Disease-induced Changes in Plant Microbiome Assembly and Functional Adaptation

Abstract

Background: Plant microbiome is an integral part of the host influencing its growth and health. The increasing evidence indicates that plant rhizosphere may recruit beneficial microbes to suppress soil-borne pathogen, but the ecological mechanisms that govern plant microbiome assembly and functions under disease in both below and aboveground compartments are not fully understood. Here we examined both bacterial and fungal communities from soils (rhizosphere and bulk soil) and multiple plant compartments (e.g. root, stem, and fruit) of chili pepper (Capsicum annuum L.) at two pepper production sites, and explored how Fusarium wilt disease (FWD) affect the assembly, co-occurrence patterns, and ecological functions of plant-associated microbiomes. Results: Our data demonstrated that FWD had less impact on reproductive organ (fruit) than on vegetative organs (root and stem), with the strongest impact in the stem upper epidermis. Fungal intra-kingdom networks presented lower stabilities and their communities were more sensitive to FWD than the bacterial communities. Moreover, the diseased pepper was more susceptible to colonization by other pathogenic fungi, but they may recruit potential beneficial bacteria to facilitate host or offspring survival, and FWD may enhance the ecological importance of fungal taxa in the interkingdom network. Further, metagenomic analysis revealed that several potential protective functional genes encoding detoxify and biofilm formation were significantly enriched in the diseased pepper.Conclusion: Together, these results significantly advance our understanding of pepper microbiome assembly and functions under biotic stress. Our work highlights the diseased plant and the aboveground compartments harbor a potential of beneficial microbiomes and functions that, in concert, can provide potential critical data for harnessing the plant microbiome for sustainable agriculture.

The phyllosphere microbiome shifts toward combating melanose pathogen

“…Microbiome changes have been described across many plant species upon pathogen challenge, such as huanglongbing in citrus [ 25 ], common scab in potato [ 26 ], and crown rot disease in wheat [ 27 ]. Changes in the microbiome that associated with improved or reduced plant performance under stressful conditions [ 28 , 29 ]. These studies emphasized that the microbiome response could play an important role in maintaining plant health.…”

Disentangling leaf-microbiome interactions in Arabidopsis thaliana by network mapping

“…We calculate the degree of each node in a network. To reduce the bias, we statistically identify the hub taxa with the highest degree and closeness centrality [13,37]. Meanwhile, six network indices, including connectivity (Con), closeness (C(u)), betweenness(B(u)), eccentricity (E(u)), eigencentrality (G(u)), and Pagerank (P(u)) are calculated, as described previously [35].…”

“…Most studies on plant microbiomes have focused on rhizosphere microbial communities and their functioning rather than on those of phyllosphere. The phyllosphere microbiomes may play essential but often overlooked roles in nutrient acquisition, abiotic stress tolerance, and disease suppression of plants [13]. Experimental studies have demonstrated that the phyllosphere harbors diverse microbial communities that in uenced ecosystem functioning [14][15][16][17][18][19].…”

Plant–Microbiome Crosstalk: Dawning from Composition and Assembly of Microbial Community to Improvement of Disease Resilience in Plants

“…Molecular interactions between host-derived R and pathogen-oriented Avr proteins activate the second line of defense, known as effector-triggered immunity (ETI). ETI is relatively faster and stronger than PTI, and usually induces localized necrosis of both pathogen and plant cells in the infected area [110,111]. PTI and ETI together constitute the innate immunity system in plants, which enable plants to recognize and resist/combat against invading pathogens.…”

“…Furthermore, pathogens also promote the colonization of other plant-harmful microbes by delivering effector proteins that cease the activities of beneficial microbes in rhizosphere community [136]. Plants and their associated microbiota are evolving simultaneously for millions of years, and this co-association of microbes and plants provides several benefits to plants including nutrient acquisition, fight against abiotic stresses, and disease suppression [111]. Hostlinked communities of beneficial microbes are involved in disease suppression and nutrient mobilization in plants [137,138].…”