Plant-Nematode Interactions Assisted by Microbes in the Rhizosphere
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Plant-Nematode Interactions Topalović and Heuer Curr. Issues Mol. Biol. (2019) 30: 75-88. caister.com/cimb Plant-Nematode Interactions Assisted by Microbes in the Rhizosphere Olivera Topalović1* and Holger Heuer1 enriched endophytically and in the rhizosphere before and during parasitism events. PPN are 1Julius Kühn-Institut, Messeweg 11-12, 38104 considered one of the major pests of agricultural Braunschweig, Germany plants and it has been estimated that they cause yield losses up to $80 billion (Handoo, 1998). The *[email protected] majority of PPN belongs to the order Tylenchida, with the endoparasitic root-knot nematodes (RKN), DOI: https://dx.doi.org/10.21775/cimb.030.075 Meloidogyne spp., cyst nematodes (CN), Heterodera spp. and Globodera spp., and root- Abstract lesion nematodes (RLN), Pratylenchus spp., being Plant health is strongly influenced by the the most devastating phytonematodes (Nicol et al., interactions between parasites/pathogens and 2011). The RKN and CN are sedentary beneficial microorganisms. In this chapter we will endoparasites with infective second-stage juveniles summarize the up-to date knowledge on soil (J2) which move through soil and infect roots of host suppressiveness as a biological tool against plants. After reaching suitable root cells, they phytonematodes and explore the nature of become sedentary, and start producing feeding monoculture versus crop rotation in this regard. sites, syncytia (CN) or giant cells (RKN). This Since nematodes are successfully antagonized by results in nematode development into females that different microbiological agents, we highlighted this protrude egg masses inside or outside the root galls phenomenon with respect to the most important (RKN), or the eggs are encumbered in encysted antagonists, and a nature of these interactions. The female bodies (CN). The genus Pratylenchus focus is on the hyperparasitic microbes of includes migratory endoparasitic nematodes with all phytonematodes such as Pasteuria sp. and egg life stages (females, males, juveniles) being motile parasites. Furthermore, we comprised the studies and infective. on the defence system expressions in plants triggered by nematode-associated microbes. The Infective stages of PPN encounter a vast number of attachment of bacteria and fungi to phytonematodes soil microbiota before entering plants. This allows and putative effects of the attachment on the the attachment of diverse microbes to their cuticle induced systemic resistance in plants are and surface coat. What nematodes are probably not discussed. Finally, our chapter is rounded up with aware of is that when allowing the attachment and the importance of incorporating the knowledge on agree on carrying the microbes to the plants, they plant-nematode-microbe interactions in the may cause self-deleterious effects, i.e. they can be integrated pest management. antagonized by transmitted microbiota. In the following lines, we will review the up-to-date Introduction knowledge on the importance and ability of Considering that every living macroorganism can be specifically attached soilborne microbes to suppress regarded as a holobiont as it is inevitably invasion and reproduction of PPN in plants. Our interconnected with its corresponding microbial intention is to confront the attainments, merits and cohabitants (Bordenstein and Theis, 2015; demerits of a plant mediated versus direct Vandenkoornhuyse et al., 2015), and transferring antagonism of PPN, with respect to different this phenomenon on the tripartite plant-nematode- nematode life strategies and antagonists involved. microbiome system, we can assume that the destiny The molecular aspects of a cross-communication of plants attacked by plant-parasitic nematodes between the plant, nematodes and nematode- (PPN) much depends on which microbes are attached microbes will be discussed, and the "75 Plant-Nematode Interactions Topalović and Heuer benefits of nematode-attached microbes to the plant population density of Criconemella xenoplax health will be summarized. dropped significantly in a suppressive soil between 1988-1991 (Kluepfel et al., 1993). Although edaphic Nematode-suppressive soils factors were nearly identical for both suppressive Two types of soil suppressiveness have been and non-suppressive sites, it was unclear whether described in the literature. One is general (non- these two sites were indeed comparable, and specific) soil suppressiveness which characterizes nematode population densities were not reduced the ability of any soil to suppress many pathogens below the damage threshold in the fields. Taking to a certain extent and is related to microbial activity into an account the feeding strategy of ectoparasitic (Davies and Spiegel, 2011). Specific soil nematodes, which do not enter the roots but feed suppressiveness is directed towards a particular only by piercing the epidermal root cells with their pathogen. It is exerted by a complete absence of stylets, it should be noted that the soil microbes pathogen establishment or, in the worst-case attached to the cuticle of these nematodes do not scenario it can cause a severe disease and then get into a direct contact with plants. This means that draw back with a continued growing of the host soil suppressiveness against ectoparasitic PPN plant (Baker and Cook, 1974). Both types of soil might be inefficient because they are less prone to suppressiveness are removed by sterilization, plant-mediated mechanisms of suppression. indicating the biological nature of soil suppressiveness, but the mechanisms and which On many occasions, it was proposed that the microbial species are involved is not sufficiently general indicators of the abundance and activity of explored. The previous research was focused on soil microbiota could give an indication whether direct antagonism of soil microbes towards microbial factors are responsible for soil soilborne phytopathogens, while plant-mediated suppressiveness. For instance, a role of the blanket mechanisms and plant-associated microbes have of sugarcane residues and mill mud amendments not been considered sufficient to explain and covering the surface of a sugarcane field was tested manage soil suppressiveness. The follow-up against the endoparasitic nematode Pratylenchus examples support the evidence that suppressive zeae (Stirling et al., 2011). Although more than 90% soils can be used as a powerful biocontrol measure of the sugarcane root biomass occupied the depth against PPN. In an early study by Crump and Kerry just beneath the trash blanket, the nematode (1987) a population of Heterodera schachtii failed to density at this depth was very low. One would increase in suppressive soil of a 2-year monoculture expect that a high total carbon and the readily of sugar beet and increased only in the third year. oxidisable carbon fraction measured within the Treatment of this soil with the fungicide Captafol upper soil profile when the soil surface mulched resulted in a greater nematode multiplication and a could have positively influenced soil microbial low fungal parasitism of females, suggesting that activity and reduced nematode population density at fungi played a role in this soil suppressiveness. The this depth (Stone et al., 2004; Stirling et al., 2005; soil was enriched with the nematophagous fungi Stirling et al., 2011). A similar observation was Pochonia chlamydosporia, Fusarium spp., and noticed after the density of Pratylenchus thornei had Cylindrocarpon destructans, which was isolated been depressed in upper soil layers of the wheat from infected females. These fungal species are fields (Stirling, 2011). well known parasites of CN (Jorgenson, 1970; Kerry, 1988). When Westphal and Becker (1999) The most common way to prove the biological had followed reproduction of H. schachtii on Swiss nature of soil suppressiveness includes the chard (Beta vulgaris L.) in a monoculture California comparison of nematode performance in sterilized field amended with H. schachtii-infested soil, the and non-sterilized soil. In assessing the effects of nematode population started declining after several gamma irradiation on soil properties, decreased years and remained very low in the following period. levels of NO3- and an increase of NH4+ were The soil suppressiveness was removed by recorded due to elimination of denitrifying bacteria biofumigation or a biocide-treatment. Similarly, a (Buchan et al., 2012). The absence of a microbial biological soil suppressiveness was responsible for community also resulted in a high abundance of a decreased reproduction of H. schachtii on Swiss labile carbon content due to its insufficient chard (Westphal et al., 2011). The soil fumigation utilization. This leads to the conclusion that the soil with iodide resulted in a higher nematode microbiota has a profound effect on plants by multiplication. In a rare example of soil manipulating soil mineral components, and soil suppressiveness against an ectoparasitic PPN the sterilization acts both against deleterious and "76 Plant-Nematode Interactions Topalović and Heuer beneficial microflora. For instance, a negative contain carbohydrate residues that specifically bind correlation was found between a shoot growth of lectins of the bacterial surface (Spiegel et al., 1995). white clover and soil gamma irradiation when The recognition between epitopes present on the studying soil suppressiveness against Meloidogyne bacterial surface and on the surface coat of hapla (Bell et al., 2016). Thus, in parallel with