Bioprotection by arbuscular mycorrhizal fungi in plants infected with Meloidogyne nematodes: A sustainable alternative
Introduction
Phytonematodes are parasitic nematodes that cause diseases in plants. Nematodes that infect plant roots are classified according to their location: those that attach and feed on cells on the outer surface of roots are called ectoparasites, while those that attach and feed on cells of the internal regions of roots are called endoparasites. Both are further subdivided according to how they move within the root. Phytonematodes that move freely inside or outside roots are called migratory, while those that settle in a feeding place are called sedentary (Perry and Wright, 1998). Parasites of the latter type cause severe damage to plants, especially in economically important crops. Meloidogyne nematodes, commonly known as root-knot nematodes, are sedentary endoparasites.
Mycorrhizae are symbiotic relationships between specific fungi and plant roots (mykes = fungus; rhiza = roots). The mutual benefit from this association comes from the specific roles that each symbiont plays—the plant provides carbohydrates and lipids (Keymer et al., 2017) to the fungus while the fungus provides the plant with mineral nutrients (P, N, and others) absorbed from the soil. Among the different types of mycorrhizae, the arbuscular type occurs in approximately 4/5 of all terrestrial plants, occupying several ecosystems. The fungi that participate in this symbiosis are called arbuscular mycorrhizal fungi (AMF), and are characterized by the formation of highly branched structures for nutrient exchange between the symbionts, called arbuscules. In general, they do not have host specificity, although a greater compatibility between certain AMF and plant species has been reported (Silva et al., 2004). More than 300 species of AMF are known today, which are in the subkingdom Mucoromyceta, phylum Glomeromycota, with 3 classes, 5 orders, 16 families, and 45 genera (Maia et al., 2015; Tedesco et al., 2018).
Arbuscular mycorrhizal fungi and Meloidogyne, both inhabitants of the rhizosphere, have opposite effects on plant growth (Siddiqui and Mahmood, 1995). Observations on the occurrence of interaction between nematodes and AMF in the field have led to several greenhouse studies under controlled conditions to better understand the process (Ingham, 1988), which is quite complex and dependent on the AMF and plant species and the interacting nematode (Cofcewicz et al., 2001; Jaizme-Vega et al., 1997), as well as the conditions to which they are subjected (Calvet et al., 2001; Maia et al., 2006). In general, sedentary nematodes, such as Meloidogyne spp., are more affected by AMF than are migratory nematodes (Borowicz, 2001; Hol and Cook, 2005).
Sustainable agriculture, supporting production high enough to guarantee human food security without negative impacts on the environment, is currently being promoted around the world. The use of AMF, that are naturally present in soil and acting as biostimulators and bioprotectors, can contribute to more sustainable cultivation practices, maintaining plant production and reducing pathogens without harming the environment. Given the importance of sustainable crop management and the lack of studies specifically addressing AMF and Meloidogyne interactions, the aim of this article was to review the use of AMF in the management of root-knot nematodes in various crops.
Section snippets
The interaction between AMF and Meloidogyne on plant growth and nematode development
The effect of AMF on the growth of plants infected with Meloidogyne is highly variable but generally positive (Borowicz, 2001; Maia et al., 2006). Moreover, the establishment of AMF often reduces nematode development (Table 1).
Mineral deficiency is a common symptom in plants parasitized by Meloidogyne, as they prevent absorption and transport of water and nutrients, negatively affecting plant development (Carneiro et al., 2002). Inoculation of such infected plants with AMF might increase the
Effects of the presence of AMF on plant tissue penetration, development, and reproduction of Meloidogyne
Besides increasing plant P uptake, AMF can also lead to a reduction in nematode reproduction as a result of the complex physiological changes induced in the plant by AMF colonization (Elsen et al., 2008). These include pre-infection changes, such as changes to plant root exudates. Vos et al. (2012a) observed a reduction in M. incognita penetration in the tomato cultivar Marmande after it received mycorrhizal root exudates, suggesting that this exudate negatively affects nematode motility in the
Interaction between AMF, Meloidogyne and other soil microorganisms
AMF also influence the mycorrhizosphere, inducing changes in soil microbial populations. This may stimulate microbial species that are antagonistic to nematodes (Azcón-Aguilar and Barea, 1996). Galal et al. (2012) observed an increase in the number of Pasteuria penetrans (Thorne) Sayre and Starr infecting M. javanica females in tomato plants treated with AMF.
Other soil organisms can positively interact with AMF to improve plant resistance to nematode attack. When AMF are inoculated together
The effect of soil amendments on the interaction between AMF and Meloidogyne
Nutrient availability, especially which of P, directly affects the interaction between AMF, nematode, and host, consequently affecting plant development. In general, the effect of AMF on plant growth is greatest in soils with low P availability. In soybean plants inoculated with AMF, the addition of P increased tolerance to Meloidogyne arenaria (Neal) Chitwood; however, AMF had the most pronounced effect on plant growth in the treatment with the least P (25 μg/g) (Carling et al., 1989). The
Final considerations
In this context, as shown by Hussey and Roncadori (1982), plants susceptible to nematodes appear to be more tolerant to the parasite when colonized by AMF. The presence of AMF may reduce the damage caused by nematodes by modifying the host plants’ response to the parasite, enabling it to better endure the infection. This protection is modulated by soil and environmental conditions (Azcón-Aguilar and Barea, 1996), and the responses are quite complex, making further studies on this interaction
Declaration of competing interest
No conflicts of interest.
Acknowledgement
The Institutional Program for excellence in the quality of the stricto sensu Support to the researcher APQ 2017 (University of Pernambuco) n ° 229. The Coordination for the Improvement of Higher Education Personnel (CAPES) for supporting the Postgraduate Program in Environmental Science and Technology (PPGCTAS), University of Pernambuco, Brazil.
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