Unveiling the Dynamics of Plant-Microbe Interactions: From Phyllosphere to Rhizosphere and Beyond

Abstract

Bacterial leaf spot (BLS) is a recurring agricultural issue affecting tomatoes and peppers around the globe. Traditionally, Xanthomonas perforans was considered the primary pathogen of tomatoes, while X. euvesicatoria was associated with peppers. However, recent studies have indicated a notable shift towards the dominance of X. perforans in pepper plants, signifying a potential expansion of its host range. Our research sought to delve into the diversity of the endemic bacterial spot pathogen Xanthomonas and uncover the factors driving microbial diversity and pathogen populations. Through a culture-independent approach, we achieved a higher-resolution method for examining pathogen populations and survey of tomato fields indicated that all eight lineages of X. perforans found in the samples collected around the globe are also circulating throughout southeastern United States. Co-occurrence of multiple lineages was common among the fields. Furthermore, we employed modeling to analyze Xanthomonas populations and disease severity alongside climate variables, emphasizing the critical role of meteorological conditions in shaping disease outcomes. This knowledge is paramount for developing precise predictive models and early warning systems to mitigate disease outbreaks. In addition to studying pathogenic strains, our research delved into the diversity and evolution of nonpathogenic Xanthomonas strains, often found alongside their pathogenic counterparts in the phyllosphere. This investigation focused on co-occurrence patterns and phylogenetic relationships to identify genomic traits that underlie their ecological strategies, spanning from commensal to weakly pathogenic to fully pathogenic lifestyles. Our results suggested that the distinction between these lifestyles in Xanthomonas is not solely defined by the type III secretion system and effectors. We also identified distinct sets of cell-wall degrading enzymes that differentiate pathogenic from commensal or weakly pathogenic lifestyles. In contrast, pathogens rely on the type III secretion system and effectors to evade host defense responses, whereas commensal Xanthomonas harbor genes that promote stress tolerance rather than avoidance, especially in the absence of the type III secretion system. The intricate relationships between plants and their associated microbiota, spanning bacteria, fungi, viruses, and protists, have evolved to form the plant microbiota over millions of years. Within this diverse community, only a subset of microbes act as pathogens, impacting specific hosts. These plant-associated microbes can be found in various niches, including the rhizosphere, phyllosphere, or endosphere, and play essential roles in nutrient acquisition, adaptation to stressors, and overall plant growth. Comprehensive comprehension of these complex plant-microbe interactions is vital for the effective management of plant diseases and the stability of ecosystems. For example, the phyllosphere microbiome, comprising microorganisms residing on the aboveground parts of plants, significantly influences plant health, productivity, and resilience to various biotic and abiotic stressors. Unlike the relatively stable rhizosphere, the phyllosphere represents a dynamic environment characterized by rapid environmental fluctuations, including temperature, humidity, UV light, and limited nutrient availability. In a world characterized by global changes such as shifts in climate and land use, these fluctuations significantly impact ecosystems and plant-microbe interactions. To shed light on these influences, we examined how elevated tropospheric ozone (O3) and Xanthomonas perforans infection impact disease outcomes and associated microbiomes in pepper plants. While pathogen infection significantly influenced the microbiome of susceptible cultivars, O3 stress exacerbated disease severity in resistant cultivars. This alteration in microbial community interactions in both biotic and abiotic stress suggests that microbiomes play a pivotal role in plant-pathogen responses under climate change. Besides phyllosphere, we also utilized a culture-independent technique to scrutinize the influence of long-term crop management and fertility on soil microbial communities. Our study involved the analysis of nine cropping systems, each employing various fertilization methods and legume cover crops. Our results indicated that long-term balanced nitrogen (N) addition significantly influences fungal communities but has a lesser impact on bacterial communities. Lower soil pH was found to significantly affect bacterial communities, while fungal communities exhibited greater resilience to changes in pH levels. While applying chemical fertilizers has previously been associated with reduced microbial diversity and richness, our research showed relative stability in soil bacterial diversity and richness under standard fertilizer treatment. This stability implies that microbial communities can adapt to prolonged fertilizer use. Overall, our research provided valuable insights into the diversity, evolution, and ecology of BLS Xanthomonas strains and the importance of plant-microbe interactions in plant disease management and adaptation to climate change. These findings contribute to developing sustainable agricultural practices that enhance plant health, productivity, and resilience in the face of evolving pathogens and changing climates.