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Plants secrete a complex array of organic compounds, constituting about a third of their photosynthetic products, into the surrounding soil. As a result, concentration gradients are established from the roots into the bulk soil, known as the rhizosphere. Soil microbes benefit from these root exudates for their survival and propagation, and consequently, the composition of the rhizosphere microbial community follows the gradient of available compounds, a phenomenon oftentimes referred to as the rhizosphere effect. However, the fine-grained changes in the microbial community along this soil-root gradient have not been well described. Yet such insights would enable us to underpin the ecological rules underlying root microbial community assembly. Therefore, here we harvested the roots of individual Arabidopsis thaliana plants grown in three different natural soils at high-resolution, such that we could interrogate community assembly and predict microbial growth rate across consecutive, fine-grained, rhizosphere ‘compartments’. We found that the strength of the rhizosphere effect depends on root proximity and that microbial communities closer to the roots harbour related microbes. Closer to the roots, microbial community assembly became less random and more driven by selection-based processes. Intriguingly, we observed priority effects, where related microbes that arrive first are more likely to establish, and that microbes might use different ecological growth strategies to colonise the rhizosphere. All effects appeared to be independent from starting conditions as microbial community composition converged on the root despite different soil ‘microbial seed banks’. Together, our results provide a high-resolution view of the microbiome changes across the soil-root gradient.

Insect herbivores are amongst the most destructive plant pests, damaging both naturally occurring and domesticated plants. As sessile organisms, plants make use of structural and chemical barriers to counteract herbivores. However, over 75% of herbivorous insect species are well adapted to their host’s defenses and these specialists are generally difficult to ward off. By actively antagonizing the number of insect eggs deposited on plants, future damage by the herbivore’s offspring can be limited. Therefore, it is important to understand which plant traits influence attractiveness for oviposition, especially for specialist insects that are well adapted to their host plants. In this study, we investigated the oviposition preference of Pieris butterflies (Lepidoptera: Pieridae) by offering them the choice between 350 different naturally occurring Arabidopsis accessions. Using a genome-wide association study of the oviposition data and subsequent fine mapping with full genome sequences of 164 accessions, we identified WRKY42 and AOC1 as candidate genes that are associated with the oviposition preference observed for Pieris butterflies. Host plant choice assays with Arabidopsis genotypes impaired in WRKY42 or AOC1 function confirmed a clear role for WRKY42 in oviposition preference of female Pieris butterflies, while for AOC1 the effect was mild. In contrast, WRKY42-impaired plants, which were preferred for oviposition by butterflies, negatively impacted offspring performance. These findings exemplify that plant genotype can have opposite effects on oviposition preference and caterpillar performance. This knowledge can be used for breeding trap crops or crops that are unattractive for oviposition by pest insects.

Volatile compounds (VCs) of Trichoderma fungi trigger induced systemic resistance (ISR) in Arabidopsis that is effective against a broad spectrum of pathogens. The root-specific transcription factor MYB72 is an early regulator of ISR and also controls the activation of iron-deficiency responses. Nitric oxide (NO) is involved in the regulation of MYB72-dependent iron-deficiency responses in Arabidopsis roots, but the role of NO in the regulation of MYB72 and ISR by Trichoderma VCs remains unexplored. Using in vitro bioassays, we applied Trichoderma VCs to Arabidopsis seedlings. Plant perception of Trichoderma VCs triggered a burst of NO in Arabidopsis roots. By suppressing this burst using an NO scavenger, we show the involvement of NO in Trichoderma VCs-mediated regulation of MYB72 expression. Using an NO scavenger and the Arabidopsis lines myb72 and nia1nia2 in in planta bioassays, we demonstrate that NO signalling is required in the roots for activation of Trichoderma VCs-mediated ISR against the leaf pathogen Botrytis cinerea. Analysis of the defence-related genes PR1 and PDF1.2 points to the involvement of root NO in priming leaves for enhanced defence. Our results support a key role of root NO signalling in the regulation of MYB72 expression during the activation of ISR by Trichoderma VCs.

One century after the first report of Dutch elm disease (DED), there is still no practical solution for this problem threatening European and American elms (Ulmus spp.). The long breeding cycles needed to select resistant genotypes and the lack of efficient treatments keep disease incidence at high levels. In this work, the expression of defense-related genes to the causal agent of DED, Ophiostoma novo-ulmi Brasier, was analyzed in in vitro clonal plantlets from two DED-resistant and two DED-susceptible Ulmus minor Mill. trees. In addition, the effect of the inoculation of an endophytic pink-pigmented yeast (Cystobasidium sp.) on the plant's defense system was tested both individually and in combination with O. novo-ulmi. The multifactorial nature of the resistance to DED was confirmed, as no common molecular response was found in the two resistant genotypes. However, the in vitro experimental system allowed discrimination of the susceptible from the resistant genotypes, showing higher levels of oxidative damage and phenolic compounds in the susceptible genotypes after pathogen inoculation. Inoculation of the endophyte before O. novo-ulmi attenuated the plant molecular response induced by the pathogen and moderated oxidative stress levels. Niche competition, endophyte-pathogen antagonism and molecular crosstalk between the host and the endophyte are discussed as possible mechanisms of stress reduction. In sum, our results confirm the complex and heterogeneous nature of DED resistance mechanisms and highlight the possibility of using certain endophytic yeasts as biological tools to improve tree resilience against biotic stress.

Volatile compounds (VCs) of Trichoderma fungi trigger an induced systemic resistance (ISR) in Arabidopsis that is effective against a broad spectrum of pathogens. The root-specific transcription factor MYB72 is an early regulator of ISR and also controls the activation of iron deficiency responses. Nitric oxide (NO) is involved in the regulation of MYB72-dependent iron deficiency responses in Arabidopsis roots, but the role of NO in the regulation of MYB72 and ISR by Trichoderma VCs remains unexplored. Using in vitro bioassays, Trichoderma VCs were applied to Arabidopsis seedlings. Plant perception of Trichoderma VCs triggered a burst of NO in Arabidopsis roots. By suppressing this burst using a NO scavenger, we show the involvement of NO in Trichoderma VCs-mediated regulation of MYB72. Using a NO scavenger and the Arabidopsis lines myb72 and nia1nia2 in in planta bioassays, we demonstrate that NO-signalling is required in the roots for the activation of Trichoderma VCs-mediated ISR against the leaf pathogen Botrytis cinerea. Analysis of the defence-related genes PR1 and PDF1.2 point to the involvement of root NO in priming leaves for enhanced defence. Our results support a key role of root NO-signalling in the regulation of MYB72 during the activation of ISR by Trichoderma VCs.