rhizosphere. Bio-fertilizers are mostly used in water. It is a free-floating water fern. It’s most common utilization is
sustainable farming for increasing soil fertility and crop productivity. They the co-cultivation with rice, as water-filled rice paddies provide a perfect
are the most important component of integrated nutrient management. habitat for the water fern to propagate. Azolla has been used as green
(Itelima et al., 2018). The mostly used microorganisms as bio-fertilizer manure due to its rapid reproduction and high nitrogen content(3-6% N
are: nitrogen fixers (N-fixer), growth promoting rhizobacteria (PGPRs) by dry weight) (Watanabale et al.,1981). The Nitrogen content is similar
like Azotobacter, Azospirillum and Phosphorus Solubilizing Bacteria to that of legumes. It is an excellent source of bio fertilizerswhich fixes the
(PSB) viz; Pseudomonas sp. and Bacillus sp. endo and ectomycorrhizal atmospheric nitrogen in symbiotic association with a cyanobacterium,
fungi, cyanobacteria and other useful microscopic organisms (Yasin et Anabaena azollae (Carrapico, 2002). Anabaenaazollae, a blue green algae
al., 2012). The use of bio-fertilizers makes the soil environment rich in all can photosynthesize independently. The entire nitrogen requirement of
kinds of micro- and macro- nutrients also helps the release of plant the Azolla frond is supplied by the algal symbioant. An Anabena-Azolla
growth regulating substances, production of antibiotics and relationship is ideal for the cultivation of rice under tropical conditions
biodegradation of organic matter in the soil (Sinha et al., 2014). Bio- because of its ability to fix atmospheric nitrogen and capacity to multiply
fertilizers, contradict to synthetic fertilizer, are more economical and at faster rates.
helpful in improving the soil structures and restoration of environment
for leveraging agriculture (Yasin et al., 2012). Bio-fertilizers are thus Azolla can flourish well in flooded rice fieldsthus, it is also extensively used
considered the alternative of chemical fertilizers. as a most suitable bio-fertilizer for the rice fields to improve the nitrogen
content within few weeks of its incorporation (Bhuvaneshwari and Singh,
Rice (Oryza sativa L.) is a major cereal crop in Nepal. Plant nutrition is very 2015). Azolla biomass can be used in rice fields as partial or complete
important for the healthy growth of crops. Nitrogen fertilization is most replacement of synthetic fertilizers because of its ability to provide 1.5-2.0
important for the yield of grain in rice plant (Chaturvedi, 2006). The million tons of nitrogen whereas the requirement of urea for same amount
demand and synchronization of Nitrogen differ with inbred and hybrid of crop production is 3.3-4.0 million tons (Raja et al., 2012). Along with the
rice varieties. Hybrid varieties having genetically high yield potential supply of nitrogen, Azolla also decreases the soil pH and water
require higher amount of nitrogen as compared to inbred varieties (Ravi temperature, inhibit NH3 volatization, and prevents weeds and mosquito
et al., 2007). The use of chemical fertilizers generally urea [CO(NH2)2] or prolification (Pabby et al., 2004). The nitrogen fixation ability of one crop
ammonium sulphate [(NH4) 2.SO4] is very common in case of Nepalese ofAzolla to the rice crop in about 20-25 days is found to be 20-40 kg Nha-
1 and the ability of Anabaena azolla system has been estimated to be 1.1 kg
rice farming system. The Nitrogen fertilizer efficiency is less than 40% and
is very costly for farmers to purchase (Joshy, 1997). Recovery of Nitrogen N ha-1 day-1 (Watanabe et al., 1977). The integration of Azolla with urea
has increased urea use efficiency (Cisse 2001; Vlek et al., 1995).
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Cite The Article: Kripa Adhikari, Sudip Bhandari, Subash Acharya (2021). An Overview Of Azolla In Rice Production: A Review.
Reviews In Food And Agriculture, 2(1): 04-08.
 Reviews In Food And Agriculture (RFNA) 2(1) (2021) 04-08

2. SOURCE OF INFORMATION To isolate the hair cells from A. filiculoides containing a packet of
Anabaena, aprocedure has been developed. (Uheda, 1986).The routes by
This paper was prepared by collecting the information from all available which metabolic exchange between the two partners of the association is
resources i. e. journals, annual reports, articles, proceedings, etc. not clearly understood. However, distribution, morphology, and transfer
published by different authors, researchers, professors and scientists as of cell structures of the two populations in the cavity trichomes suggests
well as research Centre and stations. The information was gathered and that the branched hairs of the cavity are involved in ammonium uptake
systematically arranged into different heading and subheading, by and /or metabolism (throughout the development) and simple hairs are
reviewing more than 40 research papers intensively. involved in facilitating the transfer of sucrose from the mesophyll to the
endophyte in mature cavities (Konar and Kapoor, 1972; Duckett et al.,
3. RESEARCH HIGHLIGHT 1975a; Calvert and Peters, 1981; Peters et al., 1985a). The interior surface
of a mature leaf cavity is lined with an envelope and largely filled with
The complete study reviewing different paper was done and collected gases. The mucilage is secreted by cyanobacterium (Shi et al., 1987)and
information's were systematically arranged into different subheadings those cavities free from endophyte do not contain mucilage (Lumpkin and
namely:Azolla biology, its symbiont nature with Anabena,Biological Plucknett, 1980; Duckett et al., 1975a).
Nitrogen fixation by Azolla, Production of Azollabiomass and application
to the rice crop,Nitrogen Yield by Azolla in rice field and Contribution of It is believed that only one kind of Anabaena Azollais found in the leaf
Azolla to yield of rice cavities of different Azolla species.Anabaena azollae from severalAzolla
species shared similar antigens (Ladha & Watanabe, 1982). The similarity
3.1 Genus Azolla of Anabaena Azollae in different Azolla species is also verified by ‘nif’ gene
studies (Franche et al., 1985). However, Anabaena azollae is observed not
The genus Azolla was firstly introduced by Lamarck in 1783 (Lumpkin and to be uniform through out genus Azolla, through the use of using
Plucknett, 1980). For several years Azolla belonged to family Azollaceae monoclonal antibodies technique (Plazinski et al., 1988).
but now taxonomist has assigned Azollato a monotypic family Salviniaceae
(Al-saadi and Abdullah, 2016). The genus has several species. A.pinnata 3.3 Biological Nitrogen fixation by Azolla
and A.nilotica belonging to the section Rhizosperma and A. caroliniana, A.
filiculoides, A. mexicana, A. microphylla and A. rubra belonging to section The site of Nitrogen fixation is the heterocyst of the symbiont Anabaena.
Azolla (Rothwell, 1999). The sporophyte of Azolla has a main rhizome that Nitrogenase, the nitrogen fixing enzyme, is present on the heterocysts
branched into secondary rhizomes, both bears the alternatively arranged (Peters, 1975). It is found that the nitrogenase activity in fresh isolated
small bilobed leaves. The adventitious root, which absorbs nutrients symbiont is 6-10 than that of association and 12-10 times higher than that
directly from water or from the soil in shallow water, arises from ventral of free living cyanobacteria (Becking, 1976). The endogeneous source of
sides of rhizome (Roy et al., 2016). The areal dorsal lobe is chlorophyllus, fixed nitrogen gives Azolla a good advantage over other floating
where Anabena- azollae inhibits, and a ventral lobe is partially submerged hydrophytes in many environments. Nitrogen fixation along with the high
and hyaline (Calvert et al., 1985; Peters et al., 1982; Singh, 1977). growth rate enables Azolla to accumulate greater than 10 kg of
nitrogen/ha/ day under optimum conditions (Lumpkin, 1985).
Azollais a free water fern widespread on tropic and subtropic and warm
temperate regions (Raja et al., 2012). The delicate, small triangular or The nitrogen fixation in Anabaena azollae is closely related and dependent
polygonal shaped plants grows luxuriantly in ditches, fresh water and on photosynthesis (Peters, 1976). The source of all the ATP and reductant
paddy fields (Yadav et al., 2014). Its size is generally 1-2.5 cm in diameter, required to convert nitrogen to ammonia in the symbiosis is
but some species can achieve the size of 15 cm or more (Lumpkin and photosynthesis. Simultaneous measurement of the rates of
Plucknett, 1980). Azolla reproduce both sexually and asexually but photosynthesis, respiration and C2H2 reduction in A. imbricata revealed
vegetative reproduction is more common. (Qiu and Yu, 2003). It can that nitrogenase activity is primarility dependent on the
multiply vegetatively through fragmentation and reproductively through photosynthetically captured radiation energy, and secondarily on C02
spore production. OnlyA. Mexicanaforms spores throughout the year, and fixation (Shi et al., 1981). The close interactionbetween photosynthesis
for the other species of Azollasexual reproduction occurs during limited and N2-fixation has been demonstrated by measurement of the action
periods of the year (Singh et al., 1987). Oslen reported thatAzolla strains spectra for nitrogenase- catalyzed C2H2 reduction in the association and
are capable of growth from pH 3.5-10 with its best optimum between pH in the isolated endophyte (Tyagi et al., 1981). Glutamine synthetase,
5 and 8 (Oslen, 1970). Glutamate synthetase, Glutamate dehydrogenase are the three enzymes
involved in assimilation of ammonium (Ray et al., 1978).
3.2 Anabaena Azollae symbiosis
Enzyme glutamine synthetase (GS), present in heterocyst, incorporates
Azolla (mosquito fern, duckweed fern, fairy moss, water fern) lives in the newly fixed nitrogen into glutamine. Glutamate synthetase (GOGAT) is
symbiosis with a filamentous, heterocyst- forming cyanobacterium found to be active in the vegetative cells and glutamate is transported from
calledAnabaena, occurs in the dorsal leaf cavities of the fronds, with the these cells to the heterocysts (Ladha and Watanabe, 1987). The fixed N2 is
ability of atmospheric nitrogen fixation (Pereira and Vasconcelos, 2014). transported to the host by the symbiont where it is incorporated into the
The algal symbiontAnabaena azollaeStrasburger, belongs to the phylum amino acids and these amino acids along with reductant and
Cyanophyta, order Nostocales and family Nostocaceae (Moore, 1969). photosynthate are provided to the symbiont. Anabaena azollaenot only
After the sporophyte breaks out through the apical membrane, initial fixes the nitrogen, but also excretes ammonia. Some researcher used N2 to
contact between Anabaena cells and Azolla plant takes place (Lin and find the distribution of nitrogen compounds produced by Anabaena
Watanabe, 1988). Theendosymbontshows the synchronous growth and azollae symbiosis (Peters,1976; Peters 1977). He found that N2
development (Shi et al., 1984; Hill 1975). Anabaena azollaepossesses distributed as extracellular ammonia (49.9%), intracellular ammonia
sinuous trichomes (threads) composed of bead like or barrel-shaped cells (6.4%), extracellular organic nitrogen (5.6%) and intracellular organic
without a sheath (Shen, 1960). Fjerdingstad claimed that the nitrogen (38.1%). Kannaiyan and Goyal observed ammonia excretion in
cyanobacterium is the ecoform of Anabaena variabilis (Fjerdingstad four algal symbiosis isolated from different species of Azolla (Kannaiyan
(1976). and Goyal, 1988).

Anabaena filaments associated with the apical meristem of each main and 3.4 Production of Azolla biomass and application to the rice crop
lateral branches is undifferentiated and non- nitrogen fixing (Subudhi and
Singh, 1978b). The epidermal hairs called the primary branched hairs 3.4.1 Production of Azolla biomass
(PBH) grow from the axil of dorsal lobe, as leaf cavities develop in the form
of depressions on the adaxial epidermis of the dorsal leaf lobe. Its terminal Soil based nurseries are made for the propagation of Azolla. However,
cells have an ultrastructure of transfer cells and remain in interaction with nursery plots, ditches, ponds, canals, small creeks, concrete tanks,
Anabaena filaments (Calvert and Peters, 1981). The algal filaments along polythene lined ditches can be used for Azollaproduction. Generally, in the
with PBH get partitioned into the leaf cavities,as the developing leaves are rice field, small plots bounded by strong mud bunds are used. (Kannaiyan,
displaced from the meristem. Concominant with the onset of leaf cavity 1982). Azolla to be produced and used as biofertilizer for rice, cattle slurry
closure, Anabaena cells enlarge and the alga develops heterocysts and and animal dung are effective. (Singh et al., 1993). Single Super Phosphate
starts nitrogen fixation. Simple hairs emerge from the cavity wall and more as a source of inorganic fertilizer is used for higher biomass yield. In
than 20 simple hairs develop near the photosynthetic mesophyll zone controlled conditions and availability of below mentioned factors Azolla
(Calvert and Peters, 1981). To the periphery of cavity in the matured can grow and provide sufficient amount of biomass.
dorsal leaf lobe, Anabaena Azollae are localized (Shi et al., 1984).

Cite The Article: Kripa Adhikari, Sudip Bhandari, Subash Acharya (2021). An Overview Of Azolla In Rice Production: A Review.
Reviews In Food And Agriculture, 2(1): 04-08.
 Reviews In Food And Agriculture (RFNA) 2(1) (2021) 04-08

3.4.2 Factors affecting growth and Nitrogen requirement of Azolla incorporation of 8-10 tons of Azolla/ha fresh produced the same rice yield,
47% increase in grain yield over control (Singh, 1977). Combination of
All the essential macro and micro-nutrients, except combined nitrogen is Azolla with lower dose of Nitrogen in planted paddy fields gave higher
required for optimum growth of Azolla. Azolla has been successfully paddy yield, thus a judicious combination of azolla and nitrogen provides
grown in different N-free inorganic media (Huneke, 1933). Deficiency of a better yield (Singh 1979 a,b). A group researcher found that
Calcium and Phosphorous adversely affect the growth and nitrogen Azollaincorporation increases the paddy yield by 8-14% (Yao et al., 2018).
fixation by Azolla (Singh, 1979a). The quality and intensity of light also Behera reported that the grain yield increased by34% due to the
have pronounced effect it’s on growth and nitrogen fixing ability. Various incorporation of 10 ton Azolla/ha (Behera, 1982). Kannaiyan and
observations suggest that Azolla prefers an environment with certain Bartharkur and Talukdar reported 36.6 to 38% increase in grain yield due
degree of shading. The highest N content of Azollaat 25 K lux (Lumpkin to use ofAzolla as dual crop (Kannaiyan, 1982; Bartharkur and Talukdar,
and Plucknett, 1980). 1983). Moore found the increase in rice yield by 14-40% due top
Azolladual cropping, whereas Le Van reported 6-29% higher grain yield
The optimum temperature requirement for A. mexicana, A. pinnata and A. by growing A. pinnata as a dual crop with rice (Moore, 1969; Le Van, 1963).
caroliniana are 30 °C and for A. filiculoidesis 25°C (Peters et al., 1980). A group researhcers reported the application of Azolla along with neem
Azolla biomass increased by 14-16 times in 14 days at 30/25°C, 38/30°C cake coated urea recorded the maximum grain yield of rice (Sukumar et
and 40/32°C day/night temperatures, whereas nitrogenase activity was al., 1988).
the highest on the 7th day at 30/25°C (Chapman et al., 1981). The
optimum pH requirement for proper growth and nitrogen fixation in Benefits of using Azolla on the rice field are: Basal application of Azolla at
Azolla is 5-7. Azolla plants require N2 for N2-fixation, C02 for the rate of 10-12 tones/ha enriches soil nitrogen content by 50-60 kg/ha
photosynthesis and 02 for respiration (Watanabe et al., 1977). The growth and reduces 30-35 kg of nitrogenous fertilizer requirement of rice crop.
of A. pinnata, A. mexicanaand A. filiculoides was found to be better in open Inoculation of green Azollaat the rate of 500 kg/ha increases the soil
containers due to free diffusion of gases (Becking,1979). At optimum light nitrogen content by 50 kg/ha and reduces the nitrogen fertilizer by 20-30
intensity of about 49 K lux with a day length of 12 hours, the growth rate kg/ha (Roy et al., 2016). Inoculation of Azolla on flooded water decreases
of Azollaof 150-175 mg/g fresh weigh/day (Ashton ,1971). the NH3 volatilization by 12–42% (Yao et al., 2018). Due to its high
biomass production rate, Azolla improves the soil physical structure by
3.4.3 Application of Azolla to Rice crop supplying huge amount of organic matter on its incorporation to soil
(Subedi and Shrestha, 2015. Azolla also solubilizes the, Zn, Fe and Mn and
The application of Azollais donein the field is either as a green manure make them available to the rice crop. It releases plant growth regulators
before transplanting or as a dual crop with rice after transplanting (Singh, and vitamins that enhance the growth of the rice crop. It reduces the
1979a,b; Rains and Talley, 1979). Both the methods are in practice under evaporation rate from the rice field, reduces disease occurrence,
Asian conditions, but dual cropping is more in practice as it is reported to suppresses weed growth, enhances flowering fruiting, and increases plant
benefit the rice crop (Talley et al., 1977; Singh, 1979a,b). For application establishment and survival at seedling or transplanting and so on (Biswa
as green manure, Azolla collected from nurseries, ponds or ditches is et al., 2005; Monajjem and Hajipour, 2010). Azolla also reduces the
applied in the field. After 2-3 weeks of application, a thick mat of Azolla intensity of light penetration, water evaporation, and suppress different
can be seen and it is incorporated in the soil. Then, rice can be transplanted weeds like Echinochloa crus-galli, Cyperus spp., Paspalum sp. and so on
in the field. Cattle dung, Slurry or Single Super Phosphate (25-50 kg/ha) and thus, lead to improved crop growth and productivity (Biswa et al.,
can be applied in the field. Pest control measures are to be undertaken in 2005; Monajjem and Hajipour, 2010).
case of pest infestation (Yadav et al., 2014). About 20-40 kg N/ha is
provided by one crop of Azolla application as green manure (Watanabe et 4. CONCLUSION
al., 1977).
The fundamental to successful rice production is the optimum amount of
Azolla green- manuring along with increasing the grain and straw yield, Nitrogen input and Anabaena azollae symbiosis has been known to
also enhanced the number and weight of panicles and reduces the sterility increase nitrogen input in rice cultivation. The amount of rice production
in grains. (Kulasooriya and De Silva, 1977; Singh, 1979a,b). In case of dual will be increased due to the inoculation of nitrogen fixing bacteria.
cropping, fresh inoculum of Azollais applied in the field at the rate of 0.5-1 Therefore, the effective strains of Azollain terms of nitrogen fixation from
ton/ha after the establishment of rice seedling. Single Super Phosphate different agro ecological zones are to be screened and their contribution
(20 kg/ha) can be applied in split doses. A thick mat of Azolla is formed in to rice production needs to be evaluated. Better extension strategies are
about 15-20 days of time. After the decomposition of Azolla in the field, in also the need of hour to promote the use of bio-fertilizer with other
about 8-10 days’ time, it releases the fixed nitrogen. during the crop cycle benefits.Concerted efforts are required from the part of policy makers,
of rice, another crop of Azolla can be raised in a similar way. Each crop scientists and farmers to promoteAzolla as a viable bio-fertilizer for
ofAzolla contributes on an average 30 kg N ha–1in case of dual cropping sustainable rice production.
(Yadav et al., 2014; Watanabe et al., 1977). Azolla dual cropping also helps
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Reviews In Food And Agriculture, 2(1): 04-08.
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Cite The Article: Kripa Adhikari, Sudip Bhandari, Subash Acharya (2021). An Overview Of Azolla In Rice Production: A Review.
Reviews In Food And Agriculture, 2(1): 04-08.