Folia Microbiol (2011) 56:19 DOI 10.

1007/s12223-011-0002-8

Improving Casuarina growth and symbiosis with Frankia under different soil and environmental conditionsreview
W. F. Sayed

Received: 17 January 2011 / Accepted: 17 January 2011 / Published online: 30 March 2011 # Institute of Microbiology, v.v.i, Academy of Sciences of the Czech Republic 2011

Abstract Casuarinas are very important plants for their various uses and survival in adverse sites or harsh environments. As nitrogen fixation, in symbiosis with Frankia, is an important factor for the survival of these plants under various conditions, the basis for selecting both effective and tolerant Frankia strains and Casuarina spp., are provided. Enhancement of the symbiotic relationship between Frankia and Casuarina, by mycorrhizal infection and other biofertilizing microorganisms such as Bacillus and Azospirillum, is reflected by superior plant growth. Casuarina leaf litter is also a great source for both inorganic and organic nutrients. Therefore, careful management of the top soil layer under Casuarina trees is very important. Litter decomposition ratio is affected by many physical chemical and biological factors including temperature, moisture conditions, lignin, and C-to-N and N-to-P ratios in addition to soil biota. In general, here the above relations are discussed and an alleviation model is presented for important disturbances of natural and human origin made in soil and environment, especially in the dry regions. In conclusion, we suggest how to optimize the nitrogen fixation and plant growth under the prevalent conditions.

Introduction Members of the family Casuarinaceae were introduced in many tropic, subtropic, and warm temperate regions for several purposes (National Research Council 1984). Casuarina growth is significantly improved, especially in
W. F. Sayed (*) Department of Botany, Faculty of Science, South Valley University, Qena, Egypt e-mail: farghaly11@lycos.com

poor and nitrogen-deficient soils, through its symbiotic relationship with the nitrogen-fixing actinomycete, Frankia (Barritt and Facelli 2001; Dutta and Agrawal 2001). The use of Casuarina equisetifolia plantations has been shown to improve soil physical and microbiological quality in contaminated soils (Pinyopusarerk and Williams 2000; Izquierdo et al. 2005). Therefore, these symbioses have considerable potential for the role of these plants in soil amelioration as plant growth improves soil in many ways. Improvement involves increasing soil fauna, litterfall quantity, and composition that supplies soil with organic and mineral nutrients and also maintains reasonable moisture levels (Dutta and Agrawal 2001; Gonzalez and Seastdt 2001; Benson et al. 2004). The added organic matter improves soil fertility and structure (see Fig. 1) by processes such as photosynthesis, nitrogen fixation, and nutrient retrieval (Heal et al. 1997; Rajendran 2001). The main subjects discussed here are: (1) the selection of both Casuarina and Frankia for improved plant performance and survival under different conditions; (2) the role of Casuarina plants in soil improvement including litterfall quality, quantity, and decomposition; (3) the benefits of Frankia and other soil biofertilizers and microbiota; and finally, (4) proposed alleviation methods for most of the inhibitory factors that affect Casuarina growth under different conditions especially in the dry regions.

The partners: Casuarina and Frankia The family Casuarinaceae is composed of four genera Casuarina, Allocasuarina, Gymnostoma, and Ceuthostoma (Johnson 1980, 1982, 1988). One of the unique features of the family Casuarinaceae is the highly reduced morphology of vegetative parts, all of which perform the function of

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Fig. 1 Vigorously growing C. equisetifolia surrounding an experimental farm in desert area inside the South Valley University, Qena, Egypt (litter accumulation is in the grey region close to the trees that improve soil quality by adding various nutrients)

photosynthesis (Johnson 1982; Subbarao and RodrguezBarrueco 1995). The importance of Casuarina, in arid areas and poor soils, is illustrated by its various uses (Table 1). Actinomycetes of the genus Frankia form nitrogenfixing nodules on non-leguminous trees and shrubs (including casuarinas) that are collectively called actinorhizal plants (Dawson 2008). Plant infection mechanisms, nodule formation, and structure were considerably discussed (Wall and Berry 2008; Pawlowski 2009). Actinorhizal plants are very important in the process of nitrogen fixation in the inhospitable environments and contaminated soils such as mine spoils and reclaimed land by adding from 2 to 300 kg/ ha N per year to tree environments (Myrold 1994). Some of the Casuarina-infective Frankia strains are highly effective in fixing atmospheric nitrogen leading to a better plant growth in diverse ecosystems (Valdez 2008). Infectivity tests and inoculation of Casuarina plants are carried out by adjusting Frankia protein content to 5.5 g/mL in distilled water and in inoculation of Casuarina seedlings, by injecting the solution into the surrounding soil; the same process is repeated after 1 week (Baker and Schwintzer 1990). Great variations were demonstrated between different Frankia strains in their N2-fixing effectiveness within Casuarina nodules and their role in plant growth especially in poor soils (Sayed et al. 2000; Benson et al. 2004; Izquierdo et al. 2005). Selection of Frankia strains, type of inoculum, and inoculation conditions Inoculation of each Casuarina species with selected Frankia strains is necessary for obtaining effective nitrogen fixation (Mansour 2003; Sayed et al. 2007). Type of inoculum, soil temperature, moisture, and phosphorus content, plus other factors, are very important for Casuarina

nodulation and effective nitrogen fixation by Frankia (Sayed et al. 1997, 2006; Dawson 2008). It was reported that arid environments may have smaller sets of infective Frankia (Benson et al. 2004). This illustrates the need for isolating most of the indigenous strains in soils exposed to these conditions (Sayed 2003; Benson and Dawson 2007). A description of the different types of Frankia inocula is summarized in Table 2. When using pure immobilized cultures, the Frankia protein quantity should not exceed a threshold of 0.5 g/mL of inoculum for successive Frankia growth inside the immobilizing agent (Sayed et al. 2002b). Frankia protein can be determined by the Coomassie blue assay according to Bradford (1976). In general, Frankia strains should be selected to match both environmental conditions and host plant species including toxicity of some metals, temperature, and desiccation (Schwencke and Caru 2001; Sayed et al. 2002b; Mansour 2003). Selection of Casuarina species In addition to selecting the proper Frankia strain, Casuarina species should be also selected for the following purposes: Increased N2 fixation Plants should be efficient in nitrogen fixation, in association with the appropriate Frankia. These plants should also have high tolerance to environmental stresses especially CO2, temperature, water scarcity, contamination, and wind in addition to the usual characteristics of yield, shape, and pest resistance (Diem and Dommergues 1990; Parrotta 1999; Dutta and Agrawal 2001; Sayed 2003; Dawson 2008). Drought tolerance It is related to many factors including plant species, soil water-holding capacity and fertility, and distribution of the rainfall and litterfall in the tested area (National Research Council 1984; Bashkin and Binkley 1998; Parotta 1999). Previous studies indicated that Casuarina obesa, Casuarina cristata subsp. pauper, and Casuarina decaisneana were nominated for drought tolerance with the latter species is probably the best (Diem and Dommergues 1990). Plant yield C. equisetifolia yield of wood is 40120 t/ha per year and about 40 t/ha per year of litter and cones in 10 years (Midgley et al. 1986). Other species should be tested for their yields considering that dual inoculation with Frankia,

Folia Microbiol (2011) 56:19 Table 1 The use of Casuarina trees for different purposesa (1) Timber, construction, and fuel Fences, rafters, poles, lumber, construction, and building in some areas (e.g., Papua New Guinea) Charcoal in developing countries (good firewood of around 7,000 kcal/kg) Simple pieces of furniture (e.g., in Egypt) Hardboards, particle boards, and chipboards Wheels, railroads, tool handles, piano legs, shingles, and panelling (e.g., in Malaysia and Australia)

Pulp wood for paper (e.g., wrapping and printing paper in India) (2) Agroforestry C. equisetifolia as windbreaks, increase crop yield, improve soil structure, and nitrogen content (e.g., in Egypt, China, Senegal, and India) Intercropping with root, cereal, and cash crops (e.g., coffee, peanut, and various grain legumes) Mixed forest plantation with various species (3) Rehabilitation and soil reclamation Shelterbelts in coastal areas (e.g., in China, India, and Vietnam) Reclamation of desertified and industrial-polluted soils (e.g., in Kenya and Malaysia) Rehabilitation of watershed lands as it increases soil nitrogen through symbiosis with Frankia and phosphorus with mycorrhizal fungi, recycle nutrients in soil, reduce weeds, and water loss Sand dune stabilization (e.g., in China, India, Vietnam, Seri Lanka, and Malaysia); C. equisetifolia, C. cunninghamiana, and C. glauca are the best for this purpose. (4) Other uses Young trees as fodders for cattle and sheep where food sources are scarce (assimilating branchlets are significant for its nutritional value); waste products of these animals participate in soil improvement. Landscaping along coast lines in the tropics and subtropics Tolerant to air pollution, used for planting and beautification of roads and river banks in urban areas and cities (C. equisetifolia tolerance is better than other spp.) (5) Non-wood products Casuarina bark contains 618% tannin used for leather tanning (e.g., in Madagascar) and toughening fishing nets in Indonesia Scrapped roots of C. equisetifolia are used as a treatment for dysentery, diarrhea, and stomach aches in Papua New Guinea. Leaf litter is used as mulch to prevent water loss from soil surface while growing annual crops.
a

Compiled from Thiagalingam (1983), National Research Council (1984), Diem and Dommergues (1990), Lemmens and Wulijarni-Soejipto (1992), Pinyopusarerk and House (1993), Subbarao and Rodrguez-Barrueco (1995), Schwencke and Caru (2001), and Zhong et al. (2010)

mycorrhizal fungi, and other biofertilizers will increase yield and growth (Jeffries et al. 2003; Rajendran and Devaraj 2004; Zhong et al. 2010). Salinity tolerance The most tolerant species were C. obesa, Casuarina glauca, and C. equisetifolia, respectively, within the six tested species (Clemens et al. 1983). This was based on the ability of their roots to exclude Na and Cl ions and preventing the transport of these ions to shoots. Casuarina tolerance to salinity was studied in Egypt by Girgis et al. (1992), in China by Yang et al. (2003), and in other parts of the world by Tomar and Minhas (1998), Niknam and McComb (2000), and Tomar et al. (2003). Other factors that affect plant productivity Significant differences in C. equisetifolia productivity, at different sites, result from variations in soil pH, organic

matter content, total N and P content, and moisture (Reddell et al. 1986b; Dawson et al. 1989; Benson and Dawson 2007). The important soil requirements for healthy growth of Casuarina were identified by Yadav (1983) including adequate water depth and frequency (avoiding prolonged water logging), porous and well-drained soil, and adequate nutrient supply (particularly nitrogen). Tillage is important as it improved growth of three Casuarina species in Egypt by improving soil properties (Badran et al. 1976). Studies on the effect of tillage and soil management processes demonstrated that excessive tillage should be avoided because the top soil contains litterfall rich in C and N (Addiscott and Thomas 2000; Slattery and Surapaneni 2002; Mele et al. 2004). Shading had no effect on Casuarina height but the weight of branches and leaves was higher at 100% light intensity (Shafiq et al. 1974). It was also reported that mixed plantations of Casuarina and other trees (e.g., Leucaena) improved tree biomass, litterfall, and nutrient content and reduced the level of root pathogenic fungi (Parrotta 1999; Mele et al. 2004).

4 Liang and Chen (1984) Reddell and Bowen (1985a, b) Borthakur et al. (1996) Sayed et al. (2002b) Borthakur et al. (1996) Sayed et al. (2002b, c) Sayed et al. (2006)

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References

Kohls et al. (1994)

In general, the selected plants should be able to survive waterlogged, dry, poor, contaminated, and saline soils in combination with the suitable N2 fixers (Diem and Dommergues 1990; Dutta and Agrawal 2001; Sayed 2003; Tomar et al. 2003).

The role of Casuarina litter in soil improvement

Require large amounts of nodule material May cause Casuarina wilt due to infection from soil-borne pathogens (e.g. Pseudomonas solanacearum) Containing hyphae, vesicles, spores, or intact culture The correct inoculum ensures plant receipt of the effective strain resulting in increased plant biomass Spores are resistant to higher temperatures and desiccation and can be stored for future inoculation The same advantages of using pure culture in addition to easy handling and extended shelf life under different temperature and moisture conditions Successful immobilizing agents for Frankia are calcium alginate and polyacrylamide gel (PAG)

Decomposition and nutrient release In addition to the increase in carbon and other nutrient contents, trees of C. equisetifolia have a stimulatory effect on plant rhizosphere microfauna and the top layers of soil (Fig. 1), which is correlated to litterfall quantity, quality, and decomposition ratio (Carillo-Garcia et al. 1999; Parotta 1999; Gonzalez and Seastdt 2001; Rajendran 2001; Warren and Zou 2002). Moreover, Heal et al. (1997) defined four aspects of litter quality in relation to decomposition as follows: (1) changes over time in the decomposition variables, (2) variation in litter quality within a species under different site conditions, (3) the biochemical composition of lignin and other polymers, and (4) roots and root exudates. Therefore, the interactions between plant litter quality, quantity, decomposition, and soil biota is very important (Facelli et al. 1999; Nickel et al. 2001; Santo et al. 2002; Sayed et al. 2002a; Zimpfer et al. 2003; Rajendran and Devaraj 2004). Human activities such as excessive tillage or irrigation with saline water will increase soil productivity but will reduce soil quality in future (Waid 1997; Tomar and Minhas 1998; Sayed 2003). Other physical and chemical factors may alter the activities of litter decomposition such as temperature, pH, desiccation, availability of phosphorus, and managing processes (Facelli et al. 1999; Rajendran 2001; Vestgarden 2001; Mele et al. 2004). For C. equisetifolia, high lignin and lignin/N ratios had negative effects on litter decay rate (Jamaludheen and Kumar 1999). Diseases caused by some microorganisms, such as the fungus Fomes durissimus that consumes the lignin of C. equisetifolia wood, will lower the lignin content (Santra and Nandi 1975a, b). In arid and semiarid lands, Casuarina litter add good levels of all nutrients (Schwencke and Caru 2001; Sayed et al. 2002a). These nutrients are added to soil and, if soil surface layer is removed, the result is a decline in soil fertility and the accompanied beneficial processes to Casuarina plantations such as minimizing water loss through evaporation and nodulation (Yadav 1983; Yuehua and Yangyan 1990). Finally, most of the nutrients and organic matter added during C. equisetifolia growth are located in the top 20100 mm of soil and the very high N-to-P ratio

Table 2 Characteristics of different Frankia inocula

2. Pure culturea

3. Immobilized pure intact culture or specific cell typea

1. Crushes nodule

Type of inoculum

The pure, immobilized, or liquid cultures may contain whole cell or specific cell types including hyphae, spores, or vesicles

Containing Frankia, plant debris, and contaminating microorganisms A major cause of variation in Casuarina nodulation in nurseries

Characteristics

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(164:1), indicating that the litter decomposition is limited by phosphorus (Yuehua and Yangyan 1990; Mailly and Margolis 1992; Mele et al. 2004). The introduction of more effective nitrogen-fixing Frankia strains may therefore not improve soil fertility as nodulation itself is reduced by reducing phosphorus level (Yuehua and Yangyan 1990; Wall et al. 2000). Age of plant and direct interaction with litter By using the top soil and leaf extract from three tree species (including Casuarina), the amount of nutrients in the top soil was considered very high and inhibitory for young plant (Srinivasan et al. 1990). Three Frankia strains, in a mixture of soil plus 0.5%, 3%, and 5% (W/W) C. equisetifolia litter, inhibited root nodule formation on 6-week-old seedlings (Sayed et al. 2002a). Growth of all plants was inhibited by these concentrations and only one strain formed very small nodules (strain ORS021001). The same strain showed resistance to metal ion toxicity in other studies (Sayed et al. 2000; Sayed 2003). Therefore, older casuarinas are more efficient in both litter production and nutrient uptake as indicated by the enormous increase in element concentration in the tested Casuarina species (Swaminath and Vadivaj 1989; Rajendran 2001). The older plants also develop other mechanisms for disease resistance. Flavonoids in casuarinas, such as quercetin and kampferol, have an antimicrobial effect

especially against fungi (Siqueira et al. 1991; Sayed and Wheeler 1999). Kaempferol and quercetin, along with other phenolic compounds, were the dominant flavonoids in the tested Casuarina species in Egypt (Saleh and El-Lakany 1979). Phenolic compounds may also limit Frankia colonization compartments inside the host nodule tissues (Laplaze et al. 2000). The added quercetin increased the isolated Frankia colonies, while fungal contaminants were reduced, in the isolation medium (Sayed and Wheeler 1999). Under field conditions, the ratio of litterfall decomposition is suggested to be directly related to the plant defensive action due to the amount of released flavonoids in the surrounding soil (Siqueira et al. 1991; Waid 1997).

Beneficial effects of Frankia, other biofertilizers, and soil biota Most studies on Frankia symbiosis were carried out using pure cultures to avoid contamination with other Frankia in soil (Sayed et al. 2002a, b). More studies using unsterilized soil are required in order to investigate the interaction between soil biota, litter decomposition and Frankia Casuarina symbiosis. The results obtained by Zimpfer et al. (2001, 2003) suggested the positive role of soil microbiota with respect to Frankia and Casuarina nodulation and performance.

Fig. 2 A representative model of the most important factors that affect Casuarina growth and nitrogen fixation with solutions for alleviation (based on: Bearden and Petersen (2000), Caravaca et al. (2002), Diem and Dommergues (1990), Dommergues (1997), Dutta and Agrawal (2001), Facelli et al. (1999), Fleming et al. (1988), Girgis et al. (1992), Gonzalez and Seastdt (2001), Izquierdo et al. (2005), Jamaludheen and Kumar (1999), Kahindi et al. (1997), Parrotta (1999), Rajendran (2001), Rajendran and Devaraj (2004), Reddell et al. (1986a, b; 1997), Sanginga et al. (1989), Sayed et al. (1997, 2000, 2002a, b, 2006, 2008), Schwencke and Caru (2001), Shetty et al. (1994), Slattery and Surapaneni (2002), Tomar et al. (2003), Tian et al. (2002), Warren and Zou (2002), Zhang et al. (2006), and Zhong et al. (2010)). (1), (2), (3), (4), (5) represent the alleviation methods compiled from the available literature leading to higher efficiency of

nitrogen fixation and higher plant growth (the relation between different factors are illustrated by dashed arrows) as follows: (1) Addition of organic soils, recycling organic matter, leaving the top soil layer with litterfall undisturbed, fertilization (especially with phosphorus). (2) Dual inoculation of Casuarina with Frankia and mycorrhizal fungi. (3) Proper irrigation (e.g., proper water amount that is required for each soil and condition) especially for young plants and in dry conditions. (4) Selection of efficient and tolerant Frankia strains and Casuarina spp., planting other N2-fixing trees (mixed plantation, e.g., Lucaenae), inoculation with biofertilizers including Frankia, mycorrhizae, Azospirillum, Phosphobacterium, etc., and selection of the Frankia type of inoculum (whole cell, spores, immobilized infective units, etc.). (5) Liming (supplying Ca and reducing Al)

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Effective mycorrhizal associations with Casuarina is offering other mechanisms for plant survival, mineral nutrition sufficiency, and enhanced nitrogen fixation (Diouf et al. 2003; He et al. 2005; Zhang et al. 2006; Zhong et al. 2010). In general, co-inoculation with Frankia and helper organisms, such as strains belonging to the genera Bacillus, Pseudomonas, Azospirillum, and Phosphobacterium and mycorrhizal fungi increased the Frankia nodulation capacity, biomass of host plants, as well as nutrient uptake and return from litter (Rajendran et al. 2003; Zimpfer et al. 2001, 2003; Rajendran and Devaraj 2004; Solans 2007; Chaia et al. 2010). The use of mycorrhizae also improved plant growth in saline and polluted soils and increased litter decomposition ratio (Oliveira et al. 2001; Kernaghan et al. 2002; Santo et al. 2002). The positive correlation between some dominant rhizospheric bacteria and fungi, on FrankiaCasuarina symbiosis, and plant growth was also confirmed by Sayed et al. (2007, 2008). The increase in catalase activity accompanied with the decrease in malondialdehyde and proline content of Casuarina plants indicated the superiority of indigenous Frankia strains, combined with natural soil microflora, for better plant performance (Sayed et al. 2008).

Conclusions: optimizing Casuarina growth and N2 fixation under extreme conditions Factors that affect Casuarina growth, survival, and nitrogen fixation, in symbiosis with Frankia, can be divided into two categories: (1) Natural factors of soil and environmental conditions such as low water, high temperature, and soil poverty in general (2) Human activities that alter both the environment and soil such as excess tillage, disposal of contaminants or industrial effluents in soil or irrigation water, and other processes that result in soil contamination The suggested model for alleviating these conditions (Fig. 2) is concerned with these two categories that are connected to each other and lead to soil poverty and, usually, plant growth failure. The first priority is to maintain regular and appropriate soil water content, for both of plant survival and Frankia dispersion, accompanied with well-aerated and drained soil conditions (Dawson et al. 1989; Chaia et al. 2010). The five suggested solutions (from 1 to 5 in Fig. 2) were strongly supported by previous studies (see above). The idea is to combine the appropriate solution combination for each environment, as indicated from previous work, to enhance plant productivity and allow more efficient symbiosis under such environment. For example, Casuarina plants can grow well under low

annual rainfall, absence of active microorganisms in soil, N2-poor and contaminated soils if solutions (1) and (4) are available. These include improving soil organic matter and nutrient content along with selecting the tolerant plant species inoculated with the proper combination of microorganisms (see Fig. 2). It is necessary then to have enough information, about the prevalent environmental conditions, soil structure and composition, before suggesting the proper combination (e.g., water, soil amendment technique, type, and content of the inoculum) for each condition (Table 2). For example, water requirements can be reduced if we increase organic matter content, by different additions, and select the appropriate irrigation method (solutions 1 and 3 in Fig. 2). Accordingly, plant growth in dry conditions is not supported by just adding more water but also by improving soil water-holding capacity through organic matter supplement, leaving litterfall on the ground and selecting the tolerant plants and microbes (solutions 1 and 4). Special attention should be drawn on undisturbing the top litterfall layer under older Casuarina with regular irrigation especially for young plants. The suggested alleviation methods are expected to result in the proper decomposition ratio of Casuarina litterfall that support its growth, as in all undisturbed natural environments (solutions 1, 3, and 4). Care should be taken in case of growing plants in the seedling stage in disturbed soils. In other words, these alleviation methods are suitable, under extreme environmental conditions, for young seedlings in undisturbed soils and for older plants in almost all soil types.

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