Differential effects of the rhizobacterium Pseudomonas simiae on above‐ and belowground chewing insect herbivores

Abstract

Plant growth-promoting rhizobacteria (PGPR) can enhance plant growth and defence. Via plant-mediated effects, PGPR have been reported to impact the performance of generalist leaf-chewing insects either negatively or positively. However, only a few insect species, mainly feeding on aboveground tissues, have thus far been investigated. Here, we investigated how addition of rhizobacteria to the soil in which cabbage plants are growing affects the performance of three chewing insect herbivores, two leaf chewers and one root feeder. In a greenhouse experiment, we grew white cabbage (Brassica oleracea) plants in soil supplemented with and without the rhizobacterium Pseudomonas simiae WCS417r. We investigated the consequences for three important insect pests of Brassica species, larvae of the cabbage moth Mamestra brassicae, the diamondback moth Plutella xylostella, or the cabbage root fly Delia radicum after 5 weeks of plant growth. We recorded aboveground plant biomass, insect biomass, plant defence marker gene expression levels and plant defence-related hormone concentrations. Rhizobacterial inoculation increased aboveground plant biomass in non-infested plants but not in infested plants. Rhizobacterial inoculation affected insect performance differently: on PGPR-inoculated plants biomass of Plutella xylostella was lower, while biomass of Delia radicum was higher than on control plants. However, no effect was found on Mamestra brassicae biomass. Rhizobacterial inoculation increased the expression of the defence marker gene LOX2 in P. xylostella-infested plants and MYC2 in M. brassicae-infested plants. Transcription levels of the plant defence marker gene PAL1 showed upregulation between inoculated and non-inoculated insect-free plants. Levels of the phytohormones jasmonic acid, salicylic acid and abscisic acid were similar in inoculated and non-inoculated plants. We conclude that rhizobacterial inoculation has potential to be applied in the protection of cabbage crops against the diamondback moth whereas this does not apply to reducing damage caused by the cabbage moth or cabbage root fly. K E Y W O R D S cabbage moth (Mamestra brassicae), cabbage root fly (Delia radicum), diamondback moth (Plutella xylostella), plant resistance, rhizobacteria (Pseudomonas simiae WCS417r), white cabbage (Brassica oleracea) This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

Impaired microbial N-acyl homoserine lactone signalling increases plant resistance to herbivores across variable abiotic and biotic environments

“…Our study provides new insight into how microbial signalling molecules affect plant responses to aphids. Both A. radicis strains showed a consistent suppressive effect against aphids, similar to what is known for other beneficial bacteria (Martinuz et al, 2012;Pangestiet al, 2015;Friman et al, 2020a). Here, we found an overall stronger aphid-suppressive effect of the AHL-mutant than the AHL-producing strain.…”

Shoot and root insect herbivory change the plant rhizosphere microbiome and affects cabbage–insect interactions through plant–soil feedback

“…Root herbivory by D. radicum together with Pseudomonas simiae inoculation of the plants during the conditioning phase restored plant biomass to a certain degree in the feedback phase. Although this PGPR strain is usually considered a beneficial rhizobacterium when applied to plants, including Brassica oleracea (Friman et al, 2021a), our results suggest that this beneficial effect may not persist through PSF. Notably, there are reports of rhizobacteria causing effects varying from plant-growth promotion to inhibition, depending on e.g.…”

Plant Growth-Promoting Rhizobacteria Enhance Defense of Strawberry Plants Against Spider Mites

“…Below-ground beneficial micro-organisms may affect the performance of above-ground herbivores through plant-mediated mechanisms that may involve changes in plant physiology including enhancement of the plant’s nutritional state and/or induction of systemic resistance (ISR). The latter often results involves the production of secondary plant metabolites ( Dean et al, 2009 ; Hoffmann et al, 2009 ; Kempel et al, 2009 ; Khaitov et al, 2015 ; Ruiu, 2020 ; Friman et al, 2021a ). There exists ample evidence documenting that below-ground interactions with beneficial micro-organisms enhance nutrition and growth of strawberry plants (e.g., Pırlak and Köse, 2009 ; Todeschini et al, 2018 ; Andrade et al, 2019 ); however, the effects of these belowground interactions on life history performance and population dynamics of the cosmopolitan and most serious herbivorous pest of aboveground strawberry plant tissue, T. urticae , have not yet been studied.…”

“…Beneficial below-ground microorganisms may influence the performance of herbivores via two major functional pathways, that is, enhancement of nutrition promoting plant growth and development, which in turn may favor the herbivores, or induced systemic resistance (ISR), which may disfavor the herbivores, or the combination thereof ( Kempel et al, 2009 ; Pineda et al, 2010 ; Gamalero and Glick, 2011 ; Friman et al, 2021b ). Many studies of above-belowground interactions showed that beneficial soil microorganisms such as free-living rhizobacteria can induce systemic resistance in above-ground plant parts and enhance the level of protection against herbivorous attackers ( Zehnder et al, 1997 ; Koricheva et al, 2009 ; Khoshfarman-Borji et al, 2020 ; Ruiu, 2020 ; Friman et al, 2021a ). Regarding interaction between the three species of rhizobacteria used in our study and aboveground herbivores, nothing has been known for P. brassicacearum (Pb).…”

“…During the last two decades, research on below-aboveground interactions has immensely intensified and many studies have focused on effects that cascade up and down between the communities of both subsystems ( Van der Putten et al, 2001 ; Pineda et al, 2010 ; Hoffmann et al, 2011a , b ; Friman et al, 2021b ). Plant-mediated below-aboveground interactions involving micro-organisms of the rhizosphere may occur between plant-associated and/or free-living microorganisms ( Bezemer and van Dam, 2005 ; Coskun et al, 2017 ; Dellagi et al, 2020 ), between micro-organisms and herbivores ( Hoffmann et al, 2009 ; Patiño-Ruiz and Schausberger, 2014 ; Disi et al, 2019 ; Friman et al, 2021a ) and, in turn, between micro-organisms and the herbivores’ natural enemies ( Hoffmann et al, 2011a , b ; Pineda et al, 2013 ; Gadhave et al, 2016 ). The rhizosphere microbial community may consist of a huge diversity of pathogenic, neutral and/or mutualistic micro-organisms.…”