ARBUSCULAR MYCORRHIZA OCCURRENCE IN COFFEA

Like many crops, coffee associates symbiotically with AMF (Sieverding Reference Sieverding1991). Numerous studies have shown the natural occurrence of AMF in the soils of coffee orchards, as well as the presence of mycorrhizal structures in coffee roots (Lopes et al. Reference Lopes, Oliveira, Dias and Schenck1983; Balota & Lopes Reference Balota and Lopes1996; Pavan et al. Reference Pavan, Chaves, Siqueira, Androcioli-Filho, Colozzi-Filho and Balota1999; Colozzi-Filho & Cardoso Reference Colozzi-Filho and Cardoso2000; Theodoro et al. Reference Theodoro, Alvarenga, Guimarães and Júnior2003; Muleta et al. Reference Muleta, Assefa, Nemomissa and Granhall2007). Lopes et al. (Reference Lopes, Oliveira, Dias and Schenck1983) identified 22 AMF species in coffee rhizosphere soil from a Brazilian coffee production region; the most frequent AMF genera found were Acaulospora and Glomus. These were also the predominant genera found in other coffee-cultivated soils in Venezuela, Colombia and Mexico (Riess & Sanvito Reference Riess and Sanvito1985; Toro-Garcia Reference Toro-Garcia1987; Cruz Reference Cruz1989). Other AMF genera, such as Scutellospora, Gigaspora and Sclerocystis, have also been described in different coffee orchard soils (Colozzi-Filho & Cardoso Reference Colozzi-Filho and Cardoso2000). Recently, in a native forest in Ethiopia, where coffee coexists with other trees in its original ecosystem, high AMF species richness has been reported, with representatives of five genera of AMF. Glomus was the dominant genera, followed by Gigaspora, Acaulospora, Entrophospora and Scutellospora (Muleta et al. Reference Muleta, Assefa, Nemomissa and Granhall2007).

Nevertheless, it is difficult to carry out taxonomic identification in ecological studies because of the low number of researchers in this area and the long training and experience necessary to be able to distinguish different AMF species. However, molecular techniques have helped to identify some AMF species occurring in soils or in plant roots (Rivillas & Dodd Reference Rivillas Osorio and Dodd1996; Tisserant et al. Reference Tisserant, Brenac, Requena, Jeffries and Dodd1998; Colozzi-Filho & Cardoso Reference Colozzi-Filho and Cardoso2000). Specific polymerase chain reaction (PCR) primers are being designed for different AMF to facilitate detection of symbionts within roots (Redecker Reference Redecker2000). In addition, the determination of some isozymes that occur only when AMF colonize roots has allowed for the identification of AMF in coffee, as well as some tropical legume mycorrhizae (Rivillas & Dodd Reference Rivillas Osorio and Dodd1996; Tisserant et al. Reference Tisserant, Brenac, Requena, Jeffries and Dodd1998). Even in poorly colonized coffee roots, a mycorrhiza-specific isozyme of Acaulospora tuberculata BEG41 has been found, indicating the high sensitivity of this technique in discriminating specific mycorrhizal associations (Dodd et al. Reference Dodd, Boddington, Rodriguez, Gonzalez-Chavez and Mansur2000).

The occurrence of different AMF genera and species in coffee soils and roots varies depending on several factors, such as edapho-climatic conditions and culture practices. For example, in some tropical and subtropical regions, climatic seasons are divided into rainy and dry seasons, as the amount of precipitation may vary dramatically. These changes may influence mycorrhizal colonization, as observed in coffee orchards in Brazil, with low colonization rates in the dry season that increase at the beginning of the rainy season (Saggin-Junior & Siqueira Reference Saggin-Junior, Siqueira and Siqueira1996). However, the great range in the proportion of adult coffee plants with mycorrhizae, varying from proportions as low as 0·04 to more than 0·80, indicates the existence of different environmental factors that influence colonization in the field: including different native AMF populations, soil inocula and cultural practices (Saggin-Junior & Siqueira Reference Saggin-Junior, Siqueira and Siqueira1996).

Crop age may also influence coffee mycorrhizal colonization, both positively, as already observed in coffee-shaded orchards in Colombia, or negatively, as in monocropping orchards in Brazil, where this response was related to crop sustainability (Saggin-Junior & Siqueira Reference Saggin-Junior, Siqueira and Siqueira1996) and to P requirements of coffee plants of different ages (Siqueira et al. Reference Siqueira, Saggin-Junior, Flores-Aylas and Guimarães1998; see below). Crop management and culture practices, such as liming, legume intercropping, organic management and monocropping, among many others, can alter a soil's physicochemical and biological characteristics and may thus greatly influence AMF diversity and abundance in soils. Liming, for example, usually influences AM colonization positively because of its effects on spore germination by eliminating fungistatic factors and by influencing the composition of AMF populations (Siqueira et al. Reference Siqueira, Hubbell and Mahmud1984).

In some areas of Brazil, coffee has been cultivated with high-density populations per unit area, increasing productivity and avoiding soil erosion (Pavan et al. Reference Pavan, Chaves, Siqueira, Androcioli-Filho, Colozzi-Filho and Balota1999). This cultivation system has been compared with traditional low-density cultivation, which favours soil erosion and contributes to organic matter and nutrient losses. Thus, it has been verified that high densities increase exchangeable Ca, Mg, K, extractable P, pH, moisture content and AM colonization of roots, thereby improving soil fertility (Pavan et al. Reference Pavan, Chaves, Siqueira, Androcioli-Filho, Colozzi-Filho and Balota1999).

Agroforestry systems, based on the cultivation of crops of interest under a diversity of shade trees, are recognized to reduce land degradation and increase nutrient availability (Young Reference Young1997). Additional advantages of these systems are derived from a suppression of coffee pests, such as couch grass (Digitaria salarum), temperature regulation and maintenance of diversity (Muschler Reference Muschler2001; DaMatta Reference DaMatta2004). Agroforestry coffee-growing systems are, in fact, a culture practice adopted in several countries, such as Colombia, Mexico and several countries in Central America. Cardoso et al. (Reference Cardoso, Boddington, Janssen, Oenema and Kuyper2003) investigated the vertical distribution of AMF spores under agroforestry (shaded) and monoculture coffee (unshaded) systems. Greater numbers of AMF spores were found in the deep soil layers of agroforestry systems than in monocultural coffee plantation soils. Cardoso et al. (Reference Cardoso, Boddington, Janssen, Oenema and Kuyper2003) suggested that the higher concentration of AMF spores was related to higher mycorrhiza occurrence at those soil depths, which may be important to increase P availability to plants and to improve the efficiency of P cycling processes in these coffee systems.

In a natural coffee forest in Ethiopia, the diversity of AMF spores in relation to the composition of shade tree species has been investigated recently and markedly higher densities of AMF spores were observed under leguminous shade trees compared with non-leguminous ones (Muleta et al. Reference Muleta, Assefa, Nemomissa and Granhall2007). The species of shade tree also had an influence on the distribution of AMF genera in coffee rhizospheres, with Acaulospora occurring more frequently under leguminous trees than under other shade tree families. The same authors found that nearly 0·95 of the collected coffee roots under the influence of different shade tree species were associated with two or more AMF genera, with Glomus, Gigaspora and Acaulospora being predominant.

NUTRITIONAL EFFECTS OF ARBUSCULAR MYCORRHIZA IN COFFEE

As with many other agronomic crops, AM growth promotion in coffee plants has been mainly attributed to the nutritional effects of the symbiosis (Siqueira et al. Reference Siqueira, Saggin-Junior, Flores-Aylas and Guimarães1998; Bhattacharya & Bagyaraj Reference Bhattacharya and Bagyaraj2002; Sanchez et al. Reference Sanchez, Montilla, Rivera and Cupull2005). Improvements in plant mineral nutrition are mainly related to uptake by extra-radical hyphae from the non-rhizosphere soil region and nutrient transport to the plant root (Schweiger & Jakobsen Reference Schweiger and Jakobsen2000). After N, P is the most frequently limiting macronutrient for plant growth and is needed in millimolar concentrations in the cellular environment. In order to meet this requirement, and considering the soil P-depleted areas that form around the roots, plants rely upon several mechanisms, such as high affinity transporters, the release of phosphatases and organic acids and association with AMF (Requena Reference Requena2005), which involves a highly regulated route for P exchange between plants and fungal symbionts (Poulsen et al. Reference Poulsen, Nagy, Gao, Smith, Bucher, Smith and Jakobsen2005). Thus, P is undoubtedly the most important nutrient taken up by AMF, which is reflected in the large number of reports focused on the improved P status of AM plants; this situation is no different for coffee. However, the uptake of nutrients other than P, such as N, Ca, Mg, Fe, Mn, Zn and Cu, is also influenced by AM (Clark & Zeto Reference Clark and Zeto2000). Sanchez et al. (Reference Sanchez, Montilla, Rivera and Cupull2005) found a positive effect of AMF inoculation on coffee P concentrations, which resulted in higher growth when compared with non-inoculated plants. However, depending on the AMF species inoculated, different responses were observed, with Glomus fasciculatum, Glomus mosseae and Glomus intraradices being the most efficient symbionts. In three typical coffee-cultivated soils in Costa Rica, Sanchez et al. (Reference Sanchez, Rivera, Gonzalez, Cupull, Herrera and Bustamante2000) observed that as soil fertility decreased, AMF inoculation increased efficiency in terms of growth. In this context, AM growth promotion was inversely related to soil P availability, with diminished positive effects as P availability increased. However, plant mycorrhizal dependency and symbiotic efficiency are directly influenced by soil P availability (Colozzi-Filho et al. Reference Colozzi-Filho, Siqueira, Saggin-Júnior, Guimarães and Oliveira1994; Saggin-Junior & Siqueira Reference Saggin-Júnior and Siqueira1995), making the degree of availability of adequate soil P a very important factor in the establishment of efficient mycorrhizal associations.

Osório et al. (Reference Osorio, Alzate and Ramirez2002) evaluated the effects of mycorrhizal inoculation and organic amendment on C. arabica seedling growth. Plant growth was improved by organic amendment and was further increased by mycorrhizal inoculation, but it was severely reduced in the unamended soil, which had low organic matter content, low pH, high extractable Al and low availability of P, B, Ca, Mg and K. Vaast & Zasoski (Reference Vaast and Zasoski1992) observed higher N, Ca and Mg accumulations in mycorrhizal coffee plants, which as a result showed better growth than non-mycorrhizal plants.

The beneficial effects of AM association on plant nutrition have also been observed in coffee plants propagated in vitro (Vaast et al. Reference Vaast, Zasoski and Bledsoe1996), where the association enhanced root and shoot growth of seedlings and plant P status, resulting in a lower root-to-shoot ratio when compared with non-mycorrhizal plants. Vaast et al. (Reference Vaast, Zasoski and Bledsoe1996) concluded that different AMF species presented different tolerances to increasing soil P availability, which were related to host foliar P status. The same happened for AMF pre-colonized coffee seedlings, which showed better development and a higher bean yield when transplanted into a low-fertility soil when compared with plants that were not pre-colonized (Siqueira et al. Reference Siqueira, Saggin-Junior, Flores-Aylas and Guimarães1998). In this highly weathered soil, mycorrhizal inoculation and P addition were complementary. However, the consistent effects of mycorrhiza on plant development and productivity diminished with crop age. These variable responses complicate the understanding of mycorrhizal effects on field crops, as many biological and chemical factors influence the coffee–mycorrhizal association. For example, as commented upon by Siqueira et al. (Reference Siqueira, Saggin-Junior, Flores-Aylas and Guimarães1998), young perennial plants have a high P requirement but this diminishes with plant age, explaining the importance of AMF inoculation during the nursery stage and in recently transplanted plants. In contrast, adult crops do not have the same requirement for P supplies as they do for other mineral nutrients that may represent limiting factors for coffee productivity.

Long-term P addition or high P input into soils has been related to the suppression of AM development, which may in turn reduce the uptake of Zn ions and of other nutrients by plants (Alloway Reference Alloway2004), decreasing the benefits of AM association. Phosphorus-induced Zn deficiency due to decreases in AM colonization has already been observed in coffee plants (Vaast Reference Vaast1995; Vaast et al. Reference Vaast, Zasoski and Bledsoe1996). On the other hand, increases in AM colonization resulted in higher foliar Zn concentrations, suggesting a correlation between AM colonization rates and Zn nutrition in coffee plants.

NON-NUTRITIONAL EFFECTS OF MYCORRHIZA

Besides positive nutritional effects, AM are known to increase resistance to drought and salinity and to increase tolerance to pathogens. It is recognized that AMF can influence the water balance of highly watered and dehydrated plants (Augé Reference Augé2001). The increase in root water uptake in mycorrhizal plants has been associated with an improvement in root conductance of water flow (Augé Reference Augé2001), including increases in the root length and alterations of the root morphology (Davies et al. Reference Davies, Svenson, Cole, Phavaphutanon, Duray, Olaldeportugal, Meier and Bo1996). In addition, when compared with non-mycorrhizal plants, mycorrhizal ones had higher stomatal conductance and transpiration rates, in addition to higher amounts of carbon fixed during water stress (Duan et al. Reference Duan, Neuman, Reiber, Green, Saxton and Augé1996), resulting in changes in leaf physiology and in intrinsic hydraulic or biochemical properties (Augé Reference Augé2001). More recently, it has been shown that root colonization by AMF enhances gene expression of tonoplast-localized aquaporins, transmembrane proteins that facilitate the membrane water potential gradient, thus improving the efficiency of mycorrhizal plants under drought conditions (Ruiz-Lozano Reference Ruiz-Lozano2003; Porcel et al. Reference Porcel, Gómez, Kaldenhoff and Ruiz-Lozano2005). While these studies were not performed with coffee plants, similar mechanisms might be suggested to enhance mycorrhizal coffee resistance under water deficit conditions.

In addition to the well-addressed AMF effects on plant physiology, other ecological processes have been attributed to mycorrhizal fungi, including their contributions to soil structure (reviewed by Rillig & Mummey Reference Rillig and Mummey2006), which is of great relevance for agroecosystem sustainability. AMF influence soil particle aggregation through biochemical, biophysical and biological processes, which include the mechanical action of fungal hyphae, the excretion of glycoproteins and other extracellular compounds, and AMF interactions with soil biota.

COFFEE PERFORMANCE UNDER DIFFERENT ENVIRONMENTAL STRESSES: THE ROLE OF MYCORRHIZAE

Coffee plants, as with other species and organisms, are subjected to numerous environmental stresses that may affect physiological processes. However, several plant mechanisms exist to counteract any possible negative effects on their metabolism. It is largely recognized that AM association is crucial in the ecology and physiology of many terrestrial plants, helping them to cope with several environmental stresses, such as drought, high metal concentrations, salinity and temperature stresses.

According to DaMatta (Reference DaMatta2004), world production of coffee beans is predicted to decrease dramatically, mainly due to unfavourable climatic conditions; in particular, drought is considered one of the main environmental stresses affecting coffee yield. Water limitation in coffee may cause physiological injuries, leading to the accumulation of different metabolites, such as proline (Mazzafera & Teixeira Reference Mazzafera and Teixeira1989).

The spread of coffee cultivation to marginal lands with unfavourable climatic conditions, together with global climatic changes, may constrain coffee yields and quality (Silva et al. Reference Silva, DaMatta, Ducatti, Regazzi and Barros2004); as such, drought and extreme temperatures are the main climatic limitations for expected commercial coffee production, as reviewed by DaMatta & Ramalho (Reference DaMatta and Ramalho2006). Those authors examined the importance and consequences of drought and temperature stress on coffee physiology and production. In this context, what is the role of mycorrhizae? The present authors found no reports that have studied the influence of mycorrhiza on coffee performance under different water availability or temperature conditions. Nevertheless, it can be inferred that efficient AMF inoculation may improve coffee development since mycorrhizal symbioses have resulted in better water relations for other important crop species, which in turn led to increased plant growth (Augé Reference Augé2001; Porcel et al. Reference Porcel, Gómez, Kaldenhoff and Ruiz-Lozano2005).

Soil salinity is a widespread problem restricting plant growth, especially in arid, semiarid and tropical areas. The coffee crop is expanding to new areas, until recently considered to be marginal or unsuitable for its cultivation, and it has frequently been necessary to provide additional irrigation in these regions. In addition, the lack of quality irrigation water in arid and semiarid areas, as well as in other areas with adequate climatic condition for coffee cultivation, sometimes contributes to saline/osmotic stress (Camargo Reference Camargo and Viegas1987). On this topic, some studies have shown that coffee seedlings are highly susceptible to salinity, leading to death after exposure to water salinity levels from 1·5 to 6·0 dS/m (Karasawa et al. Reference Karasawa, Silva, Miranda and Duarte2000). Nevertheless, older coffee seedlings coped well with salinity, since they are not subjected to excessive saline water (up to 2·0 dS/m) and adequate rain distribution occurs throughout the year (Matiello Reference Matiello1999). The present authors found no reports linking mycorrhizal effects to coffee performance under saline stress, but some workers have reported the presence of AM plants in salt stress environments (Ruiz-Lozano & Azcon Reference Ruiz-Lozano and Azcón2000; Aliasgharzadeh et al. Reference Aliasgharzadeh, Saleh Rastin, Towfighi and Alizadeh2001). In those studies, AMF prevented leaf dehydration caused by salinity and drought stress (Aroca et al. Reference Aroca, Porcel and Ruiz-Lozano2007) and, under control conditions, root hydraulic conductance in AM plants was about half that in non-mycorrhizal plants. The reduction in Na uptake, together with concomitant increases in P, N and Mg absorption and higher chlorophyll content in mycorrhizal plants, was suggested as important salt-alleviating mechanisms for plants growing in saline soils (Giri & Mukerji Reference Giri and Mukerji2004).

Some agricultural systems used for coffee cropping, such as monoculture, low planting density or the use of modern machinery in fields, may lead to soil compaction and soil degradation processes. The stressful effects of soil compaction result in the degradation of soil structure, reduced water potential, increased soil erosion and reduced root growth, which decrease plant growth and yields. AMF inoculation may to some extent improve plant growth (Miransari et al. Reference Miransari, Bahrami, Rejali, Malakouti and Torabi2007), mainly by increasing the root surface area through production of extra-radical hyphae.

The concentrations of heavy metals and other trace elements are increasing in soils due to human activities, threatening the correct functioning of the ecosystems. Metal toxicity in coffee, as is the case for other plant species, causes oxidative stress (Gomes-Junior et al. Reference Gomes-Junior, Moldes, Delite, Gratão, Mazzafera, Lea and Azevedo2006a, Reference Gomes-Junior, Moldes, Delite, Pompeu, Gratão, Mazzafera, Lea and Azevedob), which may lead to cellular damage and impaired function, resulting in growth and biochemical alterations (Mazzafera Reference Mazzafera1998) and excessive accumulation of metals in tissues. In the specific case of coffee soils, pesticides, fertilizers or organic amendments are the most frequent exogenous sources of metals or chemical toxicity. In addition, soils with naturally high acidity and aluminium concentrations are frequent in tropical and subtropical soils. In this respect, Al toxicity affects the normal growth of coffee shoots and roots and diminishes P, Ca and Mn foliar concentrations (Pavan & Bingham Reference Pavan and Bingham1982). The protective effects of AM against excessive concentrations of Al have been shown by some authors (Cuenca et al. Reference Cuenca, De Andrade and Meneses2001; Konrad Reference Konrad2003), suggesting that the higher P uptake by mycorrhizal roots increases intracellular P concentrations, thus decreasing Al solubility by precipitation. Agricultural soils in Costa Rica (Wilcke et al. Reference Wilcke, Kretzschmar, Bundt, Saborío and Zech2000) and Kenya (Lepp et al. Reference Lepp, Dickinson and Ormand1984), and probably those from many other coffee-producing countries, have been successively amended with high application rates of Cu-containing fungicides, extensively used in coffee orchards for disease control, resulting in Cu accumulation in different soil horizons. Sewage sludge application in coffee orchards as a plant fertilizer and soil conditioner is becoming a frequent agricultural practice and a viable solution for sludge disposal (Martins et al. Reference Martins, De Camargo and Bataclia2005). Unfortunately, depending on the origin of the sludge, it may be a source of metal accumulation in soils. Metal accumulation in soils may lead to the transfer of these heavy metals to coffee plants, causing physiological disorders or excessive metal accumulation (Dickinson et al. Reference Dickinson, Lepp and Surtan1988; Loland & Singh Reference Loland and Singh2004) that could enter the food chain via agricultural products. Several studies have addressed the role of AMF in altering the capacity of plants to accumulate heavy metals and trace elements, as well as the functioning of plants under contaminated soil conditions (Rivera-Becerril et al. Reference Rivera-Becerril, Calantzis, Turnau, Caussanel, Belimov, Gianinazzi, Strasser and Gianinazzi-Pearson2002; Andrade et al. Reference Andrade, Abreu, De Abreu and Silveira2004, Reference Andrade, Silveira, Jorge and De Abreu2007).

PATHOGEN–ARBUSCULAR MYCORRHIZA INTERACTIONS IN COFFEE

Plant-parasitic nematodes associated with coffee planting stocks in coffee nurseries and orchards include root-knot (Meloidogyne spp.) and root-lesion (Pratilenchus spp.). Coffee infection by nematodes causes reductions in plant growth and coffee bean yield, leading to important production losses ranging from 15 to 60% (Campos et al. Reference Campos, Lima and Almeida1985). Sustainable agriculture is characterized by low agro-chemical inputs for crop production systems, and plant–microbe interactions have been considered in order to promote plant nutrition and fitness. In this sense, mycorrhizal inoculation may benefit a plant's ability to resist biotic stressors by conferring a certain degree of tolerance and ability to withstand pathogenic attack (Azcón-Aguilar & Barea Reference Azcón-Aguilar and Barea1996). AMF association with plant roots may increase P uptake by plants and compete for penetration sites and nutrients with soil-borne pathogens, decreasing the deleterious effects of root pathogens (Azcón-Aguilar & Barea Reference Azcón-Aguilar and Barea1996).

Baumann (Reference Baumann2006) speculated about the possible role of caffeine exudation by coffee roots in the establishment and ‘condition’ of an adequate seedling rhizosphere for plant development, facilitating mycorrhiza formation. In this way, coffee plants would be more prepared to withstand soil-borne pathogens, such as nematodes. The recently discovered decaffeinated coffee plant would be a suitable plant material to test this suggestion (Silvarolla et al. Reference Silvarolla, Mazzafera and Fazuoli2004), as caffeine is absent in the whole plant (Silvarolla & Mazzafera, unpublished results).

Some work has shown that Gigaspora margarita or P supply increased coffee tolerance to Meloidogyne incognita, diminishing damages in fine root production (Lopes et al. Reference Lopes, Portugal, Gonçalves, Dias and Costa1987) or, independently of the added P, promoting seedling growth and improving mineral nutrition (Lana et al. Reference Lana, Zambolin, Valle and Santos1991; Vaast Reference Vaast1995). Coffee plants with well-established mycorrhizal symbioses and improved P status had enhanced tolerance to Pratylenchus coffeae, and it was observed that AM inoculation limited the extent of nematode lesions (Vaast et al. Reference Vaast, Caswell-Chen and Zasoski1998). The protective effects of AMF inoculation against nematodes have been described in other important cultures, such as olive trees, banana and peach-almond (Calvet et al. Reference Calvet, Pinochet, Hernández-Dorrego, Estaún and Camprubí2001; Elsen et al. Reference Elsen, Baimey, Swennen and De Waele2003; Castillo et al. Reference Castillo, Nico, Azcón-Aguilar, Del Río Rincón, Calvet and Jiménez-Díaz2006). In olive plants, mycorrhizal inoculation significantly reduced root galling severity resulting from root infections by Meloidogyne incognita and Meloidogyne javanica and also reduced nematode reproduction (Castillo et al. Reference Castillo, Nico, Azcón-Aguilar, Del Río Rincón, Calvet and Jiménez-Díaz2006). Several mechanisms have been suggested to explain AMF's protection against several pathogens, including increasing production of phenolic compounds, induction of some resistance mechanism and plant defence system activation (Benhamou et al. Reference Benhamou, Fortin, Hamel, St Arnaud and Shatilla1994; Gianinazzi-Pearson et al. Reference Gianinazzi-Pearson, Dumas-Gaudot, Gallotte, Tahiri-Alaoui and Gianinazzi1996). Thus, mycorrhizal inoculation of coffee plants in nurseries may be a useful practice for minimizing the deleterious effects of nematode infection (Vaast et al. Reference Vaast, Caswell-Chen and Zasoski1998).

OTHER ASPECTS OF THE COFFEE–AMF ASSOCIATION

Frequently, AMF are considered to be unable to decompose complex organic molecules due to their small production of hydrolytic enzymes and their obligatory biotrophism (Varma Reference Varma, Varma and Hock1999), and have been excluded from studies of the degradation of organic substances. However, the importance of AMF for retention and mineral nutrient recycling in montane tropical ecosystems has been pointed out recently (Aristizabal et al. Reference Aristizabal, Rivera and Janos2004), based on the occurrence of AMF spores, hyphae and vesicles within decomposing leaves of several montane plant species, including C. arabica L.

AMF may also influence the concentration and composition of secondary metabolites, such as essential oils (Khaosaad et al. Reference Khaosaad, Vierheilig, Nell, Zitterl-Eglseer and Novak2006), apocarotenoids (Fester et al. Reference Fester, Hause, Schmidt, Halfmann, Schmidt, Wray, Hause and Strack2002) and phenolic compounds (Devi & Reddy Reference Devi and Reddy2002), among others. It would be of interest to investigate the influence of these symbiotic fungi on coffee beans, as several secondary metabolites are involved in the quality of the beverage produced from these beans, including alkaloids (Ashihara Reference Ashihara2006), chlorogenic acids (Farah & Donangelo Reference Farah and Donangelo2006) and terpenes (Speer & Kölling-Speer Reference Speer and Kolling-Speer2006).

MYCORRHIZAL TECHNOLOGY APPLICATION IN COFFEE

Commercial substrates for coffee seedling production found on the market are usually poor in nutrients and require fertilization. In this respect, the use of AMF is of special interest for improving the efficient use of fertilizers and diminishing the amount required for adequate coffee seedling growth, as observed by Tristão et al. (Reference Tristão, Andrade and Silveira2006), who verified the positive effect of AMF inoculation in coffee seedlings growing in pine-bark- and coconut-fibre-based substrates.

Coffee seedlings are mainly produced by farmers from selected seeds. Seedlings at an appropriate stage are then transferred to the field. However, in coffee nurseries, in order to control soil diseases, seedlings are frequently produced in sterilized, fumigated soils or commercial substrates that are not conducive to mycorrhiza formation (Howeler et al. Reference Howeler, Sieverding and Saif1987). Inoculation of highly effective AMF is expected to greatly improve the nutritional state of seedlings and their establishment after transplantation, as already verified by some authors (Lopes et al. Reference Lopes, Oliveira, Dias and Schenck1983; Sieverding & Toro Reference Sieverding, Toro, Gianinazzi-Pearson and Gianinazzi1986; Siqueira et al. Reference Siqueira, Colozzi-Filho, Oliveira, Fernandes and Florence1987; Rivera et al. Reference Rivera, Fernández, Hernández and Fernández2003). Thus, AMF inoculation may constitute a viable economic alternative for efficient seedling production, decreasing the use of fertilizers and pesticides, diminishing the time for field transplantation and producing more vigorous plants able to better withstand environmental stresses during the acclimatization period (Costa et al. Reference Costa, Cavalcante, Lima and Maia2003). Siqueira et al. (Reference Siqueira, Saggin-Junior, Flores-Aylas and Guimarães1998) calculated the benefit under Brazilian low-fertility soil conditions of mycorrhizal pre-colonization of coffee transplants with respect to the savings on P fertilizers, estimating the mycorrhizal effect to be equal to 254 kg/ha of P₂O₅ and equal to a cost of US$ 20·00 per ha of AMF inoculation.

Arbuscular mycorrhizal inoculation has also been found to improve the growth and nutrient uptake of several in vitro propagated perennial plants (Blal et al. Reference Blal, Morel, Gianinazzi-Pearson, Fardeau and Gianinazzi1990; Vidal et al. Reference Vidal, Azcon-Aguilar, Barea and Pliegoalfaro1992; Aguín et al. Reference Aguín, Mansilla, Vilariño and Sainz2004; Lovato et al. Reference Lovato, Trouvelot, Gianinazzi-Pearson and Gianinazzi2006), and also of Arabica coffee plants (Vaast et al. Reference Vaast, Zasoski and Bledsoe1996). In vitro propagated C. arabica plants have relatively small root systems, which affects nutrient uptake efficiency and leads to a lack of benefit from fertilizer addition. AMF inoculation has been shown to improve P status and growth in coffee propagated in vitro, confirming the high AMF dependency of coffee seedlings (Vaast et al. Reference Vaast, Zasoski and Bledsoe1996).

The selection process for formulating effective AMF inoculants for a target plant and/or variety should consider the physiological and ecological adaptations of native AMF to the target environment (Calvente et al. Reference Calvente, Cano, Ferrol, Azcón-Aguilar and Barea2004). Those authors verified the higher effectiveness of native AMF for promoting growth during the commercial nursery production of olive varieties. Unfortunately, mycorrhizal technologies, such as AMF inoculants, are not always available in most coffee-producing countries, making it difficult to incorporate this sustainable technology where its use can be of highest relevance. However, commercially available mycorrhizal inoculum normally leads to an extremely high density of AMF propagules per volume of soil (Costa et al. Reference Costa, Cavalcante, Lima and Maia2003), thereby enabling a rapid mycorrhizal establishment of coffee seedlings and making AMF inoculation a highly recommended practice at the nursery stage. Therefore, AM fungi are gaining popularity as biofertilizers and biocontrol agents (Sylvia Reference Sylvia, Siqueira, Moreira, Lopes, Guilherme, Faquin, Furtini Neto and Carvalho1999) and the industry of mycorrhizal inoculum production is expanding around the world (Corkidi et al. Reference Corkidi, Allen, Merhaut, Allen, Downer, Bohn and Evans2004; Todd Reference Todd2004).