Diseased-induced multifaceted variations in community assembly and functions of plant-associated microbiomes

Abstract

Plant-associated microorganisms are believed to be part of the so-called extended plant phenotypes, affecting plant growth and health. Understanding how plant-associated microorganisms respond to pathogen invasion is crucial to controlling plant diseases through microbiome manipulation. In this study, healthy and diseased (bacterial wilt disease, BWD) tomato (Solanum lycopersicum L.) plants were harvested, and variations in the rhizosphere and root endosphere microbial communities were subsequently investigated using amplicon and shotgun metagenome sequencing. BWD led to a significant increase in rhizosphere bacterial diversity in the rhizosphere but reduced bacterial diversity in the root endosphere. The ecological null model indicated that BWD enhanced the bacterial deterministic processes in both the rhizosphere and root endosphere. Network analysis showed that microbial co-occurrence complexity was increased in BWD-infected plants. Moreover, higher universal ecological dynamics of microbial communities were observed in the diseased rhizosphere. Metagenomic analysis revealed the enrichment of more functional gene pathways in the infected rhizosphere. More importantly, when tomato plants were infected with BWD, some plant-harmful pathways such as quorum sensing were significantly enriched, while some plant-beneficial pathways such as streptomycin biosynthesis were depleted. These findings broaden the understanding of plant–microbiome interactions and provide new clues to the underlying mechanism behind the interaction between the plant microbiome and BWD.

Deciphering key factors in pathogen-suppressive microbiome assembly in the rhizosphere

“…Studies have revealed the characteristics of suppressive soils, specifically the underlying mechanism of “take-all decline” ( Cook et al., 1995 ); and they discovered the disease decline is the result of systemic acquired resistance gained through defensive microbe recruitment ( Liu et al., 2021 ). The phenomenon has not been considered from this paradigm in the beginning; however, current studies have indicated pathogen-induced microbiome recruitment and its remarkable effect on defensive microbiome assembly ( Carrión et al., 2019 ; Kuang et al., 2023 ). The recruited microbes will induce systematic resistance in plants, while they may also directly confront pathogens in the system ( Figure 1 ) through the secretion of secondary metabolites or competition for nutrients and space ( Getzke et al., 2023 ).…”

“…The rhizosphere is generally colonized by various microbes and the microbiome composition differs greatly between diseased and healthy plants ( Kuang et al., 2023 ). This implies that pathogens can be used to shape the microbiome structure in the rhizosphere.…”

“…This implies that pathogens can be used to shape the microbiome structure in the rhizosphere. As discussed previously, pathogen-induced microbial assembly is an emerging strategy that results in a distinct microbial assembly that can suppress pathogen infection ( Carrión et al., 2019 ; Kuang et al., 2023 ). An early warning role discovered in this phenomenon could be used to trigger plant immunity activation that might be evaded or suppressed by pathogens during infection.…”

“…Hence, the rhizosphere microbiome population structure, composition, and function offer valuable knowledge of the underlying interactions between plants and their associated microorganisms that cause pathogen suppression. Scientists argue whether changes in the microbiome structures are causal factors leading to diseases ( Li et al., 2023a ) or if they are merely consequences of diseases ( Kuang et al., 2023 ). Yet more investigations are needed to determine this phenomenon, numerous studies have demonstrated that the enhanced pathogen suppression in the rhizosphere is the result of changes in microbiome composition ( Carrión et al., 2019 ; Chen et al., 2020a ; Chen et al., 2022 ; Hong et al., 2023 ; Khatri et al., 2023b ; Wang et al., 2023c ; Zhu et al., 2023 ).…”

Insight into the soil bacterial community succession of Nicotiana benthamiana in response to Tobacco mosaic virus

“…Many studies have focused on comparing the differences in soil microbial communities between diseased and healthy plants ( Liang et al, 2021 ; Hossain et al, 2022 ; Tang et al, 2023 ). However, there is still limited research on the response mechanism of soil bacterial communities and plants to the pathogen attack ( Lu et al, 2022 ; Kuang et al, 2023 ). In this study, we explored the succession of soil bacterial communities of the healthy and diseased plants after N. benthamiana inoculated with TMV to indicate the role of soil bacterial communities in controlling TMV and the potential beneficial microbes.…”