Improving Casuarina growth and symbiosis with Frankiaunder different soil and environmental conditions—review

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 theirvarious uses and survival in adverse sites or harsh environ-ments. As nitrogen fixation, in symbiosis with Frankia, is animportant factor for the survival of these plants under variousconditions, the basis for selecting both effective and tolerantFrankia strains and Casuarina spp., are provided. Enhance-ment of the symbiotic relationship between Frankia andCasuarina, by mycorrhizal infection and other biofertilizingmicroorganisms such as Bacillus and Azospirillum, isreflected by superior plant growth. Casuarina leaf litter isalso a great source for both inorganic and organic nutrients.Therefore, careful management of the top soil layer underCasuarina trees is very important. Litter decomposition ratiois affected by many physical chemical and biological factorsincluding temperature, moisture conditions, lignin, and C-to-Nand N-to-P ratios in addition to soil biota. In general, here theabove relations are discussed and an alleviation model ispresented for important disturbances of natural and humanorigin made in soil and environment, especially in the dryregions. In conclusion, we suggest how to optimize thenitrogen fixation and plant growth under the prevalentconditions.

Introduction

Members of the family Casuarinaceae were introduced inmany tropic, subtropic, and warm temperate regions forseveral purposes (National Research Council 1984).Casuarina growth is significantly improved, especially in

poor and nitrogen-deficient soils, through its symbioticrelationship with the nitrogen-fixing actinomycete,Frankia (Barritt and Facelli 2001; Dutta and Agrawal2001). The use of Casuarina equisetifolia plantations hasbeen shown to improve soil physical and microbiologicalquality in contaminated soils (Pinyopusarerk and Williams2000; Izquierdo et al. 2005). Therefore, these symbioseshave considerable potential for the role of these plants insoil amelioration as plant growth improves soil in manyways. Improvement involves increasing soil fauna, litter-fall quantity, and composition that supplies soil withorganic and mineral nutrients and also maintains reason-able moisture levels (Dutta and Agrawal 2001; Gonzalezand Seastdt 2001; Benson et al. 2004). The added organicmatter improves soil fertility and structure (see Fig. 1) byprocesses such as photosynthesis, nitrogen fixation, andnutrient retrieval (Heal et al. 1997; Rajendran 2001).

The main subjects discussed here are: (1) the selection ofboth Casuarina and Frankia for improved plant perfor-mance and survival under different conditions; (2) the roleof Casuarina plants in soil improvement including litterfallquality, quantity, and decomposition; (3) the benefits ofFrankia and other soil biofertilizers and microbiota; andfinally, (4) proposed alleviation methods for most of theinhibitory factors that affect Casuarina growth underdifferent conditions especially in the dry regions.

The partners: Casuarina and Frankia

The family Casuarinaceae is composed of four generaCasuarina, Allocasuarina, Gymnostoma, and Ceuthostoma(Johnson 1980, 1982, 1988). One of the unique features ofthe family Casuarinaceae is the highly reduced morphologyof vegetative parts, all of which perform the function of

W. F. Sayed (*)Department of Botany, Faculty of Science,South Valley University,Qena, Egypte-mail: farghaly11@lycos.com

Folia Microbiol (2011) 56:1–9DOI 10.1007/s12223-011-0002-8

photosynthesis (Johnson 1982; Subbarao and Rodríguez-Barrueco 1995). The importance of Casuarina, in arid areasand poor soils, is illustrated by its various uses (Table 1).

Actinomycetes of the genus Frankia form nitrogen-fixing nodules on non-leguminous trees and shrubs (in-cluding casuarinas) that are collectively called actinorhizalplants (Dawson 2008). Plant infection mechanisms, noduleformation, and structure were considerably discussed (Walland Berry 2008; Pawlowski 2009). Actinorhizal plants arevery important in the process of nitrogen fixation in theinhospitable environments and contaminated soils such asmine 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 arehighly effective in fixing atmospheric nitrogen leading to abetter plant growth in diverse ecosystems (Valdez 2008).Infectivity tests and inoculation of Casuarina plants arecarried out by adjusting Frankia protein content to5.5 μg/mL in distilled water and in inoculation ofCasuarina seedlings, by injecting the solution into thesurrounding soil; the same process is repeated after 1 week(Baker and Schwintzer 1990). Great variations weredemonstrated between different Frankia strains in theirN2-fixing effectiveness within Casuarina nodules andtheir role in plant growth especially in poor soils (Sayedet 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 selectedFrankia strains is necessary for obtaining effective nitrogenfixation (Mansour 2003; Sayed et al. 2007). Type ofinoculum, soil temperature, moisture, and phosphorus con-tent, plus other factors, are very important for Casuarina

nodulation and effective nitrogen fixation by Frankia (Sayedet al. 1997, 2006; Dawson 2008). It was reported that aridenvironments may have smaller sets of infective Frankia(Benson et al. 2004). This illustrates the need for isolatingmost of the indigenous strains in soils exposed to theseconditions (Sayed 2003; Benson and Dawson 2007). Adescription of the different types of Frankia inocula issummarized in Table 2.

When using pure immobilized cultures, the Frankia proteinquantity should not exceed a threshold of 0.5 μg/mL ofinoculum for successive Frankia growth inside the immobi-lizing agent (Sayed et al. 2002b). Frankia protein can bedetermined by the Coomassie blue® assay according toBradford (1976).

In general, Frankia strains should be selected to matchboth environmental conditions and host plant speciesincluding toxicity of some metals, temperature, anddesiccation (Schwencke and Caru 2001; Sayed et al.2002b; Mansour 2003).

Selection of Casuarina species

In addition to selecting the proper Frankia strain, Casuarinaspecies should be also selected for the following purposes:

Increased N2 fixation

Plants should be efficient in nitrogen fixation, inassociation with the appropriate Frankia. These plantsshould also have high tolerance to environmental stressesespecially CO2, temperature, water scarcity, contamina-tion, and wind in addition to the usual characteristics ofyield, shape, and pest resistance (Diem and Dommergues1990; Parrotta 1999; Dutta and Agrawal 2001; Sayed2003; Dawson 2008).

Drought tolerance

It is related to many factors including plant species, soilwater-holding capacity and fertility, and distribution of therainfall and litterfall in the tested area (National ResearchCouncil 1984; Bashkin and Binkley 1998; Parotta 1999).Previous studies indicated that Casuarina obesa, Casuarinacristata subsp. pauper, and Casuarina decaisneana werenominated for drought tolerance with the latter species isprobably the best (Diem and Dommergues 1990).

Plant yield

C. equisetifolia yield of wood is 40–120 t/ha per year andabout 40 t/ha per year of litter and cones in 10 years(Midgley et al. 1986). Other species should be tested fortheir yields considering that dual inoculation with Frankia,

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

2 Folia Microbiol (2011) 56:1–9

mycorrhizal fungi, and other biofertilizers will increaseyield and growth (Jeffries et al. 2003; Rajendran andDevaraj 2004; Zhong et al. 2010).

Salinity tolerance

The most tolerant species were C. obesa, Casuarinaglauca, and C. equisetifolia, respectively, within the sixtested species (Clemens et al. 1983). This was based on theability of their roots to exclude Na and Cl ions andpreventing the transport of these ions to shoots. Casuarinatolerance to salinity was studied in Egypt by Girgis et al.(1992), in China by Yang et al. (2003), and in other parts ofthe world by Tomar and Minhas (1998), Niknam andMcComb (2000), and Tomar et al. (2003).

Other factors that affect plant productivity

Significant differences in C. equisetifolia productivity, atdifferent sites, result from variations in soil pH, organic

matter content, total N and P content, and moisture (Reddellet al. 1986b; Dawson et al. 1989; Benson and Dawson2007). The important soil requirements for healthy growthof Casuarina were identified by Yadav (1983) includingadequate water depth and frequency (avoiding prolongedwater logging), porous and well-drained soil, and adequatenutrient supply (particularly nitrogen). Tillage is importantas it improved growth of three Casuarina species in Egyptby improving soil properties (Badran et al. 1976). Studieson the effect of tillage and soil management processesdemonstrated that excessive tillage should be avoidedbecause the top soil contains litterfall rich in C and N(Addiscott and Thomas 2000; Slattery and Surapaneni2002; Mele et al. 2004). Shading had no effect onCasuarina height but the weight of branches and leaveswas higher at 100% light intensity (Shafiq et al. 1974). Itwas also reported that mixed plantations of Casuarina andother trees (e.g., Leucaena) improved tree biomass, litter-fall, and nutrient content and reduced the level of rootpathogenic fungi (Parrotta 1999; Mele et al. 2004).

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, recyclenutrients 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 thebest 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); wasteproducts 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 isbetter than other spp.)

(5) Non-wood products

▪ Casuarina bark contains 6–18% 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 Rodríguez-Barrueco (1995), Schwencke and Caru (2001), and Zhong et al. (2010)

Folia Microbiol (2011) 56:1–9 3

In general, the selected plants should be able to survivewaterlogged, dry, poor, contaminated, and saline soils incombination with the suitable N2 fixers (Diem andDommergues 1990; Dutta and Agrawal 2001; Sayed2003; Tomar et al. 2003).

The role of Casuarina litter in soil improvement

Decomposition and nutrient release

In addition to the increase in carbon and other nutrientcontents, trees of C. equisetifolia have a stimulatory effecton 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; Parotta1999; Gonzalez and Seastdt 2001; Rajendran 2001; Warrenand Zou 2002). Moreover, Heal et al. (1997) defined fouraspects of litter quality in relation to decomposition asfollows: (1) changes over time in the decompositionvariables, (2) variation in litter quality within a speciesunder different site conditions, (3) the biochemical compo-sition of lignin and other polymers, and (4) roots and rootexudates. Therefore, the interactions between plant litterquality, quantity, decomposition, and soil biota is veryimportant (Facelli et al. 1999; Nickel et al. 2001; Santo etal. 2002; Sayed et al. 2002a; Zimpfer et al. 2003; Rajendranand Devaraj 2004).

Human activities such as excessive tillage or irrigationwith saline water will increase soil productivity but willreduce soil quality in future (Waid 1997; Tomar and Minhas1998; Sayed 2003).

Other physical and chemical factors may alter theactivities of litter decomposition such as temperature, pH,desiccation, availability of phosphorus, and managingprocesses (Facelli et al. 1999; Rajendran 2001; Vestgarden2001; Mele et al. 2004). For C. equisetifolia, high ligninand lignin/N ratios had negative effects on litter decay rate(Jamaludheen and Kumar 1999). Diseases caused by somemicroorganisms, such as the fungus Fomes durissimus thatconsumes the lignin of C. equisetifolia wood, will lower thelignin content (Santra and Nandi 1975a, b).

In arid and semiarid lands, Casuarina litter add goodlevels of all nutrients (Schwencke and Caru 2001; Sayed etal. 2002a). These nutrients are added to soil and, if soilsurface layer is removed, the result is a decline in soilfertility and the accompanied beneficial processes toCasuarina plantations such as minimizing water lossthrough evaporation and nodulation (Yadav 1983; Yuehuaand Yangyan 1990).

Finally, most of the nutrients and organic matteradded during C. equisetifolia growth are located in thetop 20–100 mm of soil and the very high N-to-P ratioT

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4 Folia Microbiol (2011) 56:1–9

(164:1), indicating that the litter decomposition is limitedby phosphorus (Yuehua and Yangyan 1990; Mailly andMargolis 1992; Mele et al. 2004). The introduction ofmore effective nitrogen-fixing Frankia strains may there-fore not improve soil fertility as nodulation itself isreduced by reducing phosphorus level (Yuehua andYangyan 1990; Wall et al. 2000).

Age of plant and direct interaction with litter

By using the top soil and leaf extract from three treespecies (including Casuarina), the amount of nutrients inthe top soil was considered very high and inhibitory foryoung plant (Srinivasan et al. 1990). Three Frankiastrains, in a mixture of soil plus 0.5%, 3%, and 5% (W/W)C. equisetifolia litter, inhibited root nodule formation on6-week-old seedlings (Sayed et al. 2002a). Growth of allplants was inhibited by these concentrations and only onestrain formed very small nodules (strain ORS021001). Thesame strain showed resistance to metal ion toxicity inother studies (Sayed et al. 2000; Sayed 2003). Therefore,older casuarinas are more efficient in both litter productionand nutrient uptake as indicated by the enormous increasein element concentration in the tested Casuarina species(Swaminath and Vadivaj 1989; Rajendran 2001).

The older plants also develop other mechanisms fordisease resistance. Flavonoids in casuarinas, such asquercetin and kampferol, have an antimicrobial effect

especially against fungi (Siqueira et al. 1991; Sayed andWheeler 1999). Kaempferol and quercetin, along with otherphenolic compounds, were the dominant flavonoids in thetested Casuarina species in Egypt (Saleh and El-Lakany1979). Phenolic compounds may also limit Frankiacolonization compartments inside the host nodule tissues(Laplaze et al. 2000). The added quercetin increased theisolated Frankia colonies, while fungal contaminants werereduced, in the isolation medium (Sayed and Wheeler1999). Under field conditions, the ratio of litterfalldecomposition is suggested to be directly related to theplant defensive action due to the amount of releasedflavonoids 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 usingpure cultures to avoid contamination with other Frankia insoil (Sayed et al. 2002a, b). More studies using unsterilizedsoil are required in order to investigate the interactionbetween soil biota, litter decomposition and Frankia–Casuarina symbiosis. The results obtained by Zimpfer etal. (2001, 2003) suggested the positive role of soil micro-biota with respect to Frankia and Casuarina nodulation andperformance.

Fig. 2 A representative model of the most important factors thataffect Casuarina growth and nitrogen fixation with solutions foralleviation (based on: Bearden and Petersen (2000), Caravaca et al.(2002), Diem and Dommergues (1990), Dommergues (1997), Duttaand Agrawal (2001), Facelli et al. (1999), Fleming et al. (1988), Girgiset 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 etal. (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 methodscompiled from the available literature leading to higher efficiency of

nitrogen fixation and higher plant growth (the relation betweendifferent factors are illustrated by dashed arrows) as follows: (1)Addition of organic soils, recycling organic matter, leaving the top soillayer with litterfall undisturbed, fertilization (especially with phos-phorus). (2) Dual inoculation of Casuarina with Frankia andmycorrhizal fungi. (3) Proper irrigation (e.g., proper water amountthat is required for each soil and condition) especially for young plantsand in dry conditions. (4) Selection of efficient and tolerant Frankiastrains and Casuarina spp., planting other N2-fixing trees (mixedplantation, e.g., Lucaenae), inoculation with biofertilizers includingFrankia, mycorrhizae, Azospirillum, Phosphobacterium, etc., andselection of the Frankia type of inoculum (whole cell, spores,immobilized infective units, etc.). (5) Liming (supplying Ca andreducing Al)

Folia Microbiol (2011) 56:1–9 5

Effective mycorrhizal associations with Casuarina isoffering other mechanisms for plant survival, mineralnutrition sufficiency, and enhanced nitrogen fixation (Dioufet al. 2003; He et al. 2005; Zhang et al. 2006; Zhong et al.2010). In general, co-inoculation with Frankia and “helperorganisms,” such as strains belonging to the genera Bacillus,Pseudomonas, Azospirillum, and Phosphobacterium andmycorrhizal fungi increased the Frankia nodulation capacity,biomass of host plants, as well as nutrient uptake and returnfrom 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 growthin saline and polluted soils and increased litter decomposi-tion ratio (Oliveira et al. 2001; Kernaghan et al. 2002; Santoet al. 2002).

The positive correlation between some dominant rhizo-spheric bacteria and fungi, on Frankia–Casuarina symbi-osis, and plant growth was also confirmed by Sayed et al.(2007, 2008). The increase in catalase activity accompaniedwith the decrease in malondialdehyde and proline contentof Casuarina plants indicated the superiority of indigenousFrankia strains, combined with natural soil microflora, forbetter plant performance (Sayed et al. 2008).

Conclusions: optimizing Casuarina growth and N2

fixation under extreme conditions

Factors that affect Casuarina growth, survival, and nitrogenfixation, in symbiosis with Frankia, can be divided into twocategories:

(1) Natural factors of soil and environmental conditionssuch as low water, high temperature, and soil povertyin general

(2) Human activities that alter both the environment andsoil such as excess tillage, disposal of contaminants orindustrial effluents in soil or irrigation water, and otherprocesses that result in soil contamination

The suggested model for alleviating these conditions(Fig. 2) is concerned with these two categories that areconnected to each other and lead to soil poverty and,usually, plant growth failure. The first priority is tomaintain regular and appropriate soil water content, forboth of plant survival and Frankia dispersion, accompaniedwith 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 previousstudies (see above). The idea is to combine the appropriatesolution combination for each environment, as indicatedfrom previous work, to enhance plant productivity andallow 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) areavailable. These include improving soil organic matter andnutrient content along with selecting the tolerant plantspecies inoculated with the proper combination of micro-organisms (see Fig. 2). It is necessary then to have enoughinformation, about the prevalent environmental conditions,soil structure and composition, before suggesting the propercombination (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 weincrease organic matter content, by different additions, andselect the appropriate irrigation method (solutions 1 and 3in Fig. 2). Accordingly, plant growth in dry conditions isnot supported by just adding more water but also byimproving soil water-holding capacity through organicmatter supplement, leaving litterfall on the ground andselecting the tolerant plants and microbes (solutions 1 and4). Special attention should be drawn on undisturbing thetop litterfall layer under older Casuarina with regularirrigation especially for young plants. The suggestedalleviation methods are expected to result in the properdecomposition ratio of Casuarina litterfall that support itsgrowth, as in all undisturbed natural environments(solutions 1, 3, and 4). Care should be taken in case ofgrowing plants in the seedling stage in disturbed soils. Inother words, these alleviation methods are suitable, underextreme environmental conditions, for young seedlings inundisturbed soils and for older plants in almost all soiltypes.

References

Addiscott TM, Thomas D (2000) Tillage, mineralization and leaching:phosphate. Soil Tillage Res 53:255–273

Badran OA, El-Lakany MH, El-Osta ML, Abo Gazia HA (1976)Breeding and improving Casuarina trees, I. Taxonomy andmorphological characteristics of Casuarina spp. grown in Egypt.Alex J Agric Res 24:683–694

Baker DD, Schwintzer CR (1990) Introduction. In: Schwintzer CR,Tjepkema JD (eds) The biology of Frankia and actinorhizalplants. Academic, New York, NY

Barritt AR, Facelli JM (2001) Effects of Casuarina pauper litter andgrove soil on emergence and growth of understorey species inarid land of South Australia. J Arid Environ 49:569–579

Bashkin MA, Binkley D (1998) Changes in soil carbon followingafforestation in Hawaii. Ecology 79:828–833

Bearden BN, Petersen L (2000) Influence of arbuscular mycorrhizalfungi on soil structure and aggregate stability of vertisols. PlantSoil 218:173–183

Benson DR, Dawson JO (2007) Recent advances in the biography andgenecology of symbiotic Frankia and its host plants. PhysiolPlant 130:318–330

Benson DR, Van den Heuvel BD, Potter D (2004) Actinorhizalsymbiosis: diversity and biography. In: Gillings M, Holmes A

6 Folia Microbiol (2011) 56:1–9

(eds) Plant microbiology. Garland Science/BIOS Publishers,Oxford, pp 99–129

Borthakur M, Sen A, Misra AK (1996) Immobilized Frankia sporesremained viable on dry storage and on restoration to mediumregenerated active colonies. Plant Soil 181:227–231

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

Caravaca F, Hernandez MT, Garcia C, Roldan A (2002) Improvementof rhizosphere aggregates stability of afforested semi-arid plantspecies subjected to mycorrhizal inoculation and compostaddition. Geoderma 108:133–144

Carillo-Garcia A, de la Luz JL, Bashan Y, Bethlenfalvay GJ (1999)Nurse plants, mycorrhizae, and plant establishment in a disturbedarea of the Sonoran Desert. Restor Ecol 7:321–335

Chaia EE, Wall LG, Huss-Danell K (2010) Life in soil by theactinorhizal root nodule endophyte Frankia. A review. Symbiosis51:201–226

Clemens J, Campbell LC, Nurisjah S (1983) Germination, growth andmineral ion concentrations of Casuarina species under salineconditions. Aust J Bot 31:1–9

Dawson JO (2008) Ecology of actinorhizal plants. In: Pawlowski K,Newton WE (eds) Nitrogen fixing actinorhizal symbioses.Springer, Berlin, Germany, pp 199–234

Dawson JO, Kowalski DG, Dart PJ (1989) Variation with soil depth,topographic position and host species in the capacity of soilsfrom an Australian locale to nodulate Casuarina and Allocasuar-ina seedlings. Plant Soil 118:1–11

Diem HG, Dommergues YR (1990) Current and potential uses andmanagement of Casuarinaceae in the tropics and subtopics. In:Schwintzer CR, Tjepkema JD (eds) The biology of Frankia andactinorhizal plants. Academic, New York, pp 317–342

Diouf D, Diop TA, Ndoye I (2003) Actinorhizal, mycorhizal and rhizobialsymbioses: how much do we know? Afric J Biotechnol 2:1–7

Dommergues YR (1997) Contribution of actinorhizal plants to tropicalsoil productivity and rehabilitation. Soil Biol Biochem 29:931–941

Dutta RK, Agrawal M (2001) Litterfall, litter decomposition andnutrient release in five exotic plant species planted in coal minespoils. Pedobiologia 45:298–312

Facelli JM, Williams R, Fricker S, Ladd B (1999) Establishment andgrowth of seedlings of Eucalyptus obliqua: interactive effects oflitter, water and pathogens. Austral J Ecol 24:484–494

Fleming AI, Williams ER, Turnbull JW (1988) Growth and nodulationof provenances of Casuarina cunninghamiana inoculated with arange of Frankia sources. Austral J Bot 30:171–181

Girgis MGZ, Ishac YZ, Diem HG, Dommergues YR (1992) Selectionof salt tolerant Casuarina glauca and Frankia. Acta Oecol13:443–451

Gonzalez G, Seastdt TR (2001) Soil fauna and plant litter decompo-sition in tropical and subalpine forests. Ecology 82:955–964

He X, Critchley C, Ng H, Bledsoe C (2005) Nodulated N2-fixingCasuarina cunninghamiana in the sink for net N transfer fromnon-N2-fixing Eucalyptus maculata via an ectomycorrhizalfungus Pisolithus sp. using 15NH4

+ or 15NO3− supplied as

ammonium nitrate. New Phytol 167:897–912Heal OW, Anderson JM, Swift MJ (1997) Plant litter quality and

decomposition: an historical overview. In: Cadisch G, Giller KE(eds) Driven by nature: plant litter quality and decomposition.CAB International, Wallingford (UK), pp 3–30

Izquierdo L, Caravaca F, Alguacil MM, Hernandez G, Roldan A(2005) Use of microbiological indicators for evaluating successin soil restoration after revegetation of a mining area undersubtropical conditions. Appl Soil Ecol 30:3–10

Jamaludheen V, Kumar BM (1999) Litter of multipurpose trees inKerala, India: variations in the amount, quality, decay rates andrelease of nutrients. For Ecol Manag 115:1–11

Jeffries P, Gianinazzi S, Perotto S, Turnau K, Barea JM (2003) Thecontribution of arbuscular mycorhizal fungi in sustainable mainte-nance of plant health and soil fertility. Biol Fertil Soils 37:1–16

Johnson LAS (1980) Notes on Casuarinaceae I. Telopea 2:83–84Johnson LAS (1982) Notes on Casuarinaceae II. J Adel Bot Gard

6:73–87Johnson LAS (1988) Notes on Casuarinaceae III. The new genus

Ceuthostoma. Telopea 3:133–137Kahindi JHP, Woomer P, George T, de Souza MFM, Karanja NK,

Giller KE (1997) Agricultural intensification, soil biodiversityand ecosystem function in the tropics: the role of nitrogen-fixingbacteria. Appl Soil Ecol 6:55–76

Kernaghan G, Hambling B, Fung M, Khasa D (2002) In vitroselection of boreal ectomycorhizal fungi for use in reclamation ofsaline–alkaline habitats. Restor Ecol 10:43–51

Kohls SJ, Thimmapuram JC, Buschens CA, Paschke MW, Dawson JO(1994) Nodulation patterns of actinorhizal plants in the familyRosaceae. Plant Soil 162:229–239

Laplaze L, Gherbi H, Frutz T, Pawlowski K, Franche C, Macheix J-J,Auguy F, Bogusz D, Duhoux G (2000) Flavan-containing cellsdelimit Frankia infected compartments in Casuarina glaucanodules. In: Pedrosa FO et al (eds) Nitrogen fixation: frommolecules to crop productivity. Kluwer Academic Publishers,Dordrecht, pp 455–456

Lemmens RHMJ, Wulijarni-Soetjipto N (1992) Plant resources ofSouth-East Asia No. 3: dye and tannin producing plants.PROSEA Foundation, Bogor (Indonesia)

Liang ZC, Chen XH (1984) Selection of clones of Casuarina forresistance to bacterial wilt. J South China Agric Coll 5:53–59

Mailly D, Margolis HA (1992) Forest floor mineral soil improvementin Casuarina equisetifolia plantations on the coastal sand dunesin Senegal. For Ecol Manag 55:259–278

Mansour SR (2003) Survival of Frankia strains under different soilconditions. Online J Biol Sci 3:618–626

Mele PM, Yunusa IAM, Kingston KB, Rab MA (2004) Response ofsoil fertility indices to a short phase of Australian woody species,continuous annual crop rotations or a permanent pasture. SoilTillage Res 72:21–30

Midgley SJ, Turnbull WJ, Hartney VJ (1986) Fuel-wood species forsalt affected sites. Reclam Reveg Res 5:285–303

Myrold DD (1994) Frankia and the actinorhizal symbiosis. In:Weaver RW et al (eds) Methods of soil analysis, part 2:microbiological and biochemical properties. Soil Sci Soc Amer-ica, Madison, WI, USA, pp 291–328

National Research Council (1984) Casuarina: nitrogen-fixing trees foradverse sites. Natl Acad Sci USA, Washington, DC

Nickel A, Pelz O, Hahn D, Saurer M, Siegwolf R, Zeyer J (2001)Effect of inoculation and leaf litter amendment on establishmentof nodule-forming Frankia populations in soil. Appl EnvironMicrobiol 67:2603–2609

Niknam SR, McComb J (2000) Salt tolerance screening of selectedAustralian woody species—a review. For Ecol Manag 139:1–19

Oliveira RS, Dodd JC, Castro PML (2001) The mycorhizal status ofPhragmites australis in several polluted soils and sediments of anindustrialized region of Northern Portugal. Mycorrhiza 10:241–247

Parrotta JA (1999) Productivity, nutrient recycling, and succession insingle- and mixed-species plantations of Casuarina equisetifolia,Eucalyptus robusta, and Lucaena leucocephala in Puerto Rico.For Ecol Manag 124:45–77

Pawlowski K (2009) Induction of actinorhizal nodules by Frankia.Microbiol Monogr 8:127–154

Pinyopusarerk K, House APN (1993) Casuarina: an annotated bibliog-raphy of C. equisetifolia, C. cunninghamiana and C. oligodon.International Center for Research in Agroforestry, Nairobi

Pinyopusarerk K, Williams ER (2000) Range-wide provenancevariation in growth and morphological characteristics of Casuarina

Folia Microbiol (2011) 56:1–9 7

equisetifolia growth in Northern Australia. For Ecol Manag134:219–232

Rajendran K (2001) Litter production and nutrient return in an ageseries of Casuarina equisetifolia in the East Coast of India. AsianJ Microbiol Biotechnol Environ Sci 3:87–90

Rajendran K, Devaraj P (2004) Biomass and nutrient distribution andtheir return of Casuarina equisetifolia inoculated with biofertil-izers in farm land. Biomass Bioenergy 26:235–249

Rajendran K, Sugavanam V, Devaraj P (2003) Effect of microbialinoculation on quality seedling production of Casuarina equi-setifolia. Trop Forest Sci 15:82–96

Reddell P, Bowen GD (1985a) Host–Frankia specificity within theCasuarinaceae. Plant Soil 93:293–298

Reddell P, Bowen GD (1985b) Frankia source affects growth,nodulation and nitrogen fixation in Casuarina species. NewPhytol 100:115–122

Reddell P, Foster RC, Bowen GD (1986a) The effects of sodiumchloride on growth and nitrogen fixation in Casuarina obesaMiq. New Phytol 102:397–408

Reddell P, Bowen GD, Robson AD (1986b) Nodulation of Casuar-inaceae in relation to host species and soil properties. Austral JBot 34:435–444

Reddell P, Yun Y, Shipton WA (1997) Do Casuarina cunninghamianaseedlings dependent on symbiotic N2 fixation have higherphosphorus requirements than those supplied with adequatefertilizer nitrogen. Plant Soil 189:213–219

Saleh NAM, El-Lakany MH (1979) A quantitative variation in theflavonoids and phenolics of some Casuarina species. BiochemSyst Ecol 7:13–15

Sanginga N, Danso SKA, Bowen GD (1989) Nodulation and growthresponse of Allocasuarina and Casuarina species to phosphorusfertilization. Plant Soil 118:125–132

Santo AVD, Ruigliano FA, Berg B, Fioretto A, Puppi G, Alfani A (2002)Fungal mycelium and decomposition of needle litter in threecontrasting coniferous forests. Acta Oecol Int J Ecol 23:247–259

Santra S, Nandi B (1975a) Decomposition of lignin and cellulosecomponents of wood of Swietenia mahagoni, Casuarinaequisetifolia and Mimusops elegani by Fomes durissimusLloyd. Holzforschung 29:205–209

Santra S, Nandi B (1975b) Microstructural and microchemical studiesof wood decay of Casuarina equisetifolia by Fomes durissimus.Transact British Mycol Soc 65:507–509

Sayed WF (2003) Effects of land irrigation with partially-treatedwastewater on Frankia survival and infectivity. Plant Soil254:19–25

Sayed WF, Wheeler CT (1999) Effect of the flavonoid quercetin onculture and isolation of Frankia from Casuarina root nodules.Folia Microbiol 44:59–62

Sayed WF, Wheeler CT, Zahran HH, Shoreit AAM (1997) Effect oftemperature and soil moisture on the survival and symbioticeffectiveness of Frankia spp. Biol Fertil Soils 25:349–353

Sayed WF, Mohawad SM, Abd El-Karim MM (2000) Effect of Al,Co, and Pb ions on growth of Frankia spp. in a mineral medium.Folia Microbiol 45:153–156

Sayed WF, EL-Sharouny HM, Zahran HH, Ali WM (2002a) Composi-tion of Casuarina leaf litter and its influence on Frankia–Casuarina symbiosis in soil. Folia Microbiol 47:429–434

Sayed WF, EL-Sharouny HM, Zahran HH, Ali WM (2002b) Changesin growth of Frankia strains, its infectivity and effectiveness onCasuarina equisetifolia after incubation at high temperatures anddifferent desiccation regimes. Proc 2nd Intl Conf Biol Sci TantaUniv, Egypt 2:478–490

SayedWF,Wheeler CT, El-SharounyHM,Mohawad SM, Abd El-KarimMM (2002c) Effects of storage time and temperature on theinfectivity and effectiveness of Frankia entrapped in poly-acrylamide gel. Folia Microbiol 47:545–550

Sayed WF, Zahran HH, Salem WM (2006) The use of Frankia sporesas inocula for Casuarina equisetifolia plants. Catrina 1:67–73

Sayed WF, Zahran HH, Salem WM (2007) Dominant rhizosphericmicroorganisms under some casuarinas and its effect on Frankiagrowth and nodulation capacity. Egypt J Biotechnol 2:201–218

Sayed WF, Zahran HH, Salem WM (2008) Rhizospheric microbiotaand Frankia–Casuarina symbiosis. Catrina 3:101–110

Schwencke J, Caru M (2001) Advances in actinorhizal symbiois: hostplant–Frankia interactions, biology, and applications in arid landreclamation. A review. Arid Land Res Manag 15:285–327

Shafiq Y, Dahab AMA, Omran F (1974) Effects of light intensity onthe growth of seedlings of Pinus brutia, Cupressus simpervirensand Casuarina equisetifolia. Iraqi J Agric Sci Zanco 9:73–85

Shetty KG, Hetrick BAD, Figge DAH, Schwab AP (1994) Effects ofmycorrhizae and other soil microbes on revegetation of heavymetal contaminated mine spoil. Environ Pollut 86:181–188

Siqueira JO, Nair MG, Hmmerschmidt R, Safir GR (1991) Signifi-cance of phenolic compounds in plant–soil–microbial systems.CRC Plant Sci 10:63–121

Slattery WJ, Surapaneni A (2002) Effect of soil management practiceson the sequestration of carbon in duplex soils of SouthernAustralia. In: Kimble JM, Lal R, Follett RF (eds) Agriculturalpractices and policies for carbon sequestration in soil. LewisPublic, Washington, DC, pp 107–117

Solans M (2007) Discaria trinervis–Frankia symbiosis promotion bysaprophytic actinomycetes. J Basic Microbiol 47:297–303

Srinivasan K, Ramasamy M, Shantha R (1990) Tolerance of pulsecrops to allelochemicals of tree species. Ind J Pul Res 3:40–44

Subbarao NS, Rodriguez-Barrueco C (1995) Casuarinas. SciencePublishers, Inc, Lebanon, NH, USA, p 240

Swaminath MH, Vadivaj BA (1989) Studies on the N, P, and K uptakeby forestry species under irrigated and unirrigated conditions.Myforest 25:135–143

Thiagalingam K (1983) Role of Casuarina in agroforestry. In:Midgley SJ, Turnbull JW, Johnston RD (eds) Casuarina ecology,management and utilization. CSIRO, Melbourne, pp 175–177

Tian C, He X, Zhong Y, Chen J (2002) Effects of VA mycorrhizae andFrankia dual inoculation on growth and nitrogen fixation ofHippophae tibetana. For Ecol Manag 170:307–312

Tomar OS, Minhas PS (1998) Afforestation of salt-affected soils. In:Tyagi NK, Minhas PS (eds) Agricultural salinity management inIndia. Salinity Research Institute, Karnal, India, pp 453–472

Tomar OS, Minhas PS, Sharma VK, Singh YP, Gupta RK (2003)Performance of 31 tree species and soil conditions in a plantationestablished with saline irrigation. For Ecol Manag 177:333–346

Valdez M (2008) Frankia ecology. In: Pawlowski K, Newton WE(eds) Nitrogen fixing actinorhizal symbioses. Springer, Berlin,Germany, pp 49–72

Vestgarden LS (2001) Carbon and nitrogen turnover in the early stagesof Scots pine (Pinus sylvestris L.) needle litter decomposition:effects of internal and external nitrogen. Soil Biol Biochem33:465–474

Waid JS (1997) Metabolic interactions in plant litter systems. In: HealOW, Anderson JM, Swift MJ (eds) Driven by nature: plant litterquality and decomposition. CAB International, Wallingford, UK,pp 145–153

Wall LG, Berry AM (2008) Early interactions, infection andnodulation in actinorhizal symbiosis. In: Pawlowski K, NewtonWE (eds) Nitrogen fixing actinorhizal symbioses. Springer,Berlin, Germany, pp 147–166

Wall LG, Hellsten A, Huss-Danell K (2000) Nitrogen, phosphorus,and the ratio between them affect nodulation in Alnus incana andTrifolium pretense. Symbiosis 29:91–105

Warren MW, Zou X (2002) Soil macrofauna and litter nutrients inthree tropical tree plantations on a disturbed site in Puerto Rico.For Ecol Manag 170:161–171

8 Folia Microbiol (2011) 56:1–9

Yadav JSP (1983) Soil limitations for successful establishment andgrowth of Casuarina plantations. In: Midgley SJ, Turnbull JW,Johnston RD (eds) Casuarina ecology, management and utiliza-tion. CSIRO, Melbourne, pp 138–157

Yang T, Yan C, Li Y, Liang J, Tang H (2003) Na+ and Cl−

accumulation and salt resistance of Casuarina equisetifoliaseedlings under salt stress. Fujian J Agric Sci 18:155–159

Yuehua C, Yangian X (1990) Research on Casuarina plantations andnitrogen fixation in China. In: El-Lakany MH, Turnbull JW,Brewbaker JL (eds) Advances in Casuarina research and utiliza-tion. Desert Development Center, AUC, Cairo, Egypt, pp 165–173

Zhang Y, Chen Y, Li G, Chen Z, Zhang C (2006) Mycorrhizal fungalscreening and inoculant effectiveness for Casuarina junghhuhniana.Forest Res 19:392–396

Zhong C, Zhang Y, Chen Y, Jiang Q, Chen Z, Liang J, PinyopusarerkK, Franche C, Bogusz D (2010) Casuarina research andapplications in China. Symbiosis 50:107–114

Zimpfer J, Kaelke C, Smyth C, Dawson J (2001) The biotic communityincreases the infectivity of Frankia. Soil Ecol 21:67–78

Zimpfer J, Kaelke C, Smyth C, Hahn D, Dawson J (2003) Frankiainoculation, soil biota, and host tissue amendment influenceCasuarina nodulation capacity of tropical soil. Plant Soil 254:1–10

Folia Microbiol (2011) 56:1–9 9