Activation of the SA-Associated Plant Defense Pathway Alters the Composition of Soil Bacterial Communities

Abstract

Background and aimsMany plant species grow better in sterilized than in live soil. Foliar application of SA mitigates this negative effect of live soil on the growth of the plant Jacobaea vulgaris. To examine what causes the positive effect of SA application on plant growth in live soils, we analyzed the effects of SA application on the composition of active rhizosphere bacteria in the live soil. Methods We studied this over four consecutive plant cycles (generations), using mRNA sequencing of the microbial communities in the rhizosphere of J. vulgaris. ResultsOur study shows that the composition of the rhizosphere bacterial communities of J. vulgaris greatly differed among generations. Application of SA resulted in both increases and decreases in a number of active bacterial genera in the rhizosphere soil, but the genera that were affected by the treatment differed among generations. In the first generation, there were no genera that were significantly affected by the SA treatment, indicating that induction of the SA defense pathway in plants does not lead to immediate changes in the soil microbial community. 89 species out of the total 270 (32.4%) were present in all generations in all soils of SA-treated and control plants suggesting that these make up the “core” microbiome. On average in each generation, 72.9% of all genera were present in both soils. Application of SA to plants significantly up-regulated genera of Caballeronia, unclassified Cytophagaceae, Crinalium and Candidatus Thermofonsia Clade 2, and down-regulated genera of Thermomicrobiales, unclassified Rhodobacterales, Paracoccus and Flavihumibacter. While the functions of many of these bacteria are poorly understood, bacteria of the genus Caballeronia play an important role in fixing nitrogen and promoting plant growth, and hence this suggests that activation of the SA signaling pathway in J. vulgaris plants may select for bacterial genera that are beneficial to the plant. ConclusionsOverall, our study shows that aboveground activation of defenses in the plant affects soil microbial communities and, as soil microbes can greatly influence plant performance, this implies that induction of plant defenses can lead to complex above-belowground feedbacks. Further studies should examine how activation of the SA signaling pathway in the plant changes the functional genes of the rhizosphere soil bacterial community.

Belowground responses of bacterial communities to foliar SA application over four plant generations

“…Previous studies showed that inoculation of a sterilized soil with natural, live soil reduced plant growth in comparison with that in sterilized soil for the plant species Jacobaea vulgaris (Joosten et al 2009;Kos et al 2015). Interestingly, applying SA to the leaves mitigated these negative effects (Jing et al 2021). This implies that activation of SAinduced resistance may potentially suppress microbial pathogens present in live soil.…”

“…The current study focused on the effect of foliar SA application on the composition of the bacterial community in the rhizosphere in the inoculated soil. The effects of foliar application of SA on plant growth in the four generations were described elsewhere (Jing et al 2021). A summary of the effects of foliar SA application on the growth of J. vulgaris are shown in Fig.…”