Xanthomonas infection and ozone stress distinctly influence the microbial community structure and interactions in the pepper phyllosphere

Abstract

While the physiological and transcriptional response of the host to biotic and abiotic stresses have been intensely studied, little is known about the resilience of associated microbiomes and their contribution towards tolerance or response to these stresses. We evaluated the impact of elevated tropospheric ozone (O3), individually and in combination with Xanthomonas perforans infection, under open-top chamber field conditions on overall disease outcome on resistant and susceptible pepper cultivars, and their associated microbiome structure, function, and interaction network across the growing season. Pathogen infection resulted in a distinct microbial community structure and functions on the susceptible cultivar, while concurrent O3 stress did not further alter the community structure, and function. However, O3 stress exacerbated the disease severity on resistant cultivar. This altered diseased severity was accompanied by enhanced heterogeneity in associated Xanthomonas population counts, although no significant shift in overall microbiota density, microbial community structure, and function was evident. Microbial co-occurrence networks under simultaneous O3 stress and pathogen challenge indicated a shift in the most influential taxa and a less connected network, which may reflect the altered stability of interactions among community members. Increased disease severity on resistant cultivar may be explained by such altered microbial co-occurrence network, indicating the altered microbiome-associated prophylactic shield against pathogens under elevated O3. Our findings demonstrate that microbial communities respond distinctly to individual and simultaneous stressors, in this case, O3 stress and pathogen infection, and can play a significant role in predicting how plant-pathogen interactions would change in the face of climate change.

Within-host adaptation of a foliar pathogen,Xanthomonas, on pepper in presence of quantitative resistance and ozone stress

“…1a,b) and recorded disease severity levels twice during the season. As previously noted, elevated O3 did not influence disease severity levels on the susceptible cultivar (Bhandari et al, 2023). However, under elevated O3 levels, the resistant cultivar showed significantly higher disease severity scores with an average increase of 12% during mid-season and 2% during end-season compared to an ambient environment.…”

“…While the absolute abundance of Xanthomonas could not solely explain this difference (Bhandari et al, 2023), we investigated whether the amount of genetic variation available for selection to act on differed across environments and whether adaptation to the new environment was driven by new alleles of large effect that could be linked to the phenotype. Presence of mixed pathogen population and maintenance of heterogeneity in response to stressors has been referred to as a mechanism of rapid evolution resulting in higher pathogen fitness (Hiramatsu et al, 2001;Balaban et al, 2004;Aertsen & Michiels 2005;Longo & Hasty, 2006;Dhar & McKinney, 2007;Lidstrom & Konopka, 2010;Schröter & Dersch, 2019;Caballero-Huertas et al, 2023).…”

“…However, under elevated O3 levels, the resistant cultivar showed significantly higher disease severity scores with an average increase of 12% during mid-season and 2% during end-season compared to an ambient environment. This increase was accompanied by high variation in disease severity, ranging from 2-38% during mid-season and from 0-8% during the end-season (Bhandari et al, 2023) (Fig. 1c).…”

“…10 Next, we looked whether genetic differentiation in the pathogen population may account for higher disease severity values seen under elevated O3 on the resistant cultivar since the absolute abundance of Xanthomonas could not explain the observation (Fig. 1c, Bhandari et al, 2023).…”

Verlagen van de risico’s voor het optreden van bacteriële ziekten in teelten onder glas

“…Micro-organismen, die fylosfeer koloniseren, hebben verschillende functies, o.a. bescherming van de plant tegen pathogenen (Stone et al, 2018;Ehau-Taumaunu et al, 2022;Bhandari et al, 2023). Fylosfeer micro-organismen gebruiken verschillende mechanismen om plant te beschermen tegen pathogenen, zoals o.a.…”