The functional relevance of plant-microbe-insect interactions in a cereal crop system
Final Report Abstract
This project investigated the mechanisms behind microbe-induced resistance against aphids on Barley (Hordeum vulgare), as envoked by Acidovorax radicis N35, under different abiotic and biotic scenarios. We hypothesized that quorum sensing was a driving force in the process, which is in this case mediated by N-acyl homoserine lactone (AHL). To understand the role of AHL in mediating these interactions, the Helmholtz team generated a mutant strain that lacked the production of a AHL, which was then used by both the Technical University of Munich team and the Helmholtz team to perform a series of experiments to test A. radicis effects under variable environmental conditions, as well as under axanic conditions, in which A. radicis could be studied with limited environmental confounding factors. Several climate chamber studies showed that A. radicis had a consistent and reliable negative effect on aphid colony growth on Barley plants. Furthermore, we observed that the effects are rather consistent across biotic (i.e., earthworm presence) and abiotic (i.e., varying CO2, O3, soil water availability, extreme temperature) treatments. Barley cultivar and cultivation conditions, however, strongly influenced microbe-plant-insect interaction, which highlights that it is necessary to consider modulating abiotic and biotic factors in future interaction studies and for successful translation to the field, e.g., in agricultural settings. We aimed to unravel the role of quorum sensing (via AHLs) in microbe-induced resistance in a large experiment, where A. radicis wildtype and the AHL-mutant were inoculated to separate individual plants in a large climate chamber experiment. We expected that AHL knockouts would not be able to generate microbe-induced resistance in the plant, due to the absence of the signalling compound AHL. However, surprisingly, the plants did show induced resistance, with stronger effects caused by the AHL mutant. The rhizosphere microbiome was also modulated by AHL-mutant, but did not play the decisive role for aphid suppression. This suggests that the induced resistance is not solely mediated by AHL, but that different pathways may be involved. However, the strong differences between the two bacterial strains also suggest that AHL may be used by bacteria to avoid or hide from strong defense responses by the plant. This aligns with our observations that the bacterium is generally observable early after inoculation, but then seems to be eradicated by the plant within the following days, which suggests that plants actively eradicate their invaders, while at the same time generating a systemic acquired resistance-like response which makes them better defended against aphids. The AHL-mutant showed increased root colonization compared to the wildtype. This enhanced root colonization might have been responsible for the observed increase in plant aphid suppression upon AHL-mutant inoculation. Although it was surprising that AHL-mutant inoculation increased aphid suppression even stronger than the wildtype, the tendency was consistent across multiple experiments and in soil and axenic cultivation systems. For the analysis of direct and indirect AHL effects, additional AHL-mutants with impaired AHL sensing (knockout of the araR gene) were generated and tested in complementation assays. Synthetic AHL addition as well as A. radicis mutants impaired in AHL sensing showed modulated effects on plant aphid suppression. This suggests a role of AHL molecules themselves and the bacterial self-regulation coupled to quorum sensing. It remains to be investigated, e.g. by transcriptomics, which genes were differentially regulated in the respective AHL-mutants. This would give valuable insights how the impaired AHL synthesis influenced colonization and PGP-related traits important for microbe-plant-insect interaction.
Publications
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Microbial-Mediated Plant Growth Promotion and Pest Suppression Varies Under Climate Change. Frontiers in Plant Science, 11.
Zytynska, Sharon E.; Eicher, Moritz; Rothballer, Michael & Weisser, Wolfgang W.
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Importance of N-Acyl-Homoserine Lactone-Based Quorum Sensing and Quorum Quenching in Pathogen Control and Plant Growth Promotion. Pathogens, 10(12), 1561.
Hartmann, Anton; Klink, Sophia & Rothballer, Michael
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Plant Growth Promotion and Induction of Systemic Tolerance to Drought and Salt Stress of Plants by Quorum Sensing Auto-Inducers of the N-acyl-homoserine Lactone Type: Recent Developments. Frontiers in Plant Science, 12.
Hartmann, Anton; Klink, Sophia & Rothballer, Michael
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Impaired microbial N‐acyl homoserine lactone signalling increases plant resistance to aphids across variable abiotic and biotic environments. Plant, Cell & Environment, 45(10), 3052-3069.
Sanchez‐Mahecha, Oriana; Klink, Sophia; Heinen, Robin; Rothballer, Michael & Zytynska, Sharon
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Part-night exposure to artificial light at night has more detrimental effects on aphid colonies than fully lit nights. Philosophical Transactions of the Royal Society B: Biological Sciences, 378(1892).
Heinen, Robin; Sanchez-Mahecha, Oriana; Martijn, Bezemer T.; Dominoni, Davide M.; Knappe, Claudia; Kollmann, Johannes; Kopatsch, Anton; Pfeiffer, Zoë A.; Schloter, Michael; Sturm, Sarah; Schnitzler, Jörg-Peter; Corina, Vlot A. & Weisser, Wolfgang W.
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Microbe‐induced plant resistance against insect pests depends on timing of inoculation but is consistent across climaticconditions. Functional Ecology, 38(4), 848-860.
Sanchez‐Mahecha, Oriana; Klink, Sophia; Rothballer, Michael; Sturm, Sarah; Weisser, Wolfgang W.; Zytynska, Sharon & Heinen, Robin
