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Casuarina in Africa: Distribution, role and importance of arbuscular mycorrhizal, ectomycorrhizal fungi and Frankia on plant development
Journal of Environmental Management 128 (2013) 204e209
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Journal of Environmental Management journal homepage: www.elsevier.com/locate/jenvman
Review
Casuarina in Africa: Distribution, role and importance of arbuscular mycorrhizal, ectomycorrhizal fungi and Frankia on plant development Nathalie Diagne a, Diegane Diouf a, b, Sergio Svistoonoff c, Aboubacry Kane a, b, Kandioura Noba a, Claudine Franche c, Didier Bogusz c, Robin Duponnois d, * a
Laboratoire Commun de Microbiologie IRD/ISRA/UCAD, Centre de Recherche de Bel Air, BP 1386 Dakar, Senegal Département de Biologie Végétale, Université Cheikh Anta Diop (UCAD), BP 5005 Dakar, Senegal Groupe Rhizogenèse, Unité Mixte de Recherche Diversité et Adaptation et Développement des Plantes (DIADE), Institut de Recherche pour le Développement (IRD), 911 avenue Agropolis, BP 5045, 34394 Montpellier, Cedex 5, France d Laboratoire des Symbioses Tropicales et Méditerranéennes (LSTM), TA10/J, IRD, UMR 113 CIRAD/INRA/IRD/SUP-AGRO/UM2, Campus International de Baillarguet, 34398 Montpellier, Cedex, France b c
a r t i c l e i n f o
a b s t r a c t
Article history: Received 21 March 2012 Received in revised form 18 April 2013 Accepted 1 May 2013 Available online 7 June 2013
Exotic trees were introduced in Africa to rehabilitate degraded ecosystems. Introduced species included several Australian species belonging to the Casuarinaceae family. Casuarinas trees grow very fast and are resistant to drought and high salinity. They are particularly well adapted to poor and disturbed soils thanks to their capacity to establish symbiotic associations with mycorrhizal fungi -both arbuscular and ectomycorrhizal- and with the nitrogen-fixing bacteria Frankia. These trees are now widely distributed in more than 20 African countries. Casuarina are mainly used in forestation programs to rehabilitate degraded or polluted sites, to stabilise sand dunes and to provide fuelwood and charcoal and thus contribute considerably to improving livelihoods and local economies. In this paper, we describe the geographical distribution of Casuarina in Africa, their economic and ecological value and the role of the symbiotic interactions between Casuarina, mycorrhizal fungi and Frankia. Ó 2013 Elsevier Ltd. All rights reserved.
Keywords: Casuarina Ecosystem degradation Mycorrhizal symbiosis Frankia Afforestation programmes
1. Introduction The population explosion and rapid urbanisation are major threats in Africa, as they increase the dependence of the population on natural ecosystem resources. Overexploited ecosystems are degraded mainly as a result of a reduction in soil fertility. The introduction of nitrogen fixing and highly mycotrophic plant species is a promising way to increase soil fertility. Among these species, exotic trees such as Casuarina are widespread in tropical and subtropical zones where they play an important role due to their symbiotic relationships with mycorrhizal fungi and Frankia bacteria. These microorganisms increase plant growth and development (Zhong et al., 2010; Yang and Paszkowski, 2011). They also improve nutrient availability e particularly P and N- for the plant host and in return, they benefit from plant carbohydrates (He and Critchley,
* Corresponding author. Present address: Laboratoire des Symbioses Tropicales et Méditerranéennes, UMR CIRAD/IRD/SupAgro/UM2/USC INRA, TA A-82/J, Campus International de Baillarguet, 34398 Montpellier Cedex 5, France. Tel.: þ33 (0)4 67 59 37 86; fax: þ33 (0)467 59 38 02. E-mail address: [email protected] (R. Duponnois). URL: http://www.mpl.ird.fr/lstm/ 0301-4797/$ e see front matter Ó 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.jenvman.2013.05.009
2008; Smith and Read, 2008). However, the success of inoculation depends on the type, viability, efficiency and infectivity of the inoculum (Rossi et al., 2007). Casuarinaceae species are actinorhizal plants which originated from Australia. The term casuarina comes from the Malay word ‘kasuari’ due to the resemblance of the twigs and the plumage of the cassowary bird (Boland et al., 1994). These trees are widely established around the world with the exception of Antarctica. The family comprises four genera (Allocasuarina, Casuarina, Ceuthostoma and Gymnostoma) and approximately 86 species and 13 subspecies (Steane et al., 2003; Bisby et al., 2007). Among them, Casuarina equisetifolia, Casuarina glauca and C. cunninghamia are the most frequently introduced species in most African countries with the exception of Zimbabwe where C. junghuhniama is more widely planted (NRC, 1984). However, C. equisetifolia is the most widespread and the best known species. Casuarina grow best in humid tropical and subtropical climates in areas where the average rainfall ranges from 200 mm to 5000 mm, at altitudes between 0 and 1800 m above the sea level. Casuarina species are among the fastestgrowing of all trees and, in their early growth stages, they can grow up to two to 3 m per year, and reach a final height of 20e30 m (NRC, 1984). The wood is dense, hard and smokeless. It produces high
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quality charcoal and burns with great heat even when green; it has low ash content. C. equisetifolia is one of the best types of firewood in the world (El-Lakany et al., 1990). The calorific value of its wood is up to 5000 kcal kg1 and that of its charcoal more than 7000 kcal kg1. Casuarina is used in the reclamation of salt-affected land, as windbreaks, for the stabilization of sand dunes, and for the production of firewood and timber. However, up to now, little is known about the exact Casuarina distribution in Africa: its potential benefits for the rehabilitation of degraded lands and the management of soil fertility. This review focuses on: 1) the distribution and ecology of Casuarina in Africa, 2) its uses and 3) the importance of the symbiotic relationships between Casuarina, arbuscular mycorrhizal (AMF), ectomycorrhizal (EMF) and/or Frankia bacteria in improving the role of Casuarina in soil rehabilitation. 2. Geographic distribution of Casuarina and its ecological importance in Africa 2.1. Geographic distribution of Casuarina in Africa Casuarina is widely distributed in Africa, where three of the four genera have been introduced: five species of Casuarina, three Allocasuarina spp. and one Gymnosoma sp. (Gtari and Dawson, 2011) have been introduced in Algeria, Benin, Burkina Faso, Cameroon, Central African Republic, Chad, Congo, Ivory Coast, Democratic Republic of Congo, Djibouti, Egypt, Eritrea, Ethiopia, Gabon, Gambia, Ghana, Guinea, Guinea-Bissau, Kenya, Liberia, Madagascar, Malawi, Mali, Mauritania, Niger, Nigeria, Senegal, Sierra Leone, Somalia, South Africa, Sudan, Tanzania, Togo, Uganda and Zimbabwe (Orwa et al., 2009; Gtari and Dawson, 2011) (Table 1). In some countries, including Senegal, Egypt, Benin, Kenya, South Africa, and Madagascar, Casuarina is widely planted, whereas in others its presence is very reduced and is limited to decoration. The selection of a particular species depends on several factors: the climatic conditions in the area concerned, proximity to the sea, wind, soil erosion and soil mineral deficiencies at the plantation sites (Sayed, 2011). 2.2. Importance of Casuarina plantations in Africa As pioneer species, Casuarina grows well in Africa in a range of climates and soils including disturbed, poor, coastal, and spoiled soils. In tropical and subtropical countries, it has been shown that Casuarina growth is stimulated by hot weather (Digiamberardino, 1986). Casuarina plantations have been established in the Niayes region in Senegal along the western coast between Dakar and StLouis, along the Mediterranean Coast of North Africa, in the Nile Delta and the Nile Valley in Egypt, in the Sémé zone in Benin between Cotonou and Porto Novo, and on the coastal dunes of KwaZulu-Natal in South Africa. In these countries, Casuarina plays a major role in sustaining ecosystem fertility. Table 1 Members of the Casuarinaceae family introduced in Africa. Species
Distribution in Africa
1. 2. 3. 4. 5. 6. 7. 8. 9.
North Africa, Tropical Africa North Africa, Tropical Africa North Africa, Tropical Africa Southern, Northern, Tropical Africa Southern, Northern Africa, Madagascar Southern, Northern, Tropical Africa Northern, Tropical Africa Tropical Africa Tropical Africa
Allocasuarina littoralis Allocasuarina torulosa Allocasuarina verticillata Casuarina cunninghamiana Casuarina equisetifolia Casuarina glauca (swamp oak) Casuarina junghuhniana Casuarina obesa (swamp she-oak) Gymnostoma deplancheanum
Source: Gtari and Dawson (2011).
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In the Niayes region in Senegal, the species is C equisetifolia. There, it stabilizes the coastal sand dunes and acts as a windbreak. This plantation produces large quantities of litter which is used as biofertilizer by local farmers. Leaf litter has been estimated at 3.3 t ha1 year1 in plantations between 6 and 34 years old (Mailly and Margolis, 1992). Extensively used in compost, the litter reduces the use of chemical products and improves soil fertility. The addition of composted litter to sand soils improves plant growth and yield (Soumaré et al., 2004). Similar positive effects were obtained by adding ramial chipped wood. The positive role of C. equisetifolia in soil fertility was demonstrated by Diallo et al. (2005); who found a high mineral N content in C. equisetifolia amended soil and net soil mineralization primarily influenced by C. equisetifolia. In Senegal, Casuarina is not widely used for wood production but dead branches are collected by the local populations for domestic uses such as firewood (Cisse and Gourbiere, 1993). C. equisetifolia is planted along streets and beaches as an ornamental tree. In other countries like Egypt, Casuarina is planted to protect desert highways thanks to its ability to grow well under harsh environmental conditions. In Egypt, Casuarina is mostly used for its significant ecological roles such as crop protection, shelterbelt, irrigation stabilisation, drainage canal banks, land reclamation and protection of buildings. In the Nile Delta and in the Nile Valley, Casuarina trees were planted to provide shade, to limit border effects, and as a windbreak. Biomass productivity of 12-year-old irrigated plantations has been estimated at 496 t ha1 of which the wood volume was 294 m3 ha1 (Megahed and El-Lakany, 1986). Used as a shelterbelt in intercropping systems in Egypt, C. glauca increased the yield of the sheltered crops (El-Sayed et al., 1983). In Egypt, this species plays an important economic role in the production of fuel timber, charcoal, wood for industry and for the manufacture of particle board. C. equisetifolia plantations also play an important role in Benin, where their wood is used by local people for fuelwood and timber. A ten-year-old C. equisetifolia plantation near the sea produced around 200 stacked cubic metres per ha1 (Buffe, 1961). In Kenya, Casuarina is mainly grown for poles and as an ornamental plant and is much less used for firewood, charcoal and as a windbreak. The major use of Casuarina is for the construction of local tourist hotels, villas and homes (Mbuvi et al., 2011). Casuarina was also used for the rehabilitation of the Bamburi cement factory in Mombasa (Siachoono, 2010). In Southern Africa, Casuarina has been used to reclaim former mining land and to stabilise the coastal dunes of KwaZulu-Natal. Two thirds of the area was replanted with C. equisetifolia for the development of a local charcoal industry (Van Aarde et al., 1996). In Madagascar C. equisetifolia was planted in Ivoloina region for the production of improved seeds to be used in forestation programmes. Casuarina cunninghamiana was planted in Mahelia for the same purpose (Chaix and Ramamonjisao, 2001). The above data confirm the ecological role of Casuarina in Africa, but several studies have shown that the growth and performance of Casuarina can be enhanced when it is associated with symbiotic microorganisms (Shah et al., 2006; He and Critchley, 2008). To ensure the sustainability of Casuarina plantation and to improve yield, we need to understand the relationship between the tree, mycorrhizal fungi (AMF, EMF) and nitrogen fixing Frankia bacteria. 3. Symbiotic relationship between Casuarina, AMF, EMF and/ or Frankia bacteria The efficiency of mycorrhizal and Frankia infection depends on the habitat of the host, the prevailing environmental conditions, and the associated plant species. Ectomycorrhizal, endomycorrhizal and Frankia symbionts can occur in the same plant root (Wang and Qiu, 2006).
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3.1. Casuarina/arbuscular mycorrhizal symbiosis AMF obligate symbionts can be cultivated in vivo or in vitro (Diop, 2004). AMF can be isolated in the field or trapped in soils using different methods as described by (Utobo et al., 2011), or used to transform hairy roots of carrot (Daucus Carota L.) (Declerck et al., 1998). After isolation, propagules such as spores, mycorrhizal roots, and hyphae are generally used for inoculation (Smith and Read, 2008; Eskandari and Danesh, 2010). Inoculation with AMF enhances plant growth by increasing nutrient availability via its network of hyphae which is extensively involved in nutrient uptake (Smith and Read, 2008). AMF significantly improves the ability of plants to acquire soil P (Smith et al., 2011) and in return, they benefit from plant carbohydrates (Kiers et al., 2011). Inoculation with AMF increases plant height, biomass and P content compared to non-inoculated plants (Elumalai and Raaman, 2009; Zhong et al., 2010). Among 13 symbiotic fungi, Glomus mosseae, Glomus fasciculatum, G. versiforme and Acaulospora laevis are considered to be the most efficient AMF to facilitate C. equisetifiolia development (Vasanthakrishna and Bagyaraj, 1993; Vasanthakrishna et al., 1995). Furthermore, mycorrhizal symbiosis confers resistance to abiotic stresses in Casuarina species (Zhong et al., 2010). Several studies have shown that arbuscular mycorrhizae are found in Casuarina species growing in dry conditions and that they play an important role by improving plant tolerance to drought (Zhang et al., 2010). This mechanism is based on a range of biochemical and physiological responses such as a lower permeability of plasma membrane induced by the AMF, and high soluble sugar and P content in the aerial parts of the plant. AMF also confer resistance to flooding (Rutto et al., 2002). C. equisetifolia mycorrhized seedlings were shown to be better adapted to flooding conditions than noninoculated seedlings (Osundina, 1997). It has also been shown that AMF protect the host plant against pathogens (Liu et al., 2007; Sayeed and Siddiqui, 2008). Other studies carried out by Evelin et al. (2009) showed that AMF improve plant tolerance to salt stress. However, the capabilities of AMF to protect plants from salt stress depend on the behaviour of each AMF species. In association with C. equisetifolia, AMF can be used to rehabilitate polluted soils such as those contaminated by heavy metals (e.g. former mines); they enhance plant growth on severely disturbed sites (Karimi et al., 2011). However, AMF colonisation may be reduced in disturbed conditions and a moderate AMF colonization level was obtained in a naturally revegetated former coal mine with C. equisetifolia (Kumar et al., 2003). Nevertheless, AMF are very important in disturbed conditions because they improve soil health (Gianinazzi et al., 2010). 3.2. Casuarina/ectomycorrhizal symbiosis In addition to symbiosis with AMF, Casuarina species are associated with EMF (Wang and Qiu, 2006). Ectomycorrhizal strains are isolated from fruiting bodies, and pure cultures are maintained in the laboratory as described by Rossi et al. (2007) and Diagne et al. (2013). Different types of EMF inocula such as soil containing propagules, fungal spores from fruiting bodies and vegetative mycelia are used to inoculate plants in the field or in the nursery (Rossi et al., 2007). Inoculation with selected specific and compatible EMF increases C. equisetifolia seedling growth and biomass, and improves plant nutrient contents such as N and P (Elumalai and Raaman, 2009; Zhong et al., 2010). However, a specific relationship between the fungal partner and the host plant is often observed. Theodorou and Reddell (1991) observed that Amanita sp. formed ectomycorrhizae on Allocasuarina littoralis and C. cunninghamiana but not on C. equisetifolia. Similar results
concerning host specificity were obtained by Dell et al. (1994). In glasshouse experiments, Duponnois et al. (2003) found that some ectomycorrhizal fungi were unable to colonize Casuarina while effective colonization was obtained with Allocasuarina using the same fungal strains. These authors concluded that Allocasuarina verticillata was ectomycorrhizal dependent, whereas C. glauca was endomycorrhizal dependent. Similar results were obtained by Thoen et al. (1990), who showed that the ability to form ectomycorrhizae is more common with the genus Allocasuarina than with the genus Casuarina. Sometimes the relationship between Casuarina and ECM fungi can fail and for instance, infection with Scleroderma can lead to seedling death (Dell et al., 1994). Ectomycorrhizal strains of Pisolithus and Scleroderma isolates formed a mantle and a Hartig net on A. verticillata but failed to form a Hartig net on C. glauca. Furthermore, it has been demonstrated that the intensity of ectomycorrhizal infection with Pisolithus tinctorius and Lacaria laccata is higher with C. equisetifolia than with C. cunninghamiana (Theodorou and Reddel, 1991). Taken together, these results indicate specificity between the plant and EMF. Like AMF, EMF improves plant resistance to different types of stress (Smith and Read, 2008). The beneficial effect of EMF on plant resistance to disease has been demonstrated in exotic species including Acacia holosericea (Duponnois et al., 2000). These symbiotic microorganisms increase plant resistance to pathogens by creating a physical barrier which prevents the pathogen from entering the plant root. It has also been demonstrated that the EMF strain Pisolithus tinctorius increased Casuarina tolerance to salt (Zhong et al., 2010). Taken together, these results highlight the importance of inoculating Casuarina with a specific EMF.
3.3. Tripartite Casuarina/ectomycorrhizal/arbuscular mycorrhizal symbiosis Plants of the Casuarina family can enter a relationship with EMF and/or AMF mycorrhizal fungi (Table 2) (Wang and Qiu, 2006). A total of 50% Casuarinaceae plants are associated with EMF, around 25% with AMF and 25% of Casuarinaceae species form symbioses with both (Wang and Qiu, 2006). During mycorrhizal establishment, colonisation with EMF and AMF do not occur simultaneously. AMF is established first followed by EMF. However, in the rare cases when EMF is established first, it could reduce AMF colonisation by forming a mantle which acts as a barrier to AMF infection. However, when AMF is established first, it has no negative effects on EMF infection (Chilvers et al., 1987). Dual inoculation with EMF and AMF improved plant growth (Misbahuzzaman and Newton, 2006; Ramanankierana et al., 2007). For C. equisetifolia plants, inoculation with both AMF and EMF significantly increased biomass and P content compared to plants inoculated with either AMF or EMF alone (Elumalai and Raaman, 2009). These results show the beneficial effects of AMF and EMF on plant performance and the positive effect of mycorrhizal symbiosis is very important for the sustainability and management of agricultural ecosystems (Gianinazzi et al., 2010). However, an antagonistic effect was observed when both symbionts were inoculated and was generally the result of high ectomycorrhizal colonization (Duponnois et al., 2003). Chen et al. (2000) showed that the EMF Laccaria strain was able to reduce AMF colonization. To avoid antagonistic effects, inoculation with compatible AMF and EMF is thus recommended. Casuarina is a pioneer species that is well adapted to environmental stresses. Some Casuarinas plants such as C. equisetifolia are known to be bio-accumulators (Ukpebor et al., 2010).
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Table 2 AMF and EMF able to form mycorrhiza in Casuarinas plants. AMF fungal species
Host plant species
ECM fungal species
Host plants species
Acaulospora laevis Gerdemann and Trappe Glomus albidum Walker and Rhodes
C. equisetioflia Casuarina sp.
Aminata sp. Elaphomyces sp
G. claroideum Schenck and Smith
Casuarina sp.
Hysterangium sp.
G. clarum Nicolson and Schenck
Casuarina sp.
Laccaria laccate (Scop ex Fr.) Bk. and Br
G. fascicultum (Thaxter Sensu Gerdemann) Gerdemann and Trappe G.geosporum (Nicolson and Gerdemann) Walker G.intraradices Schenck and Smith
C. equisetifolia
Paxillus involutus (Batch ex Fr.) Fr
C. cunninghamiana C. equisetifolia ssp. equisetifolia. L C. cunninghamiana Miq. Elaphomyces sp. C. equisetifolia ssp. equisetifolia. L C. cunninghamiana Miq. Elaphomyces sp. C. equisetifolia ssp. equisetifolia. L C. cunninghamiana Miq. Elaphomyces sp. Casuarina sp.
Casuarina sp. C. glauca
P. albus IR100 Bougher and Smith Pisolithis tinctorius (Pers.) Coker and Couch
Casuarina sp.
Rhizopogon luteolus Fr. and Nord
Allocasuarina verticillata C. equisetifolia ssp. equisetifolia. L C. cunninghamiana Miq. Elaphomyces sp. Casuarina sp.
G.mossae (Nicolson and Gerdemann) Gerdemann and Trappe G. rubiforme (Gerdemann and Trappe) Almeida and Schenck G. versiforme (Karsten) Berch Gigaspora margarita (Gerdemann and Trappe)
Casuarina sp.
Suillus granulatus (L. ex Fr.) Kuntze
Casuarina sp.
C. equisetifolia Casuarina sp.
S. piperatus (Bull ex Fr.) O. Kuntze Scleroderma sp.
Casuarina sp. C. equisetifolia ssp. equisetifolia. L C. cunninghamiana Miq. Elaphomyces sp.
Scutellospora sp. Gerdemann and Trappe Scutellospora sp. Gerdemann and Trappe Gigaspora margarita Becker and Hall
Casuarina sp. Casuarina sp. Casuarina. sp.
Sources: Theodorou and Reddell (1991); Vasanthakrishna et al. (1995), Duponnois et al. (2003); He and Critchley, (2008).
Inoculation with mycorrhizal fungi was shown to increase Casuarina resistance to different stresses (Smith and Read, 2008). Since Casuarina is more commonly associated with AMF, few studies are available on the association of Casuarina with EMF and AMF. 3.4. Casuarina/Frankia symbiosis Frankia is a genus of nitrogen fixing Gramþ filamentous bacteria that lives in symbiosis with actinorhizal plants including Casuarina spp. The symbiotic microorganism Frankia is the only member of the family Frankiaceae in the order Actinomycetales (Normand et al., 1996). Frankia has only been cultured since 1978, when the first successful isolation was carried out from root nodules of Comptonia peregrina (Callaham et al., 1978). The development of genetic tools for Frankia has been hampered by the lack of a reliable gene transfer system (Benson et al., 2011). To overcome this problem, the genomes of four Frankia strains were recently sequenced (Normand et al., 2007; Persson et al., 2011). Frankia strains are isolated from lobe nodule as described by (Zhang et al., 2012). Inoculation of these bacteria can be carried out in different forms; pure culture, Frankia entrapped in alginate beads, as a crushed nodule suspension, or using the soil from around nodulated plants (Mansour et al., 1990). After inoculation, different factors such as soil temperature, pH, type of soil, can affect the establishment of the Casuarina-Frankia symbiosis (Mansour, 2003). In the field, thanks to their symbiotic association with Frankia, actinorhizal trees such as Casuarina can grow on nitrogen deficient soils. The amount of nitrogen fixed by actinorhizal trees is comparable to the amounts fixed by legumes and their Rhizobium symbionts and these trees can contribute significantly to the Neconomy of ecosystems (Diem and Dommergues, 1990). In different environments, Frankia can increase the development of actinorhizal plants. However, response to Frankia inoculation may depend upon environmental conditions (Sayed, 2011). Numerous studies have demonstrated the positive effect of Frankia on the development of Casuarina (e.g. Elumaila and Raaman, 2009). Inoculation with efficient and effective Frankia strains increases growth, biomass, N and P content and Casuarina survival (Tellal et al., 2008; Valdez, 2008; Zhang et al., 2012). A Frankia inoculation experiment on C. cunninghamiana carried out in the hot dry river valley in Yuanmou, Yunnan Province, increased
the survival of inoculated seedlings by 10%e20.6% compared with uninoculated seedlings after transfer to the field (Zhong et al., 2010). The height of the trees after two years differed significantly among Frankia treatments. However, not all Frankia strains improved tree growth (Zhong et al., 2010). It is important to distinguish between the specificity related to the nodulation process and the specificity which concerns the nitrogen-fixing potential of the system. Reddell and Bowen (1985) observed a range of responses from ineffectiveness in nitrogen fixation to high effectiveness between Casuarina species-Frankia source combinations. To determine which strain of Frankia is the best symbiont for specific casuarina species inoculation experiments with both microorganisms are needed. Inoculation has been shown to improve Casuarina performance and establishment during reforestation programmes by enhancing nitrogen fixation and improving tolerance to abiotic and biotic stresses such as drought, salinity, polluted sites etc. (Tani and Sasakawa, 2003; Bargali, 2011). Inoculation with Frankia may mitigate the negative effect of root rot in C. equisetifolia caused by Rhizoctonia sp. (Huang et al., 2011). Accordingly, the outstanding ability of actinorhizal plants to survive in harsh conditions such as former mines or nitrogen deficient soils (Barrit and Facelli, 2001; Dutta and Agrawal, 2002) is largely due to their ability to form a relationship with Frankia. 3.5. Tetrapartite symbiosis: Casuarina/arbuscular mycorrhizal/ ectomycorrhizal/Frankia Casuarina forms a relationship with Frankia, AMF and EMF. Inoculation with Frankia increase N2 fixation by 15e80%, ectomycorrhizal colonization by 10e70% and endomycorrhizal colonization by 10e50% with EMF (He and Crichley, 2008). Several authors have reviewed the relationship between the mycorrhizal and actinorhizal symbioses in non-legumes. As expected, the presence of mycorrhizae and Frankia on the same roots stimulated the development and the nitrogen-fixing activity of the actinorhizal symbiosis by improving the mineral nutrition of the host plant, particularly phosphorus uptake (Gentili and Huss-Danell, 2003). Dual inoculation with AMF and Frankia enhanced Casuarina growth more than single inoculation (Vasanthakrishna et al., 1994).
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However these authors observed that the effect of G. fasciculatum was greater than that of Frankia. Inoculation of C. equisetifolia with both Frankia and G. mosseae increased total dry weight by more than 80% compared to plants inoculated with Frankia alone (Gauthier et al., 1983). Similar positive effects on plant development were obtained in other actinorhizal species (Oliveira et al., 2005; Orfanoudakis et al., 2010). In addition, Muthukumar and Udaiyan (2010) reported that seedlings inoculated with Frankia and G. geosporum had more -and heavier- nodules compared to seedlings inoculated with Frankia alone. These authors showed that inoculation with Frankia improved AMF colonisation which is involved in plant nutrient uptake. They also reported that by improving nutrient acquisition, the tetra-partite association (Frankia, G. geosporum, Paenibacillus polymyxa and C. equisetifolia) enhanced the growth and the seedling quality of C. equisetifolia under tropical nursery conditions. Inoculation with either AMF or EMF, with AMF and EMF, or with AMF, EMF and Frankia all improved Casuarina growth. Elumalai and Raaman (2009) demonstrated that triple inoculation with EMF, AMF and Frankia significantly increased fungal colonization and infection and also increased shoot and root length in C. equisetifolia. Similar results were obtained by Rajendran and Devaraj (2004) who found more nutrients including N, P, Ca, K and Mg released by litter from plants inoculated with AM and Frankia together. Inoculation with EMF or AMF increased plant nutrients and it was also demonstrated that through the common mycorrhizal network (CMN) formed by EMF or EMF mycorrhizal fungi; N was transferred from plant to another (He et al., 2009). The beneficial role of AMF and Frankia symbiosis was documented in two recent reviews: He and Crichley (2008), and Sayed (2011). Previously, Gardner (1986) reported that nodulation could be inhibited in C. equisetifolia colonised with AMF. This inhibition might be the result of competition between the microsymbionts for infection sites and/or nutrients. The same author suggests that competition for root infection between microsymbionts could be avoided by applying the inoculum at different times. Inoculation with Frankia alone increased plant height and wood production. It has been demonstrated that mycorrhiza fungi promote the success of Frankia symbiosis in Casuarina species by increasing N2 fixation, and the uptake of nutrients such as phosphorus (He and Critchley, 2008). Triple inoculation with EMF, AMF and Frankia was shown to significantly increase fungal colonisation and infection as well as shoot and root length in C. equisetifolia (Elumalai and Raaman, 2009). The same authors showed that these microorganisms also increased plant nutrient content including N and Pi in C. equisetifolia. As already mentioned in this paper, inoculation with microsymbionts such as AMF, EMF, and Frankia may be a biological tool to improve Casuarina performance in forestation programmes. 4. Conclusion Due to their tolerance to adverse soil and climate conditions Casuarina trees are biological tool for rehabilitation of degraded lands. The ability of Casuarina to survive in such harsh conditions is largely due to the symbiotic relationship with AMF, EMF, and Frankia. However, care should be taken to choose the best combination of Casuarina and the symbiotic microorganisms (Mansour, 2003; Sayed et al., 2007, Sayed, 2011) to be used in reforestation programmes. Strategies for plant improvement should include the selection of Casuarina species and varieties, and also the selection of the appropriate Frankia, AMF and EMF strains adapted to specific conditions such as drought, salinity, heavy metal pollution, flooding etc. Furthermore, the Casuarina plant should be associated with an effective and efficient symbiotic which will increase the efficiency of nitrogen fixation and P uptake for plant growth.
Casuarina, AMF, EMF, Frankia symbioses should be managed in a way to enhance Casuarina resistance to diseases and pests and improve performance under saline, waterlogged, drought and coastal conditions. References Bargali, K., 2011. Actinorhizal plants of Kumaun Himalaya and their ecological significance. Afr. J. Plant Sci. 5, 401e406. Benson, D.R., Brooks, J.M., Huang, Y., Bickhart, D.M., Mastronunzio, J.E., 2011. The biology of Frankia sp. strains in the post-genome era. Mol. Plant Microbe. Interact 24, 1310e1316. Bisby, F.A., Roskov, Y.R., Ruggiero, M.A., Orrell, T.M., Paglinawan, L.E., Brewer, P.W., Bailly, N., van Hertum, J. (Eds.), 2007. Species 2000 and ITIS Catalogue of Life: 2007 Annual Checklist. Reading, UK. Digital resource at. www.catalogueoflife. org/annual-checklist/2007/Species 2000. Boland, D.J., Brooker, M.I.H., Chippendale, G.M., Hall, N., Hyland, B.P.M., Johnston, R.D., Kleinig, D.A., Turner, J.D., 1994. Forest Trees of Australia. CSIRO, Melbourne, Australia. Barritt, A.R., Facelli, J.H.M., 2001. Effects of Casuarina pauper litter and grove soil on emergence and growth of understorey species in arid lands of South Australia. J Arid Environ 49, 569e579. Buffe, J., 1961. Les plantations de Casuarina equisetifolia (filao) dans le SudDahomey e Direction des Eaux et Forêts/CTFT: Expériences et travaux de reboisement forestier et de restauration des sols. Nogent-sur-Marne, France. Callaham, D., Del Tredici, P., Torrey, J.G., 1978. Isolation and cultivation in vitro of the actinomycetes causing root nodulation in Comptonia. Science 199, 899e902. Chaix, G., Ramamonjisao, L., 2001. Seeds production for Madagascar afforestation. Bois et Forêts des Tropiques 269, 46e63. Chen, Y.L., Brundrett, M.C., Dell, B., 2000. Effects of ectomycorrhizal and vesiculararbuscular mycorrhizas, alone and in competition, on root colonization and growth of Eucalyptus globulus and E. urophylla. New Phytol. 146, 545e556. Chilvers, G.A., Lapeyrie, F.F., Horan, D.P., 1987. Ectomycorrhizal vs endomycorrhizal fungi within the same roots system. New Phytol. 107, 441e448. Cisse, M., Gourbière, F., 1993. Décomposition de la litière de Filao (Casuarina equisetifolia forst) au Sénégal. Activité de la microfaune détritivore. ORSTOM, Dakar, 71p. multigr. Declerck, S., Strullu, D.G., Plenchette, C., 1998. Monoxenic culture of the intraradical forms of Glomus sp. isolated from a tropical ecosystem: a proposed methodology for germplasm collection. Mycologia 90, 579e585. Dell, B., Malajczuk, N., Bougher, N.L., Thomson, G., 1994. Development and function of Pisolithus and Scleroderma ectomycorrhizas formed in vivo with AlloCasuarina, Casuarina and Eucalyptus. Mycorrhiza 5, 129e138. Diagne, N., Thioulouse, J., Sanguin, H., Prin, Y., Krasova-Wade, T., Sylla, S., Galiana, A., Baudoin, E., Neyra, M., Svistoonoff, S., Lebrun, M., Duponnois, R., 2013. Ectomycorrhizal diversity enhances growth and nitrogen fixation of Acacia mangium seedlings. Soil Biol. Biochem. 57, 468e476. Diallo, M.D., Guisse, A., Badiane-Niane, A., Sall, S., Chotte, J.L., 2005. In situ effect of some tropical litters on N mineralization. Arid Land Res. Manag. 19, 173e181. Diem, H.G., Dommergues, Y.R., 1990. Current and potential uses and management of Casuarinaceae in the tropics and subtropics. In: Schwintzer, C.R., Tjepkema, J.D. (Eds.), The Biology of Frankia and Actinorhizal Plants. Academic Press, New York, pp. 317e342. Digiamberardino, T., 1986. Changes in a south east Florida Coastal Ecosystem after Elimination of Casuarina equisetifolia. Unpublished. Nova University. Diop, T.A., 2004. In vitro culture of arbuscular mycorrhizal fungi: advances and future prospects. Afr. J. Biotechnol. 2, 692e697. Duponnois, R., Founoune, H., Bâ, A.M., Plenchette, C., El jafaari, S., Nyera, M., Ducousso, M., 2000. Ectomycorrhization of Acacia holosericea A. Cunn. ex G. Don by Pisolithus spp. in Senegal: effect on plant growth and on the roots e knot nematode Meloidogyne javanica. Ann. Sc. For. 57, 345e350. Duponnois, R., Diedhiou, S., Chotte, J.L., Sy, M.O., 2003. Relative importance of the endomycorrhizal and/or ectomycorrhizal associations in AlloCasuarina and Casuarina genera. Can. J. Microbiol. 50, 691e696. Dutta, R.K., Agrawal, M., 2002. Effect of tree plantations on the soil characteristics and microbial activity of coal mine spoil land. Trop. Ecol. 43, 315e324. El-Lakany, M.H., Turnbull, J.W., Brewbaker, J.L., 1990. Advances in Casuarina Research and Utilization. DDC, AUC, Cairo, Egypt, 241p. El-Sayed, A.B., Omran, T.A., Khalil, A.E., 1983. Biomass characteristics of young Casuarina plantations in northwestern region of Egypt. Alex. J. Agric. Res. 31, 411e422. Elumalai, S., Raaman, N., 2009. In vitro synthesis of Frankia and mycorrhiza with Casuarina equisetifolia and ultrastructure of root system. Indian J. Exp. Biol. 47, 289e297. Eskandari, A., Danesh, Y.R., 2010. Study of life cycle of arbuscular mycorrhizal fungus Glomus intraradices using in vitro culturing technique. J. Phytol. 2, 69e75. Evelin, H., Kapoor, R., Giri, B., 2009. AMF in alleviation of salt stress: a review. Ann. Bot. 104, 1263e1280. Gardner, L.C., 1986. Mycorrhizae of actinorhizal plants. MIRCEN J. 2, 147e160. Gauthier, D., Diem, H.G., Dommergues, Y., 1983. Preliminary results of research on Frankia and Endomycorrhizae associated with Casuarina equisetifolia. In: Midgeley, S.J., Turnbull, J.W., Johnson, R.D. (Eds.), Casuarina Ecology, Management and Utilization. CSIRO, Melbourne, Australia, pp. 211e217.
N. Diagne et al. / Journal of Environmental Management 128 (2013) 204e209 Gentili, F., Huss-Danell, K., 2003. Local and systemic effects of phosphorus and nitrogen on nodulation and nodule function in Alnus incana. J. Exp. Bot. 54, 2757e2767. Gianinazzi, S., Gollotte, A., Binet, M.N., van Tuinen, D., Redecker, D., Wipf, D., 2010. Agroecology: the key role of arbuscular mycorrhizas in ecosystem services. Mycorrhiza 20, 519e530. Gtari, M., Dawson, J.O., 2011. An overview of actinorhizal plants in Africa. Funct. Plant Biol. 38, 653e661. He, X.H., Critchley, C., 2008. Frankia nodulation, mycorrhization and interactions between Frankia and mycorrhizal fungi in casuarina plants. In: Varma, Ajit (Ed.), Mycorrhiza e State of the Art, Genetics and Molecular Biology, Eco-function, Biotechnology, Eco-physiology, Structure and Systematics, third ed. Springere Verlap GmbH, Germany, pp. 767e781. He, X., Xu, M., Qiu, G.Y., Zhou, J., 2009. Use of 15N stable isotope to quantify nitrogen transfer between mycorrhizal plants. J. Plant Ecol. 2, 107e118. Huang, J., He, Hueyou, Cai, Shouping, Ke, Yuzhu, Chen, Duanqin, Tang, Chensheng, 2011. Current research on main casuarina diseases and insects in China. In: Zhong, C., Pinyopusarerk, K., Kalinganire, A., Franche, C. (Eds.), Improving Smallholder Livelihoods through Improved Casuarina Productivity. Proceedings of the 4th International Casuarina workshop. Haikou 22e25 March 2010, pp. 232e238. Karimi, A., Khodaverdiloo, H., Sepehri, M., Sadaghiani, M.R., 2011. AMF and heavy metal contaminated soils. Afr. J. Microbiol. Res. 5, 1571e1576. Kiers, E.T., Duhamel, M., Beesetty, Y., Mensah, J.A., Franken, O., Verbruggen, E., Fellbaum, C.R., Kowalchuk, G.A., Hart, M.M., Bago, A., Palmer, T.M., West, S.A., Vandenkoornhuyse, P., Jansa, J., Bücking, H., 2011. Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333, 888. http://dx.doi.org/ 10.1126/science.1208473. Kumar, A., Raghuwanshi, R., Upadhyay, R.S., 2003. Vesicular-arbuscular mycorrhizal association in naturally revegetated coal mine spoil. Trop. Ecol. 44, 253e256. Liu, J., Maldonado-Mendoza, I., Lopez-Meyer, M., Cheung, F., Town, C.D., Harrison, M.J., 2007. Arbuscular mycorrhizal symbiosis is accompanied by local and systemic alterations in gene expression and an increase in disease resistance in the shoots. Plant J. 50, 529e544. Mailly, D., Margolis, H.A., 1992. Forest floor and mineral soil development in Casuarina equisetifolia plantations on the coastal sand dunes of Senegal. For. Ecol. Manage. 55, 1e4. Mansour, S.R., 2003. Survival of Frankia strains under different soil conditions. J. Biol. Sci. 3, 618e626. Mansour, S.R., Dewedar, A., Torrey, J.G., 1990. Isolation, culture, and behaviour of Frankia strain HFPCgI4 from root nodules of Casuarina glauca. Bot. Gaz. 151, 490e496. Mbuvi, M.T.E., Muchiri, M.N., Wairungu, S.N., 2011. Modern silviculture practices versus livehood needs: the case of Casuarina growing along the Kenya Coastal Region. In: Improving Smallholder Livelihoods through Improved Casuarina Productivity. Proceedings of the 4th International Casuarina Workshop. Haikou 22e25 March 2010, pp. 232e238. Megahed, M.H., El-Lakany, M.H., 1986. Biomass characteristics of young Casuarina plantations in northwestern region of Egypt. Alex. J. Agric. Res. 31, 411e422. Muthukumar, T., Udaiyan, K., 2010. Growth response and nutrient utilization of Casuarina equisetifolia seedlings inoculated with bioinoculants under tropical nursery conditions. New Forests 40, 101e118. Misbahuzzaman, K., Newton, A., 2006. Effect of dual arbuscular-ectomycorrhizal inoculation on mycorrhiza formation and growth in E. camaldulensis Dehnh. Seedlings under different nutrient regime. Int. J. Agri Biol. 8, 848e854. National Research Council, 1984. Casuarinas: Nitrogen-fixing Trees for Adverse Sites. National Academy Press, Washington DC, USA. Normand, P., Orso, S., Cournoyer, B., Jeannin, P., Chapelon, C., Dawson, J., Evtushenko, L., Misra, A.K.,1996. Molecular phylogeny of the genus Frankia and related genera and emendation of family Frankiaceae. Int. J. Syst. Bacteriol. 46, 1e9. Normand, P., Lapierre, P., Tisa, L.S., Gogarten, J.P., Alloisio, N., Bagnarol, E., Bassi, C.A., Berry, A.M., Bickhart, D.M., Choisne, N., Couloux, A., Cournoyer, B., Cruveiller, S., Daubin, V., Demange, N., Francino, M.P., Goltsman, E., Huang, Y., Kopp, O.R., Labarre, L., Lapidus, A., Lavire, C., Marechal, J., Martinez, M., Mastronunzio, J.E., Mullin, B.C., Niemann, J., Pujic, P., Rawnsley, T., Rouy, Z., Schenowitz, C., Sellstedt, A., Tavares, F., Tomkins, J.P., Vallenet, D., Valverde, C., Wall, L.G., Wang, Y., Medigue, C., Benson, D.R., 2007. Genome characteristics of facultatively symbiotic Frankia sp. strains reflect host range and host plant biogeography. Genome Res. 17, 7e15. Oliveira, R.S., Castro, P.M.L., Dodd, J.C., Vosátka, M., 2005. Synergistic effect of Glomus intraradices and Frankia spp. on the growth and stress recovery of Alnus glutinosa in an alkaline anthropogenic sediment. Chemosphere 60, 1462e1470. Orfanoudakis, M., Wheeler, C.T., Hooker, J.E., 2010. Both the arbusculuar mycorrhizal fungus Gigaspora rosea and Frankia increase root system branching and reduce root hair frequency in Alnus glutinosa. Mycorrhiza 20, 117e126. Orwa, C., Mutua, A., Kindt, R., Jamnadass, R., Anthony, S., 2009. Agroforestry Database: a Tree Reference and Selection Guide Version 4.0. World Agroforestry Centre, Kenya. Osundina, M.A., 1997. Nodulation and growth of mycorrhizal Casurarina equisetifolia J.R and G. First in response to flooding. Bio. Fertil. Soils 26, 95e99. Persson, T., Benson, D.R., Normand, P., Vanden Heuvel, B., Pujic, P., Chertkov, O., Teshima, H., Bruce, D.C., Detter, C., Tapia, R., Han, S., Han, J., Woyke, T., Pitluch, P., Pennacchio, L., Nolan, M., Ivanova, N., Pati, A., Land, M.L., Pawlowski, K.,
209
Berry, A.M., 2011. Genome sequence of Candidatus Frankia datiscae Dg1, the uncultured microsymbiont from nitrogen-fixing root nodules of the dicot Datisca glomerata. J. Bacteriol. 193, 7017e7018. Rajendran, K., Devaraj, P., 2004. Biomass and nutrient distribution and their return of Casuarina equisetifolia inoculated with biofertilizers in farmland. Biomass Bioenerg. 26, 235e249. Ramanankierana, N., Ducousso, M., Rakotoarimanga, N., Prin, Y., Thioulouse, J., Randrianjohany, E., Ramaroson, L., Kisa, M., Galiana, A., Duponnois, R., 2007. Arbuscular and ectomycorrhizal of Uapaca bojeri L. (Euphorbiaceae): sporophore diversity, and soil microbial of root colonization, and effects on seedling growth and soil microbial catabolic diversity. Mycorrhiza 17, 195e208. Reddell, P., Bowen, G.D., 1985. Frankia source affects growth, nodulation and nitrogen fixation in Casuarina species. New Phytol. 100, 115e122. Rossi, J.M., Agenor Jr., F., Vetúria, L., Oliveira, V.L., 2007. Inoculant production of ectomycorrhizal fungi by solid and submerged fermentations. Food Technol. Biotechnol 45, 277e286. Rutto, K.L., Mizutani, F., Kadoya, K., 2002. Effect of root-zone flooding on mycorrhizal and non-mycorrhizal peach (Prunus persica Batsch) seedlings. Sci. Hort. 94, 285e295. Sayed, W.F., 2011. Improving Casuarina growth and symbiosis with Frankia under different soil environmental conditions-review. Folia Microbiol. 56, 1e9. Sayed, W.F., Zahran, H.H., Salem, W.M., 2007. Dominant rhizospheric microorganisms under some casuarinas and its effect on Frankia growth and nodulation capacity. Egypt. J. Biotechnol. 2, 201e218. Sayeed, M., Siddiqui, Z.A., 2008. AMF as potential bioprotectants against plant pathogens. Mycorrhizae: Sustain. Agric. For., 61e97. Shah, S.K., Shah, R.P., Xu, H.L., Aryal, U.K., 2006. Biofertilizers: an alternative source of nutrients for sustainable production of tree crops. J. Sustain. Agr 29, 85e95. Siachoono, S.M., 2010. Land reclamation efforts in Haller Park, Mombasa. Int. J. Biodiversity Conservation 2, 019e025. Smith, S.E., Read, D.J., 2008. Mycorrhizal Symbiosis, third ed. Academic Press. Smith, S.E., Jakobsen, I., Groenlund, M., Smith, F.A., 2011. Roles of arbuscular mycorrhizas in plant phosphorus nutrition: interactions between pathways of phosphorus uptake in arbuscular mycorrhizal roots have important implications for understanding and manipulating plant phosphorus acquisition. Plant Physiol. 156, 1050e1057. Soumaré, M.D., Mnkeni, P.N.S., Khouma, M., 2004. Effects of ramial chipped wood and litter compost of Casuarina equisetifolia Tomato growth and soil properties in Niayes, Senegal. In: Bationo, A. (Ed.), Managing Nutrient Cycles to Sustain Soil Fertility in Sub-saharan Africa. Triscope Consulting Publishers, p. 502p. Steane, D.A., Wilson, K.L., Hill, R.S., 2003. Using matK sequence data to unravel the phylogeny of Casuarinaceae. Mol. Phylogenet. Evol. 28, 47e59. Tani, C., Sasakawa, H., 2003. Salt tolerance of Casuarina equisetifolia and Frankia Ceql strain isolated from the root nodules of C. equisetifolia. Soil. Sci. Plant. Nutr 49, 215e222. Tellal, M., Qarro, M., Arahou, M., Abourouh, M., Tellal, R., Rhazi, L., Douira, A., 2008. Effet de l’actinomycète Frankia sur la croissance et la fixation de l’azote de Casuarina glauca et Casuarina cunninghamiana. Sécheresse 19, 211e216. Theodorou, C., Reddell, P., 1991. In vitro synthesis of ectomycorrhizas on Casuarinaceae with range of mycorrhizal fungi. New Phytol. 118, 279e288. Thoen, D., Sougoufara, B., Dommergues, Y., 1990. In vitro mycorrhization of Casuarina and AlloCasuarina species by Pisolithus isolates. Can. J. Bot. 68, 2537e2542. Ukpebor, E.E., Ukpebor, J.E., Aigbokhan, E., Goji, I., Onojeghuo, A.O., Okonkwo, A.C., 2010. Delonix regia and Casuarina equisetifolia as passive biomonitors and a bioaccumulators of atmospheric trace metals. J. Environ. Sci. 22, 1073e1079. Utobo, E.B., Ogbodo, E.N., Nwogbaga, A.C., 2011. Techniques for extraction and quantification of arbuscular mycorrhizal fungi. L. A. R. C. J. I 2, 68e78. Valdez, M., 2008. Frankia ecology. In: Pawlowski, K., Newton, W.E. (Eds.), Nitrogen Fixing Actinorhizal Symbioses. Springer, Berlin, Germany, pp. 4e72. Van Aarde, R.I., Coe, M., Niering, W.A., 1996. On the rehabilitation of the coastal dunes of KwaZulu-Natal. S. Afr. J. Sci. 92, 122e124. Vasanthakrishna, M., Bagyaraj, D.J., 1993. Selection of efficient VA mycorrhizal fungi for inoculating Casuarina equisetifolia. Arid. Soil Res. Rehabil. 7, 377e380. Vasanthakrishna, M., Bagyaraj, J.D., Nirmalnath, P.J., 1994. Responses of Casuarina equisetifolia to inoculation with Glomus fasciculatum and/or Frankia. For. Ecol. Manag. 68, 399e402. Vasanthakrishna, M., Bagyaraj, J.D., Nirmalnath, P.J., 1995. Selection of efficient VA mycorrhizal fungi for Casuarina equisetifolia e second screening. New For. 9, 157e162. Wang, B., Qiu, Y.L., 2006. Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16, 299e363. Yang, S.Y., Paszkowski, U., 2011. Phosphate import at the Arbuscule: just a nutrient? Mol. Plant Microbe. Interact. 24, 1296e1299. Zhang, Y., Zhong, C.L., Chen, Y., Chen, Z., Jiang, Q.B., Wu, C., Pinyopusarerk, K., 2010. Improving drought tolerance of Casuarina equisetifolia seedlings by arbuscular mycorrhizas under glasshouse conditions. New For.. http://dx.doi.org/10.1007/ s11056-010-9198-8. Zhang, X., Shen, A., Wang, Q., Chen, Y., 2012. Identification and nitrogen fixation effects of symbiotic Frankia isolated from Casuarina spp. in Zhejiang, China. Afr. J. Biotechnol. 11 (17), 4022e4029. Zhong, C., Zhang, Y., Chen, Y., Jiang, Q., Chen, Z., Liang, J., Pinyopusarerk, K., Franche, C., Bogusz, D., 2010. Casuarina research and applications in China. Symbiosis 50, 107e114.
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Review
Casuarina in Africa: Distribution, role and importance of arbuscular mycorrhizal, ectomycorrhizal fungi and Frankia on plant development Nathalie Diagne a, Diegane Diouf a, b, Sergio Svistoonoff c, Aboubacry Kane a, b, Kandioura Noba a, Claudine Franche c, Didier Bogusz c, Robin Duponnois d, * a
Laboratoire Commun de Microbiologie IRD/ISRA/UCAD, Centre de Recherche de Bel Air, BP 1386 Dakar, Senegal Département de Biologie Végétale, Université Cheikh Anta Diop (UCAD), BP 5005 Dakar, Senegal Groupe Rhizogenèse, Unité Mixte de Recherche Diversité et Adaptation et Développement des Plantes (DIADE), Institut de Recherche pour le Développement (IRD), 911 avenue Agropolis, BP 5045, 34394 Montpellier, Cedex 5, France d Laboratoire des Symbioses Tropicales et Méditerranéennes (LSTM), TA10/J, IRD, UMR 113 CIRAD/INRA/IRD/SUP-AGRO/UM2, Campus International de Baillarguet, 34398 Montpellier, Cedex, France b c
a r t i c l e i n f o
a b s t r a c t
Article history: Received 21 March 2012 Received in revised form 18 April 2013 Accepted 1 May 2013 Available online 7 June 2013
Exotic trees were introduced in Africa to rehabilitate degraded ecosystems. Introduced species included several Australian species belonging to the Casuarinaceae family. Casuarinas trees grow very fast and are resistant to drought and high salinity. They are particularly well adapted to poor and disturbed soils thanks to their capacity to establish symbiotic associations with mycorrhizal fungi -both arbuscular and ectomycorrhizal- and with the nitrogen-fixing bacteria Frankia. These trees are now widely distributed in more than 20 African countries. Casuarina are mainly used in forestation programs to rehabilitate degraded or polluted sites, to stabilise sand dunes and to provide fuelwood and charcoal and thus contribute considerably to improving livelihoods and local economies. In this paper, we describe the geographical distribution of Casuarina in Africa, their economic and ecological value and the role of the symbiotic interactions between Casuarina, mycorrhizal fungi and Frankia. Ó 2013 Elsevier Ltd. All rights reserved.
Keywords: Casuarina Ecosystem degradation Mycorrhizal symbiosis Frankia Afforestation programmes
1. Introduction The population explosion and rapid urbanisation are major threats in Africa, as they increase the dependence of the population on natural ecosystem resources. Overexploited ecosystems are degraded mainly as a result of a reduction in soil fertility. The introduction of nitrogen fixing and highly mycotrophic plant species is a promising way to increase soil fertility. Among these species, exotic trees such as Casuarina are widespread in tropical and subtropical zones where they play an important role due to their symbiotic relationships with mycorrhizal fungi and Frankia bacteria. These microorganisms increase plant growth and development (Zhong et al., 2010; Yang and Paszkowski, 2011). They also improve nutrient availability e particularly P and N- for the plant host and in return, they benefit from plant carbohydrates (He and Critchley,
* Corresponding author. Present address: Laboratoire des Symbioses Tropicales et Méditerranéennes, UMR CIRAD/IRD/SupAgro/UM2/USC INRA, TA A-82/J, Campus International de Baillarguet, 34398 Montpellier Cedex 5, France. Tel.: þ33 (0)4 67 59 37 86; fax: þ33 (0)467 59 38 02. E-mail address: [email protected] (R. Duponnois). URL: http://www.mpl.ird.fr/lstm/ 0301-4797/$ e see front matter Ó 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.jenvman.2013.05.009
2008; Smith and Read, 2008). However, the success of inoculation depends on the type, viability, efficiency and infectivity of the inoculum (Rossi et al., 2007). Casuarinaceae species are actinorhizal plants which originated from Australia. The term casuarina comes from the Malay word ‘kasuari’ due to the resemblance of the twigs and the plumage of the cassowary bird (Boland et al., 1994). These trees are widely established around the world with the exception of Antarctica. The family comprises four genera (Allocasuarina, Casuarina, Ceuthostoma and Gymnostoma) and approximately 86 species and 13 subspecies (Steane et al., 2003; Bisby et al., 2007). Among them, Casuarina equisetifolia, Casuarina glauca and C. cunninghamia are the most frequently introduced species in most African countries with the exception of Zimbabwe where C. junghuhniama is more widely planted (NRC, 1984). However, C. equisetifolia is the most widespread and the best known species. Casuarina grow best in humid tropical and subtropical climates in areas where the average rainfall ranges from 200 mm to 5000 mm, at altitudes between 0 and 1800 m above the sea level. Casuarina species are among the fastestgrowing of all trees and, in their early growth stages, they can grow up to two to 3 m per year, and reach a final height of 20e30 m (NRC, 1984). The wood is dense, hard and smokeless. It produces high
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quality charcoal and burns with great heat even when green; it has low ash content. C. equisetifolia is one of the best types of firewood in the world (El-Lakany et al., 1990). The calorific value of its wood is up to 5000 kcal kg1 and that of its charcoal more than 7000 kcal kg1. Casuarina is used in the reclamation of salt-affected land, as windbreaks, for the stabilization of sand dunes, and for the production of firewood and timber. However, up to now, little is known about the exact Casuarina distribution in Africa: its potential benefits for the rehabilitation of degraded lands and the management of soil fertility. This review focuses on: 1) the distribution and ecology of Casuarina in Africa, 2) its uses and 3) the importance of the symbiotic relationships between Casuarina, arbuscular mycorrhizal (AMF), ectomycorrhizal (EMF) and/or Frankia bacteria in improving the role of Casuarina in soil rehabilitation. 2. Geographic distribution of Casuarina and its ecological importance in Africa 2.1. Geographic distribution of Casuarina in Africa Casuarina is widely distributed in Africa, where three of the four genera have been introduced: five species of Casuarina, three Allocasuarina spp. and one Gymnosoma sp. (Gtari and Dawson, 2011) have been introduced in Algeria, Benin, Burkina Faso, Cameroon, Central African Republic, Chad, Congo, Ivory Coast, Democratic Republic of Congo, Djibouti, Egypt, Eritrea, Ethiopia, Gabon, Gambia, Ghana, Guinea, Guinea-Bissau, Kenya, Liberia, Madagascar, Malawi, Mali, Mauritania, Niger, Nigeria, Senegal, Sierra Leone, Somalia, South Africa, Sudan, Tanzania, Togo, Uganda and Zimbabwe (Orwa et al., 2009; Gtari and Dawson, 2011) (Table 1). In some countries, including Senegal, Egypt, Benin, Kenya, South Africa, and Madagascar, Casuarina is widely planted, whereas in others its presence is very reduced and is limited to decoration. The selection of a particular species depends on several factors: the climatic conditions in the area concerned, proximity to the sea, wind, soil erosion and soil mineral deficiencies at the plantation sites (Sayed, 2011). 2.2. Importance of Casuarina plantations in Africa As pioneer species, Casuarina grows well in Africa in a range of climates and soils including disturbed, poor, coastal, and spoiled soils. In tropical and subtropical countries, it has been shown that Casuarina growth is stimulated by hot weather (Digiamberardino, 1986). Casuarina plantations have been established in the Niayes region in Senegal along the western coast between Dakar and StLouis, along the Mediterranean Coast of North Africa, in the Nile Delta and the Nile Valley in Egypt, in the Sémé zone in Benin between Cotonou and Porto Novo, and on the coastal dunes of KwaZulu-Natal in South Africa. In these countries, Casuarina plays a major role in sustaining ecosystem fertility. Table 1 Members of the Casuarinaceae family introduced in Africa. Species
Distribution in Africa
1. 2. 3. 4. 5. 6. 7. 8. 9.
North Africa, Tropical Africa North Africa, Tropical Africa North Africa, Tropical Africa Southern, Northern, Tropical Africa Southern, Northern Africa, Madagascar Southern, Northern, Tropical Africa Northern, Tropical Africa Tropical Africa Tropical Africa
Allocasuarina littoralis Allocasuarina torulosa Allocasuarina verticillata Casuarina cunninghamiana Casuarina equisetifolia Casuarina glauca (swamp oak) Casuarina junghuhniana Casuarina obesa (swamp she-oak) Gymnostoma deplancheanum
Source: Gtari and Dawson (2011).
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In the Niayes region in Senegal, the species is C equisetifolia. There, it stabilizes the coastal sand dunes and acts as a windbreak. This plantation produces large quantities of litter which is used as biofertilizer by local farmers. Leaf litter has been estimated at 3.3 t ha1 year1 in plantations between 6 and 34 years old (Mailly and Margolis, 1992). Extensively used in compost, the litter reduces the use of chemical products and improves soil fertility. The addition of composted litter to sand soils improves plant growth and yield (Soumaré et al., 2004). Similar positive effects were obtained by adding ramial chipped wood. The positive role of C. equisetifolia in soil fertility was demonstrated by Diallo et al. (2005); who found a high mineral N content in C. equisetifolia amended soil and net soil mineralization primarily influenced by C. equisetifolia. In Senegal, Casuarina is not widely used for wood production but dead branches are collected by the local populations for domestic uses such as firewood (Cisse and Gourbiere, 1993). C. equisetifolia is planted along streets and beaches as an ornamental tree. In other countries like Egypt, Casuarina is planted to protect desert highways thanks to its ability to grow well under harsh environmental conditions. In Egypt, Casuarina is mostly used for its significant ecological roles such as crop protection, shelterbelt, irrigation stabilisation, drainage canal banks, land reclamation and protection of buildings. In the Nile Delta and in the Nile Valley, Casuarina trees were planted to provide shade, to limit border effects, and as a windbreak. Biomass productivity of 12-year-old irrigated plantations has been estimated at 496 t ha1 of which the wood volume was 294 m3 ha1 (Megahed and El-Lakany, 1986). Used as a shelterbelt in intercropping systems in Egypt, C. glauca increased the yield of the sheltered crops (El-Sayed et al., 1983). In Egypt, this species plays an important economic role in the production of fuel timber, charcoal, wood for industry and for the manufacture of particle board. C. equisetifolia plantations also play an important role in Benin, where their wood is used by local people for fuelwood and timber. A ten-year-old C. equisetifolia plantation near the sea produced around 200 stacked cubic metres per ha1 (Buffe, 1961). In Kenya, Casuarina is mainly grown for poles and as an ornamental plant and is much less used for firewood, charcoal and as a windbreak. The major use of Casuarina is for the construction of local tourist hotels, villas and homes (Mbuvi et al., 2011). Casuarina was also used for the rehabilitation of the Bamburi cement factory in Mombasa (Siachoono, 2010). In Southern Africa, Casuarina has been used to reclaim former mining land and to stabilise the coastal dunes of KwaZulu-Natal. Two thirds of the area was replanted with C. equisetifolia for the development of a local charcoal industry (Van Aarde et al., 1996). In Madagascar C. equisetifolia was planted in Ivoloina region for the production of improved seeds to be used in forestation programmes. Casuarina cunninghamiana was planted in Mahelia for the same purpose (Chaix and Ramamonjisao, 2001). The above data confirm the ecological role of Casuarina in Africa, but several studies have shown that the growth and performance of Casuarina can be enhanced when it is associated with symbiotic microorganisms (Shah et al., 2006; He and Critchley, 2008). To ensure the sustainability of Casuarina plantation and to improve yield, we need to understand the relationship between the tree, mycorrhizal fungi (AMF, EMF) and nitrogen fixing Frankia bacteria. 3. Symbiotic relationship between Casuarina, AMF, EMF and/ or Frankia bacteria The efficiency of mycorrhizal and Frankia infection depends on the habitat of the host, the prevailing environmental conditions, and the associated plant species. Ectomycorrhizal, endomycorrhizal and Frankia symbionts can occur in the same plant root (Wang and Qiu, 2006).
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3.1. Casuarina/arbuscular mycorrhizal symbiosis AMF obligate symbionts can be cultivated in vivo or in vitro (Diop, 2004). AMF can be isolated in the field or trapped in soils using different methods as described by (Utobo et al., 2011), or used to transform hairy roots of carrot (Daucus Carota L.) (Declerck et al., 1998). After isolation, propagules such as spores, mycorrhizal roots, and hyphae are generally used for inoculation (Smith and Read, 2008; Eskandari and Danesh, 2010). Inoculation with AMF enhances plant growth by increasing nutrient availability via its network of hyphae which is extensively involved in nutrient uptake (Smith and Read, 2008). AMF significantly improves the ability of plants to acquire soil P (Smith et al., 2011) and in return, they benefit from plant carbohydrates (Kiers et al., 2011). Inoculation with AMF increases plant height, biomass and P content compared to non-inoculated plants (Elumalai and Raaman, 2009; Zhong et al., 2010). Among 13 symbiotic fungi, Glomus mosseae, Glomus fasciculatum, G. versiforme and Acaulospora laevis are considered to be the most efficient AMF to facilitate C. equisetifiolia development (Vasanthakrishna and Bagyaraj, 1993; Vasanthakrishna et al., 1995). Furthermore, mycorrhizal symbiosis confers resistance to abiotic stresses in Casuarina species (Zhong et al., 2010). Several studies have shown that arbuscular mycorrhizae are found in Casuarina species growing in dry conditions and that they play an important role by improving plant tolerance to drought (Zhang et al., 2010). This mechanism is based on a range of biochemical and physiological responses such as a lower permeability of plasma membrane induced by the AMF, and high soluble sugar and P content in the aerial parts of the plant. AMF also confer resistance to flooding (Rutto et al., 2002). C. equisetifolia mycorrhized seedlings were shown to be better adapted to flooding conditions than noninoculated seedlings (Osundina, 1997). It has also been shown that AMF protect the host plant against pathogens (Liu et al., 2007; Sayeed and Siddiqui, 2008). Other studies carried out by Evelin et al. (2009) showed that AMF improve plant tolerance to salt stress. However, the capabilities of AMF to protect plants from salt stress depend on the behaviour of each AMF species. In association with C. equisetifolia, AMF can be used to rehabilitate polluted soils such as those contaminated by heavy metals (e.g. former mines); they enhance plant growth on severely disturbed sites (Karimi et al., 2011). However, AMF colonisation may be reduced in disturbed conditions and a moderate AMF colonization level was obtained in a naturally revegetated former coal mine with C. equisetifolia (Kumar et al., 2003). Nevertheless, AMF are very important in disturbed conditions because they improve soil health (Gianinazzi et al., 2010). 3.2. Casuarina/ectomycorrhizal symbiosis In addition to symbiosis with AMF, Casuarina species are associated with EMF (Wang and Qiu, 2006). Ectomycorrhizal strains are isolated from fruiting bodies, and pure cultures are maintained in the laboratory as described by Rossi et al. (2007) and Diagne et al. (2013). Different types of EMF inocula such as soil containing propagules, fungal spores from fruiting bodies and vegetative mycelia are used to inoculate plants in the field or in the nursery (Rossi et al., 2007). Inoculation with selected specific and compatible EMF increases C. equisetifolia seedling growth and biomass, and improves plant nutrient contents such as N and P (Elumalai and Raaman, 2009; Zhong et al., 2010). However, a specific relationship between the fungal partner and the host plant is often observed. Theodorou and Reddell (1991) observed that Amanita sp. formed ectomycorrhizae on Allocasuarina littoralis and C. cunninghamiana but not on C. equisetifolia. Similar results
concerning host specificity were obtained by Dell et al. (1994). In glasshouse experiments, Duponnois et al. (2003) found that some ectomycorrhizal fungi were unable to colonize Casuarina while effective colonization was obtained with Allocasuarina using the same fungal strains. These authors concluded that Allocasuarina verticillata was ectomycorrhizal dependent, whereas C. glauca was endomycorrhizal dependent. Similar results were obtained by Thoen et al. (1990), who showed that the ability to form ectomycorrhizae is more common with the genus Allocasuarina than with the genus Casuarina. Sometimes the relationship between Casuarina and ECM fungi can fail and for instance, infection with Scleroderma can lead to seedling death (Dell et al., 1994). Ectomycorrhizal strains of Pisolithus and Scleroderma isolates formed a mantle and a Hartig net on A. verticillata but failed to form a Hartig net on C. glauca. Furthermore, it has been demonstrated that the intensity of ectomycorrhizal infection with Pisolithus tinctorius and Lacaria laccata is higher with C. equisetifolia than with C. cunninghamiana (Theodorou and Reddel, 1991). Taken together, these results indicate specificity between the plant and EMF. Like AMF, EMF improves plant resistance to different types of stress (Smith and Read, 2008). The beneficial effect of EMF on plant resistance to disease has been demonstrated in exotic species including Acacia holosericea (Duponnois et al., 2000). These symbiotic microorganisms increase plant resistance to pathogens by creating a physical barrier which prevents the pathogen from entering the plant root. It has also been demonstrated that the EMF strain Pisolithus tinctorius increased Casuarina tolerance to salt (Zhong et al., 2010). Taken together, these results highlight the importance of inoculating Casuarina with a specific EMF.
3.3. Tripartite Casuarina/ectomycorrhizal/arbuscular mycorrhizal symbiosis Plants of the Casuarina family can enter a relationship with EMF and/or AMF mycorrhizal fungi (Table 2) (Wang and Qiu, 2006). A total of 50% Casuarinaceae plants are associated with EMF, around 25% with AMF and 25% of Casuarinaceae species form symbioses with both (Wang and Qiu, 2006). During mycorrhizal establishment, colonisation with EMF and AMF do not occur simultaneously. AMF is established first followed by EMF. However, in the rare cases when EMF is established first, it could reduce AMF colonisation by forming a mantle which acts as a barrier to AMF infection. However, when AMF is established first, it has no negative effects on EMF infection (Chilvers et al., 1987). Dual inoculation with EMF and AMF improved plant growth (Misbahuzzaman and Newton, 2006; Ramanankierana et al., 2007). For C. equisetifolia plants, inoculation with both AMF and EMF significantly increased biomass and P content compared to plants inoculated with either AMF or EMF alone (Elumalai and Raaman, 2009). These results show the beneficial effects of AMF and EMF on plant performance and the positive effect of mycorrhizal symbiosis is very important for the sustainability and management of agricultural ecosystems (Gianinazzi et al., 2010). However, an antagonistic effect was observed when both symbionts were inoculated and was generally the result of high ectomycorrhizal colonization (Duponnois et al., 2003). Chen et al. (2000) showed that the EMF Laccaria strain was able to reduce AMF colonization. To avoid antagonistic effects, inoculation with compatible AMF and EMF is thus recommended. Casuarina is a pioneer species that is well adapted to environmental stresses. Some Casuarinas plants such as C. equisetifolia are known to be bio-accumulators (Ukpebor et al., 2010).
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Table 2 AMF and EMF able to form mycorrhiza in Casuarinas plants. AMF fungal species
Host plant species
ECM fungal species
Host plants species
Acaulospora laevis Gerdemann and Trappe Glomus albidum Walker and Rhodes
C. equisetioflia Casuarina sp.
Aminata sp. Elaphomyces sp
G. claroideum Schenck and Smith
Casuarina sp.
Hysterangium sp.
G. clarum Nicolson and Schenck
Casuarina sp.
Laccaria laccate (Scop ex Fr.) Bk. and Br
G. fascicultum (Thaxter Sensu Gerdemann) Gerdemann and Trappe G.geosporum (Nicolson and Gerdemann) Walker G.intraradices Schenck and Smith
C. equisetifolia
Paxillus involutus (Batch ex Fr.) Fr
C. cunninghamiana C. equisetifolia ssp. equisetifolia. L C. cunninghamiana Miq. Elaphomyces sp. C. equisetifolia ssp. equisetifolia. L C. cunninghamiana Miq. Elaphomyces sp. C. equisetifolia ssp. equisetifolia. L C. cunninghamiana Miq. Elaphomyces sp. Casuarina sp.
Casuarina sp. C. glauca
P. albus IR100 Bougher and Smith Pisolithis tinctorius (Pers.) Coker and Couch
Casuarina sp.
Rhizopogon luteolus Fr. and Nord
Allocasuarina verticillata C. equisetifolia ssp. equisetifolia. L C. cunninghamiana Miq. Elaphomyces sp. Casuarina sp.
G.mossae (Nicolson and Gerdemann) Gerdemann and Trappe G. rubiforme (Gerdemann and Trappe) Almeida and Schenck G. versiforme (Karsten) Berch Gigaspora margarita (Gerdemann and Trappe)
Casuarina sp.
Suillus granulatus (L. ex Fr.) Kuntze
Casuarina sp.
C. equisetifolia Casuarina sp.
S. piperatus (Bull ex Fr.) O. Kuntze Scleroderma sp.
Casuarina sp. C. equisetifolia ssp. equisetifolia. L C. cunninghamiana Miq. Elaphomyces sp.
Scutellospora sp. Gerdemann and Trappe Scutellospora sp. Gerdemann and Trappe Gigaspora margarita Becker and Hall
Casuarina sp. Casuarina sp. Casuarina. sp.
Sources: Theodorou and Reddell (1991); Vasanthakrishna et al. (1995), Duponnois et al. (2003); He and Critchley, (2008).
Inoculation with mycorrhizal fungi was shown to increase Casuarina resistance to different stresses (Smith and Read, 2008). Since Casuarina is more commonly associated with AMF, few studies are available on the association of Casuarina with EMF and AMF. 3.4. Casuarina/Frankia symbiosis Frankia is a genus of nitrogen fixing Gramþ filamentous bacteria that lives in symbiosis with actinorhizal plants including Casuarina spp. The symbiotic microorganism Frankia is the only member of the family Frankiaceae in the order Actinomycetales (Normand et al., 1996). Frankia has only been cultured since 1978, when the first successful isolation was carried out from root nodules of Comptonia peregrina (Callaham et al., 1978). The development of genetic tools for Frankia has been hampered by the lack of a reliable gene transfer system (Benson et al., 2011). To overcome this problem, the genomes of four Frankia strains were recently sequenced (Normand et al., 2007; Persson et al., 2011). Frankia strains are isolated from lobe nodule as described by (Zhang et al., 2012). Inoculation of these bacteria can be carried out in different forms; pure culture, Frankia entrapped in alginate beads, as a crushed nodule suspension, or using the soil from around nodulated plants (Mansour et al., 1990). After inoculation, different factors such as soil temperature, pH, type of soil, can affect the establishment of the Casuarina-Frankia symbiosis (Mansour, 2003). In the field, thanks to their symbiotic association with Frankia, actinorhizal trees such as Casuarina can grow on nitrogen deficient soils. The amount of nitrogen fixed by actinorhizal trees is comparable to the amounts fixed by legumes and their Rhizobium symbionts and these trees can contribute significantly to the Neconomy of ecosystems (Diem and Dommergues, 1990). In different environments, Frankia can increase the development of actinorhizal plants. However, response to Frankia inoculation may depend upon environmental conditions (Sayed, 2011). Numerous studies have demonstrated the positive effect of Frankia on the development of Casuarina (e.g. Elumaila and Raaman, 2009). Inoculation with efficient and effective Frankia strains increases growth, biomass, N and P content and Casuarina survival (Tellal et al., 2008; Valdez, 2008; Zhang et al., 2012). A Frankia inoculation experiment on C. cunninghamiana carried out in the hot dry river valley in Yuanmou, Yunnan Province, increased
the survival of inoculated seedlings by 10%e20.6% compared with uninoculated seedlings after transfer to the field (Zhong et al., 2010). The height of the trees after two years differed significantly among Frankia treatments. However, not all Frankia strains improved tree growth (Zhong et al., 2010). It is important to distinguish between the specificity related to the nodulation process and the specificity which concerns the nitrogen-fixing potential of the system. Reddell and Bowen (1985) observed a range of responses from ineffectiveness in nitrogen fixation to high effectiveness between Casuarina species-Frankia source combinations. To determine which strain of Frankia is the best symbiont for specific casuarina species inoculation experiments with both microorganisms are needed. Inoculation has been shown to improve Casuarina performance and establishment during reforestation programmes by enhancing nitrogen fixation and improving tolerance to abiotic and biotic stresses such as drought, salinity, polluted sites etc. (Tani and Sasakawa, 2003; Bargali, 2011). Inoculation with Frankia may mitigate the negative effect of root rot in C. equisetifolia caused by Rhizoctonia sp. (Huang et al., 2011). Accordingly, the outstanding ability of actinorhizal plants to survive in harsh conditions such as former mines or nitrogen deficient soils (Barrit and Facelli, 2001; Dutta and Agrawal, 2002) is largely due to their ability to form a relationship with Frankia. 3.5. Tetrapartite symbiosis: Casuarina/arbuscular mycorrhizal/ ectomycorrhizal/Frankia Casuarina forms a relationship with Frankia, AMF and EMF. Inoculation with Frankia increase N2 fixation by 15e80%, ectomycorrhizal colonization by 10e70% and endomycorrhizal colonization by 10e50% with EMF (He and Crichley, 2008). Several authors have reviewed the relationship between the mycorrhizal and actinorhizal symbioses in non-legumes. As expected, the presence of mycorrhizae and Frankia on the same roots stimulated the development and the nitrogen-fixing activity of the actinorhizal symbiosis by improving the mineral nutrition of the host plant, particularly phosphorus uptake (Gentili and Huss-Danell, 2003). Dual inoculation with AMF and Frankia enhanced Casuarina growth more than single inoculation (Vasanthakrishna et al., 1994).
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However these authors observed that the effect of G. fasciculatum was greater than that of Frankia. Inoculation of C. equisetifolia with both Frankia and G. mosseae increased total dry weight by more than 80% compared to plants inoculated with Frankia alone (Gauthier et al., 1983). Similar positive effects on plant development were obtained in other actinorhizal species (Oliveira et al., 2005; Orfanoudakis et al., 2010). In addition, Muthukumar and Udaiyan (2010) reported that seedlings inoculated with Frankia and G. geosporum had more -and heavier- nodules compared to seedlings inoculated with Frankia alone. These authors showed that inoculation with Frankia improved AMF colonisation which is involved in plant nutrient uptake. They also reported that by improving nutrient acquisition, the tetra-partite association (Frankia, G. geosporum, Paenibacillus polymyxa and C. equisetifolia) enhanced the growth and the seedling quality of C. equisetifolia under tropical nursery conditions. Inoculation with either AMF or EMF, with AMF and EMF, or with AMF, EMF and Frankia all improved Casuarina growth. Elumalai and Raaman (2009) demonstrated that triple inoculation with EMF, AMF and Frankia significantly increased fungal colonization and infection and also increased shoot and root length in C. equisetifolia. Similar results were obtained by Rajendran and Devaraj (2004) who found more nutrients including N, P, Ca, K and Mg released by litter from plants inoculated with AM and Frankia together. Inoculation with EMF or AMF increased plant nutrients and it was also demonstrated that through the common mycorrhizal network (CMN) formed by EMF or EMF mycorrhizal fungi; N was transferred from plant to another (He et al., 2009). The beneficial role of AMF and Frankia symbiosis was documented in two recent reviews: He and Crichley (2008), and Sayed (2011). Previously, Gardner (1986) reported that nodulation could be inhibited in C. equisetifolia colonised with AMF. This inhibition might be the result of competition between the microsymbionts for infection sites and/or nutrients. The same author suggests that competition for root infection between microsymbionts could be avoided by applying the inoculum at different times. Inoculation with Frankia alone increased plant height and wood production. It has been demonstrated that mycorrhiza fungi promote the success of Frankia symbiosis in Casuarina species by increasing N2 fixation, and the uptake of nutrients such as phosphorus (He and Critchley, 2008). Triple inoculation with EMF, AMF and Frankia was shown to significantly increase fungal colonisation and infection as well as shoot and root length in C. equisetifolia (Elumalai and Raaman, 2009). The same authors showed that these microorganisms also increased plant nutrient content including N and Pi in C. equisetifolia. As already mentioned in this paper, inoculation with microsymbionts such as AMF, EMF, and Frankia may be a biological tool to improve Casuarina performance in forestation programmes. 4. Conclusion Due to their tolerance to adverse soil and climate conditions Casuarina trees are biological tool for rehabilitation of degraded lands. The ability of Casuarina to survive in such harsh conditions is largely due to the symbiotic relationship with AMF, EMF, and Frankia. However, care should be taken to choose the best combination of Casuarina and the symbiotic microorganisms (Mansour, 2003; Sayed et al., 2007, Sayed, 2011) to be used in reforestation programmes. Strategies for plant improvement should include the selection of Casuarina species and varieties, and also the selection of the appropriate Frankia, AMF and EMF strains adapted to specific conditions such as drought, salinity, heavy metal pollution, flooding etc. Furthermore, the Casuarina plant should be associated with an effective and efficient symbiotic which will increase the efficiency of nitrogen fixation and P uptake for plant growth.
Casuarina, AMF, EMF, Frankia symbioses should be managed in a way to enhance Casuarina resistance to diseases and pests and improve performance under saline, waterlogged, drought and coastal conditions. References Bargali, K., 2011. Actinorhizal plants of Kumaun Himalaya and their ecological significance. Afr. J. Plant Sci. 5, 401e406. Benson, D.R., Brooks, J.M., Huang, Y., Bickhart, D.M., Mastronunzio, J.E., 2011. The biology of Frankia sp. strains in the post-genome era. Mol. Plant Microbe. Interact 24, 1310e1316. Bisby, F.A., Roskov, Y.R., Ruggiero, M.A., Orrell, T.M., Paglinawan, L.E., Brewer, P.W., Bailly, N., van Hertum, J. (Eds.), 2007. Species 2000 and ITIS Catalogue of Life: 2007 Annual Checklist. Reading, UK. Digital resource at. www.catalogueoflife. org/annual-checklist/2007/Species 2000. Boland, D.J., Brooker, M.I.H., Chippendale, G.M., Hall, N., Hyland, B.P.M., Johnston, R.D., Kleinig, D.A., Turner, J.D., 1994. Forest Trees of Australia. CSIRO, Melbourne, Australia. Barritt, A.R., Facelli, J.H.M., 2001. Effects of Casuarina pauper litter and grove soil on emergence and growth of understorey species in arid lands of South Australia. J Arid Environ 49, 569e579. Buffe, J., 1961. Les plantations de Casuarina equisetifolia (filao) dans le SudDahomey e Direction des Eaux et Forêts/CTFT: Expériences et travaux de reboisement forestier et de restauration des sols. Nogent-sur-Marne, France. Callaham, D., Del Tredici, P., Torrey, J.G., 1978. Isolation and cultivation in vitro of the actinomycetes causing root nodulation in Comptonia. Science 199, 899e902. Chaix, G., Ramamonjisao, L., 2001. Seeds production for Madagascar afforestation. Bois et Forêts des Tropiques 269, 46e63. Chen, Y.L., Brundrett, M.C., Dell, B., 2000. Effects of ectomycorrhizal and vesiculararbuscular mycorrhizas, alone and in competition, on root colonization and growth of Eucalyptus globulus and E. urophylla. New Phytol. 146, 545e556. Chilvers, G.A., Lapeyrie, F.F., Horan, D.P., 1987. Ectomycorrhizal vs endomycorrhizal fungi within the same roots system. New Phytol. 107, 441e448. Cisse, M., Gourbière, F., 1993. Décomposition de la litière de Filao (Casuarina equisetifolia forst) au Sénégal. Activité de la microfaune détritivore. ORSTOM, Dakar, 71p. multigr. Declerck, S., Strullu, D.G., Plenchette, C., 1998. Monoxenic culture of the intraradical forms of Glomus sp. isolated from a tropical ecosystem: a proposed methodology for germplasm collection. Mycologia 90, 579e585. Dell, B., Malajczuk, N., Bougher, N.L., Thomson, G., 1994. Development and function of Pisolithus and Scleroderma ectomycorrhizas formed in vivo with AlloCasuarina, Casuarina and Eucalyptus. Mycorrhiza 5, 129e138. Diagne, N., Thioulouse, J., Sanguin, H., Prin, Y., Krasova-Wade, T., Sylla, S., Galiana, A., Baudoin, E., Neyra, M., Svistoonoff, S., Lebrun, M., Duponnois, R., 2013. Ectomycorrhizal diversity enhances growth and nitrogen fixation of Acacia mangium seedlings. Soil Biol. Biochem. 57, 468e476. Diallo, M.D., Guisse, A., Badiane-Niane, A., Sall, S., Chotte, J.L., 2005. In situ effect of some tropical litters on N mineralization. Arid Land Res. Manag. 19, 173e181. Diem, H.G., Dommergues, Y.R., 1990. Current and potential uses and management of Casuarinaceae in the tropics and subtropics. In: Schwintzer, C.R., Tjepkema, J.D. (Eds.), The Biology of Frankia and Actinorhizal Plants. Academic Press, New York, pp. 317e342. Digiamberardino, T., 1986. Changes in a south east Florida Coastal Ecosystem after Elimination of Casuarina equisetifolia. Unpublished. Nova University. Diop, T.A., 2004. In vitro culture of arbuscular mycorrhizal fungi: advances and future prospects. Afr. J. Biotechnol. 2, 692e697. Duponnois, R., Founoune, H., Bâ, A.M., Plenchette, C., El jafaari, S., Nyera, M., Ducousso, M., 2000. Ectomycorrhization of Acacia holosericea A. Cunn. ex G. Don by Pisolithus spp. in Senegal: effect on plant growth and on the roots e knot nematode Meloidogyne javanica. Ann. Sc. For. 57, 345e350. Duponnois, R., Diedhiou, S., Chotte, J.L., Sy, M.O., 2003. Relative importance of the endomycorrhizal and/or ectomycorrhizal associations in AlloCasuarina and Casuarina genera. Can. J. Microbiol. 50, 691e696. Dutta, R.K., Agrawal, M., 2002. Effect of tree plantations on the soil characteristics and microbial activity of coal mine spoil land. Trop. Ecol. 43, 315e324. El-Lakany, M.H., Turnbull, J.W., Brewbaker, J.L., 1990. Advances in Casuarina Research and Utilization. DDC, AUC, Cairo, Egypt, 241p. El-Sayed, A.B., Omran, T.A., Khalil, A.E., 1983. Biomass characteristics of young Casuarina plantations in northwestern region of Egypt. Alex. J. Agric. Res. 31, 411e422. Elumalai, S., Raaman, N., 2009. In vitro synthesis of Frankia and mycorrhiza with Casuarina equisetifolia and ultrastructure of root system. Indian J. Exp. Biol. 47, 289e297. Eskandari, A., Danesh, Y.R., 2010. Study of life cycle of arbuscular mycorrhizal fungus Glomus intraradices using in vitro culturing technique. J. Phytol. 2, 69e75. Evelin, H., Kapoor, R., Giri, B., 2009. AMF in alleviation of salt stress: a review. Ann. Bot. 104, 1263e1280. Gardner, L.C., 1986. Mycorrhizae of actinorhizal plants. MIRCEN J. 2, 147e160. Gauthier, D., Diem, H.G., Dommergues, Y., 1983. Preliminary results of research on Frankia and Endomycorrhizae associated with Casuarina equisetifolia. In: Midgeley, S.J., Turnbull, J.W., Johnson, R.D. (Eds.), Casuarina Ecology, Management and Utilization. CSIRO, Melbourne, Australia, pp. 211e217.
N. Diagne et al. / Journal of Environmental Management 128 (2013) 204e209 Gentili, F., Huss-Danell, K., 2003. Local and systemic effects of phosphorus and nitrogen on nodulation and nodule function in Alnus incana. J. Exp. Bot. 54, 2757e2767. Gianinazzi, S., Gollotte, A., Binet, M.N., van Tuinen, D., Redecker, D., Wipf, D., 2010. Agroecology: the key role of arbuscular mycorrhizas in ecosystem services. Mycorrhiza 20, 519e530. Gtari, M., Dawson, J.O., 2011. An overview of actinorhizal plants in Africa. Funct. Plant Biol. 38, 653e661. He, X.H., Critchley, C., 2008. Frankia nodulation, mycorrhization and interactions between Frankia and mycorrhizal fungi in casuarina plants. In: Varma, Ajit (Ed.), Mycorrhiza e State of the Art, Genetics and Molecular Biology, Eco-function, Biotechnology, Eco-physiology, Structure and Systematics, third ed. Springere Verlap GmbH, Germany, pp. 767e781. He, X., Xu, M., Qiu, G.Y., Zhou, J., 2009. Use of 15N stable isotope to quantify nitrogen transfer between mycorrhizal plants. J. Plant Ecol. 2, 107e118. Huang, J., He, Hueyou, Cai, Shouping, Ke, Yuzhu, Chen, Duanqin, Tang, Chensheng, 2011. Current research on main casuarina diseases and insects in China. In: Zhong, C., Pinyopusarerk, K., Kalinganire, A., Franche, C. (Eds.), Improving Smallholder Livelihoods through Improved Casuarina Productivity. Proceedings of the 4th International Casuarina workshop. Haikou 22e25 March 2010, pp. 232e238. Karimi, A., Khodaverdiloo, H., Sepehri, M., Sadaghiani, M.R., 2011. AMF and heavy metal contaminated soils. Afr. J. Microbiol. Res. 5, 1571e1576. Kiers, E.T., Duhamel, M., Beesetty, Y., Mensah, J.A., Franken, O., Verbruggen, E., Fellbaum, C.R., Kowalchuk, G.A., Hart, M.M., Bago, A., Palmer, T.M., West, S.A., Vandenkoornhuyse, P., Jansa, J., Bücking, H., 2011. Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333, 888. http://dx.doi.org/ 10.1126/science.1208473. Kumar, A., Raghuwanshi, R., Upadhyay, R.S., 2003. Vesicular-arbuscular mycorrhizal association in naturally revegetated coal mine spoil. Trop. Ecol. 44, 253e256. Liu, J., Maldonado-Mendoza, I., Lopez-Meyer, M., Cheung, F., Town, C.D., Harrison, M.J., 2007. Arbuscular mycorrhizal symbiosis is accompanied by local and systemic alterations in gene expression and an increase in disease resistance in the shoots. Plant J. 50, 529e544. Mailly, D., Margolis, H.A., 1992. Forest floor and mineral soil development in Casuarina equisetifolia plantations on the coastal sand dunes of Senegal. For. Ecol. Manage. 55, 1e4. Mansour, S.R., 2003. Survival of Frankia strains under different soil conditions. J. Biol. Sci. 3, 618e626. Mansour, S.R., Dewedar, A., Torrey, J.G., 1990. Isolation, culture, and behaviour of Frankia strain HFPCgI4 from root nodules of Casuarina glauca. Bot. Gaz. 151, 490e496. Mbuvi, M.T.E., Muchiri, M.N., Wairungu, S.N., 2011. Modern silviculture practices versus livehood needs: the case of Casuarina growing along the Kenya Coastal Region. In: Improving Smallholder Livelihoods through Improved Casuarina Productivity. Proceedings of the 4th International Casuarina Workshop. Haikou 22e25 March 2010, pp. 232e238. Megahed, M.H., El-Lakany, M.H., 1986. Biomass characteristics of young Casuarina plantations in northwestern region of Egypt. Alex. J. Agric. Res. 31, 411e422. Muthukumar, T., Udaiyan, K., 2010. Growth response and nutrient utilization of Casuarina equisetifolia seedlings inoculated with bioinoculants under tropical nursery conditions. New Forests 40, 101e118. Misbahuzzaman, K., Newton, A., 2006. Effect of dual arbuscular-ectomycorrhizal inoculation on mycorrhiza formation and growth in E. camaldulensis Dehnh. Seedlings under different nutrient regime. Int. J. Agri Biol. 8, 848e854. National Research Council, 1984. Casuarinas: Nitrogen-fixing Trees for Adverse Sites. National Academy Press, Washington DC, USA. Normand, P., Orso, S., Cournoyer, B., Jeannin, P., Chapelon, C., Dawson, J., Evtushenko, L., Misra, A.K.,1996. Molecular phylogeny of the genus Frankia and related genera and emendation of family Frankiaceae. Int. J. Syst. Bacteriol. 46, 1e9. Normand, P., Lapierre, P., Tisa, L.S., Gogarten, J.P., Alloisio, N., Bagnarol, E., Bassi, C.A., Berry, A.M., Bickhart, D.M., Choisne, N., Couloux, A., Cournoyer, B., Cruveiller, S., Daubin, V., Demange, N., Francino, M.P., Goltsman, E., Huang, Y., Kopp, O.R., Labarre, L., Lapidus, A., Lavire, C., Marechal, J., Martinez, M., Mastronunzio, J.E., Mullin, B.C., Niemann, J., Pujic, P., Rawnsley, T., Rouy, Z., Schenowitz, C., Sellstedt, A., Tavares, F., Tomkins, J.P., Vallenet, D., Valverde, C., Wall, L.G., Wang, Y., Medigue, C., Benson, D.R., 2007. Genome characteristics of facultatively symbiotic Frankia sp. strains reflect host range and host plant biogeography. Genome Res. 17, 7e15. Oliveira, R.S., Castro, P.M.L., Dodd, J.C., Vosátka, M., 2005. Synergistic effect of Glomus intraradices and Frankia spp. on the growth and stress recovery of Alnus glutinosa in an alkaline anthropogenic sediment. Chemosphere 60, 1462e1470. Orfanoudakis, M., Wheeler, C.T., Hooker, J.E., 2010. Both the arbusculuar mycorrhizal fungus Gigaspora rosea and Frankia increase root system branching and reduce root hair frequency in Alnus glutinosa. Mycorrhiza 20, 117e126. Orwa, C., Mutua, A., Kindt, R., Jamnadass, R., Anthony, S., 2009. Agroforestry Database: a Tree Reference and Selection Guide Version 4.0. World Agroforestry Centre, Kenya. Osundina, M.A., 1997. Nodulation and growth of mycorrhizal Casurarina equisetifolia J.R and G. First in response to flooding. Bio. Fertil. Soils 26, 95e99. Persson, T., Benson, D.R., Normand, P., Vanden Heuvel, B., Pujic, P., Chertkov, O., Teshima, H., Bruce, D.C., Detter, C., Tapia, R., Han, S., Han, J., Woyke, T., Pitluch, P., Pennacchio, L., Nolan, M., Ivanova, N., Pati, A., Land, M.L., Pawlowski, K.,
209
Berry, A.M., 2011. Genome sequence of Candidatus Frankia datiscae Dg1, the uncultured microsymbiont from nitrogen-fixing root nodules of the dicot Datisca glomerata. J. Bacteriol. 193, 7017e7018. Rajendran, K., Devaraj, P., 2004. Biomass and nutrient distribution and their return of Casuarina equisetifolia inoculated with biofertilizers in farmland. Biomass Bioenerg. 26, 235e249. Ramanankierana, N., Ducousso, M., Rakotoarimanga, N., Prin, Y., Thioulouse, J., Randrianjohany, E., Ramaroson, L., Kisa, M., Galiana, A., Duponnois, R., 2007. Arbuscular and ectomycorrhizal of Uapaca bojeri L. (Euphorbiaceae): sporophore diversity, and soil microbial of root colonization, and effects on seedling growth and soil microbial catabolic diversity. Mycorrhiza 17, 195e208. Reddell, P., Bowen, G.D., 1985. Frankia source affects growth, nodulation and nitrogen fixation in Casuarina species. New Phytol. 100, 115e122. Rossi, J.M., Agenor Jr., F., Vetúria, L., Oliveira, V.L., 2007. Inoculant production of ectomycorrhizal fungi by solid and submerged fermentations. Food Technol. Biotechnol 45, 277e286. Rutto, K.L., Mizutani, F., Kadoya, K., 2002. Effect of root-zone flooding on mycorrhizal and non-mycorrhizal peach (Prunus persica Batsch) seedlings. Sci. Hort. 94, 285e295. Sayed, W.F., 2011. Improving Casuarina growth and symbiosis with Frankia under different soil environmental conditions-review. Folia Microbiol. 56, 1e9. Sayed, W.F., Zahran, H.H., Salem, W.M., 2007. Dominant rhizospheric microorganisms under some casuarinas and its effect on Frankia growth and nodulation capacity. Egypt. J. Biotechnol. 2, 201e218. Sayeed, M., Siddiqui, Z.A., 2008. AMF as potential bioprotectants against plant pathogens. Mycorrhizae: Sustain. Agric. For., 61e97. Shah, S.K., Shah, R.P., Xu, H.L., Aryal, U.K., 2006. Biofertilizers: an alternative source of nutrients for sustainable production of tree crops. J. Sustain. Agr 29, 85e95. Siachoono, S.M., 2010. Land reclamation efforts in Haller Park, Mombasa. Int. J. Biodiversity Conservation 2, 019e025. Smith, S.E., Read, D.J., 2008. Mycorrhizal Symbiosis, third ed. Academic Press. Smith, S.E., Jakobsen, I., Groenlund, M., Smith, F.A., 2011. Roles of arbuscular mycorrhizas in plant phosphorus nutrition: interactions between pathways of phosphorus uptake in arbuscular mycorrhizal roots have important implications for understanding and manipulating plant phosphorus acquisition. Plant Physiol. 156, 1050e1057. Soumaré, M.D., Mnkeni, P.N.S., Khouma, M., 2004. Effects of ramial chipped wood and litter compost of Casuarina equisetifolia Tomato growth and soil properties in Niayes, Senegal. In: Bationo, A. (Ed.), Managing Nutrient Cycles to Sustain Soil Fertility in Sub-saharan Africa. Triscope Consulting Publishers, p. 502p. Steane, D.A., Wilson, K.L., Hill, R.S., 2003. Using matK sequence data to unravel the phylogeny of Casuarinaceae. Mol. Phylogenet. Evol. 28, 47e59. Tani, C., Sasakawa, H., 2003. Salt tolerance of Casuarina equisetifolia and Frankia Ceql strain isolated from the root nodules of C. equisetifolia. Soil. Sci. Plant. Nutr 49, 215e222. Tellal, M., Qarro, M., Arahou, M., Abourouh, M., Tellal, R., Rhazi, L., Douira, A., 2008. Effet de l’actinomycète Frankia sur la croissance et la fixation de l’azote de Casuarina glauca et Casuarina cunninghamiana. Sécheresse 19, 211e216. Theodorou, C., Reddell, P., 1991. In vitro synthesis of ectomycorrhizas on Casuarinaceae with range of mycorrhizal fungi. New Phytol. 118, 279e288. Thoen, D., Sougoufara, B., Dommergues, Y., 1990. In vitro mycorrhization of Casuarina and AlloCasuarina species by Pisolithus isolates. Can. J. Bot. 68, 2537e2542. Ukpebor, E.E., Ukpebor, J.E., Aigbokhan, E., Goji, I., Onojeghuo, A.O., Okonkwo, A.C., 2010. Delonix regia and Casuarina equisetifolia as passive biomonitors and a bioaccumulators of atmospheric trace metals. J. Environ. Sci. 22, 1073e1079. Utobo, E.B., Ogbodo, E.N., Nwogbaga, A.C., 2011. Techniques for extraction and quantification of arbuscular mycorrhizal fungi. L. A. R. C. J. I 2, 68e78. Valdez, M., 2008. Frankia ecology. In: Pawlowski, K., Newton, W.E. (Eds.), Nitrogen Fixing Actinorhizal Symbioses. Springer, Berlin, Germany, pp. 4e72. Van Aarde, R.I., Coe, M., Niering, W.A., 1996. On the rehabilitation of the coastal dunes of KwaZulu-Natal. S. Afr. J. Sci. 92, 122e124. Vasanthakrishna, M., Bagyaraj, D.J., 1993. Selection of efficient VA mycorrhizal fungi for inoculating Casuarina equisetifolia. Arid. Soil Res. Rehabil. 7, 377e380. Vasanthakrishna, M., Bagyaraj, J.D., Nirmalnath, P.J., 1994. Responses of Casuarina equisetifolia to inoculation with Glomus fasciculatum and/or Frankia. For. Ecol. Manag. 68, 399e402. Vasanthakrishna, M., Bagyaraj, J.D., Nirmalnath, P.J., 1995. Selection of efficient VA mycorrhizal fungi for Casuarina equisetifolia e second screening. New For. 9, 157e162. Wang, B., Qiu, Y.L., 2006. Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16, 299e363. Yang, S.Y., Paszkowski, U., 2011. Phosphate import at the Arbuscule: just a nutrient? Mol. Plant Microbe. Interact. 24, 1296e1299. Zhang, Y., Zhong, C.L., Chen, Y., Chen, Z., Jiang, Q.B., Wu, C., Pinyopusarerk, K., 2010. Improving drought tolerance of Casuarina equisetifolia seedlings by arbuscular mycorrhizas under glasshouse conditions. New For.. http://dx.doi.org/10.1007/ s11056-010-9198-8. Zhang, X., Shen, A., Wang, Q., Chen, Y., 2012. Identification and nitrogen fixation effects of symbiotic Frankia isolated from Casuarina spp. in Zhejiang, China. Afr. J. Biotechnol. 11 (17), 4022e4029. Zhong, C., Zhang, Y., Chen, Y., Jiang, Q., Chen, Z., Liang, J., Pinyopusarerk, K., Franche, C., Bogusz, D., 2010. Casuarina research and applications in China. Symbiosis 50, 107e114.