ReviewArbuscular mycorrhizal fungi act as biostimulants in horticultural crops
Graphical abstract
Introduction
A primary issue for modern horticulture is facing two contradictory objectives, such as the need to produce food for the increasing world population and to minimise damage to the environment, which can in turn negatively impact horticulture (Duhamel and Vandenkoornhuyse, 2013). Meeting the former two goals represents a major sustainability challenge to the horticultural industry and scientists (Owen et al., 2015). In the last decade, several technological innovations were proposed in order to enhance the sustainability of production systems through a significant reduction of chemicals. A promising and effective tool would be the use of ‘biostimulants’. The term biostimulants, often used in the plural form (Hamza and Suggars, 2001), refers to a group of compounds that act neither as fertilisers nor as pesticides, but have a positive impact on plant performance when applied in small quantities (Du Jardin, 2012, Calvo et al., 2014). However, plant biostimulant is still a ‘moving target’ in the European Union, and its use in the scientific community is still nebulous (Du Jardin, 2012). According to a general definition introduced by the European Biostimulants Industry Council (EBIC) in 2012, ‘Plant biostimulants contain substance(s) and/or microorganisms whose function when applied to plants or to rhizosphere is to stimulate natural processes to enhance nutrient uptake, efficiency, tolerance to abiotic stress, and crop quality, with no direct action on pests’ (www.biostimulants.eu). Among beneficial microorganisms, arbuscular mycorrhizal fungi (AMF) play a key role in plant performance and nutrition due to their capacity to improve plant mineral uptake (Smith and Read, 2008). AMF can only be grown in the presence of host plants (i.e. obligate symbionts; Owen et al., 2015), and are widely used in horticulture, in particular Rhizophagus (formerly known as Glomus) intraradices and Funneliformis (formerly known as Glomus) mosseae (Krüger et al., 2012). In fact, while the majority of inoculants presented on the market were mostly nitrogen-fixing bacteria products, it is expected that phosphorus-mobilising products including AMF will see an increase in demand (Transparancy Market Research, 2014).
AMF symbiosis is particularly important for enhancing the uptake of the relatively immobile and insoluble phosphate ions in soil, due to interactions with soil bi- and trivalent cations, principally Ca2+, Fe3+, and Al3+ (Tinker and Nye, 2000, Fitter et al., 2011). The basis of this symbiosis is the capacity of AMF to develop a network of external hyphae capable of extending the surface area (up to 40 times) and also the explorable soil volume for nutrient uptake (Giovannetti et al., 2001), throughout the production of enzymes and/or excretions of organic substances (Marschner, 1998). AMF can secrete phosphatases to hydrolyse phosphate from organic P compounds (Koide and Kabir, 2000, Marschner, 2012), and thus improving crop productivity under low input conditions (i.e. phosphorus deficiency, Smith et al., 2011). The extraradical hyphae are also important to increase the uptake of ammonium, immobile micronutrients such as Cu and Zn and other soil-derived mineral cations (K+, Ca2+, Mg2+, and Fe 3+) (Clark and Zeto, 2000, Smith and Read, 2008). AMF have been shown not only to improve plant nutrition (biofertilisers), but they also interfere with the phytohormone balance of the plant, thereby influencing plant development (bioregulators) and alleviating the effects of environmental stresses (bioprotector). This leads not only to increases in biomass and yield, but also to changes in various quality parameters (Antunes et al., 2012). The production of horticultural crops with high contents of phytochemicals (i.e. carotenoids, flavonoids and polyphenols) is a primary target that meets the demands of consumers and researchers due to their health-benefit effects (Rouphael et al., 2010a). In a recent review, Sbrana et al. (2014) reported that AMF symbiosis could induce changes in plant secondary metabolism leading to the enhanced biosynthesis of phytochemicals with health promoting properties. The same authors suggested that further research should investigate the mechanism(s) responsible for the increase in plant secondary metabolism through the selection of promising AMF taxa that are able to improve the nutraceutical value of horticultural products (Giovannetti et al., 2013).
In addition to the advantages mentioned above, AMF impart other important benefits such as tolerance to drought (Augé, 2001, Jayne and Quigley, 2014) and adverse soil chemical conditions in particular salinity (Evelin et al., 2009, Porcel et al., 2012), nutrient deficiency, heavy metal contamination (Garg and Chandel, 2010) and adverse soil pH conditions (Seguel et al., 2013, Rouphael et al., 2015).
Another promising tool and a meaningful approach for sustainable horticulture would be the co-inoculation with AMF and other microorganisms such as bacteria (i.e. PGPR) and beneficial fungi (i.e. Trichoderma spp.) (Xiang et al., 2012, Nadeem et al., 2014, Colla et al., 2015). The combined use of bacteria and AMF has been investigated in several studies but with contrasting results (Nadeem et al., 2014, Baum et al., 2015, Owen et al., 2015, Colla et al., 2015 and references cited therein). The synergetic/antagonistic effects of microbial inoculants were attributed to the nature and compatibility of the microbial strains used, as well as the interactions that take place between bacteria/fungi and plant species. Therefore, understanding which factors limit the performance of these bio inoculants will be very useful for improving the efficiency of this inoculum pool (Xiang et al., 2012, Nadeem et al., 2014).
Crop management involves a number of practices, which can influence AM symbiosis positively or negatively (see chapter 4; Gosling et al., 2006 and references cited therein). For instance, ploughing and high fertiliser application (i.e. P) can decrease AMF abundance and colonisation (Daniell et al., 2001, Avio et al., 2013, Lehmann et al., 2014). Other factors that may have detrimental effects on AMF symbiosis include the use of specific biocides and cropping with non-host plants (i.e. Brassicaceae, Chenopodiaceae) (Njeru et al., 2015). The later factor can be more deleterious to a highly mycorrhizal plants than phosphorus application or tillage (Gavito and Miller, 1998).
Another important factor is the genotype of a crop. Different cultivars of tomato, for instance, can respond to mycorrhization either with positive growth responses or with an increase in shoot phosphate concentrations (Boldt et al., 2011). Also, the fungal strain which is selected and used for inoculation of the plants can play a role. In petunia, for example, three different fungal species showed generally positive effects, but only one was able to protect the plant against a pathogenic root fungus (Hayek et al., 2012). Particular effects of AMF inoculation should therefore be tested among different genotypes and environmental conditions.
In short, the maximum multiple benefits will be obtained using efficient AMF strains after the accurate selection of compatible species/genotype-fungus combinations, and through favourable management practices (Regvar et al., 2003).
The present review focuses on the recent advances of the biostimulant actions of AMF on plant health, nutrition and quality of horticultural crops (fruit trees, vegetables and ornamentals). The agronomical and physiological processes conferring tolerance to abiotic stresses in AMF plants as well as the influence of bacteria interaction and farm management will also be covered. The review will conclude by identifying several possibilities for future studies to improve the biostimulant.
Section snippets
Taxonomy
AMF are formed between roots and a particular group of fungi, which are taxonomically separated from all other true fungi in the phylum Glomeromycota (Schüssler et al., 2001). Fossil and molecular phylogenetic data indicate that the first land plants already harboured AMF and would probably not have been able to enter the land without (Redecker et al., 2000). AMF are probably the most widespread plant symbionts and are formed by 80–90% of land plant species (Newman and Reddell 1987). This
Functional significance of bacteria associated with AMF
The establishment and efficiency of AMF symbiosis may be affected by bacteria living associated with mycorrhizal roots, spores, sporocarps and extraradical hyphae. Bacteria associated with AMF show different functional abilities, particularly the promotion of spore germination and asymbiotic hyphal growth. Although spores of some AMF species germinate well in axenic culture, higher spore germination percentages and germling extent have been reported in the presence of soil and rhizosphere
Influence of crop management practices on AMF
Efficient crop management is established to achieve horticultural produces with high yield and quality. In a previous review paper, Gosling et al. (2006) stated that ‘crop management involves a range of practices which can impact on the AMF association, both directly, by damaging or killing AMF, and indirectly, by creating conditions that are either favourable or unfavorable to AMF’. Compared with natural ecosystems, crop management has a negative impact on the AMF association. Agricultural
Drought
AMF are known to present an effective and sustainable tool with which to enhance drought tolerance in horticultural crops, including fruit trees, vegetables and flowers (Asrar et al., 2012, Wu et al., 2013, Jayne and Quigley, 2014, Baum et al., 2015) (Table 1).
AMF often induces modifications in the root architecture of plants, in particular root length, density, diameter, and number of lateral roots (Wu et al., 2013 and references cited therein). Better root system architecture in mycorrhizal
Effect of AMF on nutraceutical value of horticultural products
Recent findings showed that AMF symbioses are able to modify host plant primary and secondary metabolism, stimulating the production of phytochemicals in the roots and shoots of mycorrhizal plants (Sbrana et al., 2014). Such physiological changes may be ascribed to a transient activation of host defence reactions in colonised roots and the accumulation of antioxidant compounds, such as the yellow pigment mycorradicin, which is produced in the roots of mycorrhizal gramineous plants (Strack and
Conclusions and prospects
The use of arbuscular mycorrhizal symbionts as a biostimulant in horticultural crops has greatly increased in the last two decades, mostly due to their ability to secure production and yield stability in an environmentally sustainable way. Throughout the review, we have examined the promising biostimulant effects of AMF to enhance the root system and thus, macro and micronutrients uptake via increased nutrient transport and/or solubilisation. Maximum benefits will be only achieved by adopting
Acknowledgements
The authors thank Louis Mercy (INOQ GmbH) for contributing Fig. 1. D.S. and P.F. are supported by the Federal Ministry for Consumer Protection, Food and Agriculture, by the Brandenburg Ministry of Sciences, Research and Cultural Affairs, and by the Thuringian Ministry of Infrastructure and Agriculture.
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