Interaction of Symbiotic Rhizobia and Parasitic Root-Knot Nematodes in Legume Roots: From Molecular Regulation to Field Application

Abstract

Legumes form two types of root organs in response to signals from microbes: nodules and root galls. In the field, these interactions occur concurrently, and often interact with each other. The outcomes of these interactions vary, and can depend on natural variation in rhizobia and nematode populations in the soil, as well as abiotic conditions. While rhizobia are symbionts that contribute fixed nitrogen to their hosts, parasitic root knot nematodes (RKN) cause galls as feeding structures that consume plant resources without a contribution to the plant. Yet, the two interactions share similarities, including rhizosphere signaling, repression of host defence responses, activation of host cell division and differentiation, nutrient exchange and alteration of root architecture. Rhizobia activate changes in defence and development through Nod factor signaling, with additional functions of effector proteins and exopolysaccharides. RKN inject large numbers of protein effectors into plant cells that directly suppress immune signaling and manipulate developmental pathways. This review examines the molecular control of legume interactions with rhizobia and RKN to elucidate shared and distinct mechanisms of these root-microbe interactions. Many of the molecular pathways targeted by both organisms overlap, yet recent discoveries have singled out differences in the spatial control of expression of developmental regulators that may have enabled activation of cortical cell division during nodulation in legumes. The interaction of legumes with symbionts and parasites highlights the importance of a comprehensive view of root-microbe interactions for future crop management and breeding strategies.

Modulators or facilitators? Roles of lipids in plant root–microbe interactions

“…Plants initiate an interaction by secreting these chemical signals into the rhizosphere. Some examples are plant-produced flavonoids [PK] such as 2-phenyl-1,4benzopyrone derivatives involved in root nodule formation [35]; inhibitory flavonoids such as phytoalexin, medicarpin, and glyceollin [36]; and the volatile organic compound (VOC) (E)-βcaryophyllene [PR] that functions as a plant bioprotectant against herbivores and pathogens and as an attractant for organisms preying on root-feeding herbivores from maize roots [37,38]. These chemotactic attractors can facilitate the recruitment, nutrition, shaping, and tuning of the microbial communities from a reservoir of microorganisms present in the soil by encouraging, limiting, or inhibiting microbial activity and proliferation [8,9,36] (Figure 2A-1).…”

“…Perception of these compounds then leads to the stimulation of regulatory or signaling cascades that cause various responses in the microbes. Root-secreted substances have been thought to influence the gene expression of different microorganisms in the rhizosphere, which are not in proximity to and associated with plants [36]. Chemical communication (cell-cell signaling) with signal molecules called 'autoinducers' that increase in concentration as a function of cell density, found in bacteria [39] and recently in fungi [40], coordinate a wide range of activities within and between different species as a function of population density.…”

A generalist nematode destabilises plant competition: no evidence for direct effects, but strong evidence for indirect effects on rhizobium abundance

“…Interactions between hosts and co-occurring symbiotes is a common and important phenomenon in disease ecology (Budischak et al, 2012;Hersh et al, 2012;Marchetto & Power, 2018;Wood et al, 2018;Costa et al, 2021). How plant hosts respond to nematode infection has especially important consequences for rhizobia nodulation because of the overlap in signalling pathways used by root-knot nematodes and rhizobia (Wood et al, 2018;Costa et al, 2021).…”

“…We predicted that in the absence of parasitic nematodes, the legume M. lupulina would have an advantage over non-legumes and legume species with fewer nodules because higher nitrogen budgets increase photosynthetic efficiency and benefit hosts (Venterink, 2011;Wood et al, 2018;Evans & Clarke, 2019). In the presence of nematodes, we predicted that a decrease in rhizobia abundance on M. lupulina would shift the competitive advantage to non-legume species and legume species that lost fewer (or gained) rhizobia nodules after nematode inoculation (Wood et al, 2018;Costa et al, 2021). Such a shift might alter fitness differences (biomass changes in Fig.…”

“…To capture ecologically relevant variation in hostpathogen interactions, our community of plant hosts included species from three taxonomic families known to vary in their resistance to Meloidogyne: asters (Asteraceae), grasses (Poaceae) and nitrogen-fixing legumes (Fabaceae) (Castagnone-Sereno et al, 2013). Less information is known about tolerance to Meloidogyne in this system, but hosts often exhibit a trade-off between resistance and tolerance (Paudel & Sanfac ¸on, 2018;Costa et al, 2021). If competitor species are more resistant to Meloidogyne than our focal host M. lupulina, then we expect pathogen dilution to stabilise competitive interactions (Fig.…”