Reciprocal plant‐mediated antagonism between a legume plant virus and soil rhizobia

Abstract

1. Beneficial plant-associated soil microbes can promote plant tolerance to stress and promote nutrient uptake. Yet, the benefits of microbes for plant health can be altered by above-ground stressors like herbivores and pathogens. However, few studies have assessed reciprocal plant-mediated interactions between beneficial soil microbes and multiple above-ground stressors.2. We assessed if soil rhizobia influenced complex interactions among pea host plants, a vector herbivore (aphids) and a plant virus (Pea enation mosaic virus, PEMV). We also examined how aphids and PEMV affected the function of soil rhizobia.3. We show that plants attacked by PEMV produced fewer root nodules and had lower fresh root nodule biomass per g of fresh plant root biomass, and decreased expression of genes associated with nodulation, suggesting PEMV inhibited nitrogen fixation by rhizobia. However, soil rhizobia decreased aphid abundance and PEMV titre on host plants, such that rhizobia decreased the susceptibility of plants to herbivores and pathogens. 4. Assays of amino acids, and gene expression related to hormone signalling, show interactions among rhizobia, plants, aphids and PEMV were mediated by plant defence and nutrients. Viruliferous aphids induced salicylic acid in plants, and salicylic acid suppressed the function of rhizobia. Aphids feeding on plants grown in rhizobia-inoculated soil also obtained fewer essential amino acids than those feeding on plants grown in un-inoculated sterilized soil.5. Mutually antagonistic plant-mediated interactions between soil microbes and above-ground stressors affected plant susceptibility and herbivore nutrient uptake. This suggests ecological effects of soil microbes and above-ground stressors for plant health will likely vary based on multi-trophic plant-mediated interactions among herbivores, pathogens and soil microbes.

Legume plant defenses and nutrients mediate indirect interactions between soil rhizobia and chewing herbivores

“…We observed plants attacked by S. lineatus had fewer nodules and lower nodule biomass than controls, suggesting antagonistic effects of S. lineatus on legume-rhizobia symbiosis. Previous studies have also shown that outbreaks of S. lineatus can promote the spread of aphid-borne viruses that also impede the function of rhizobia (Chisholm et al, 2019;Basu et al, 2021a); thus, we have shown that S. lineatus may negatively affect plant-rhizobia symbiosis through multiple indirect pathways.…”

Effects of Soil Rhizobia Abundance on Interactions between a Vector, Pathogen, and Legume Plant Host

“…Lipoxygenase 2 ( LOX2 ) works upstream of jasmonic acid biosynthesis, a phytohormone hormone used in defense against herbivore pests [ 29 , 30 ]. Similarly, 1-aminocyclopropane-1-carboxylic acid synthases 2 ( ACS2 ) is associated with ethylene synthesis [ 31 , 32 ], and Aldehyde oxidase 3 ( AO3 ) is associated with abscisic acid synthesis [ 33 , 34 ]. Besides ABA biosynthesis, AO3 is also involved in the production of reactive oxygen species (ROS) which, together with abscisic acid, provides resistance against pathogen infection [ 35 ].…”

Characterization of Rhizobium Isolates as Biocontrol Agents Against Fusarium Solani and Macrophomina Phaseolina

“…Rhizobia can improve plant growth through N 2 fixation and the availability of nutrients and minerals. Similarly, Rhizobia have shown to increase plant growth via the secretion of secondary metabolites of alkaloids and flavonoids that improve plant defense against pathogens (Basu et al, 2021). Earlier studies stated that Rhizobia could stimulate auto defenses in legumes via hormone signaling and start programmed cell death in pathogens (Dodds and Rathjen, 2010;Kumar et al, 2011).…”