Interaction between endophytic Proteobacteria strains and Serendipita indica enhances biocontrol activity against fungal pathogens

Abstract

Aims Plants host communities of fungal and bacterial endophytes, establishing a complex network of multipartite interactions, but the mechanisms whereby they interact are poorly understood. Some fungi, such as the beneficial mycorrhiza-like fungus Serendipita (=Piriformospora) indica, can be helped by bacteria for establishment, survival and colonization. Although this fungus harbors a Rhizobium as an endofungal bacterium, we hypothesized that other bacteria might also establish associations with the fungus and combining S. indica with bacteria might enhance plant growth and health. Methods The interactions among S. indica and four e n d o p h y t i c P r o t e o b a c t e r i a b e l o n g i n g t o Methylobacterium, Tardiphaga, Rhodanobacter and Trinickia spp. were characterized in vitro and for their effect on tomato growth and biocontrol of Fusarium oxysporum and Rhizoctonia solani. Possible mechanisms behind these interactions were described based on genome and microscopic analyses, using fungal and bacterial strains tagged with fluorescent markers. Results All bacteria stimulated S. indica growth in vitro. Moreover, several of the bacteria stimulated growth of tomato plants, but co-inoculations with S. indica and bacteria did not perform better than single inoculations. Contrarily, combinations of S. indica and bacteria significantly reduced disease progression of fungal pathogens. These microbes seem to cooperate in the process of root colonization for instance by increasing fungal sporulation and hyphae expansion, showing multipartite interaction between microbes and plants. Interestingly, the strain of Trinickia internally colonizes spores of S. indica as an endofungal bacterium during in vitro-co-culturing, suggesting further that the fungus might acquire formerly unrecognized genera of bacteria and genome analysis of the bacteria revealed many genes potentially involved in fungal and plant growth stimulation, biocontrol and root colonization, highlighting putative mechanisms of plantfungal-bacterial interaction. Conclusions Our study represents an important step towards unraveling the complex interactions among plants, S. indica, endophytic bacteria and fungal pathogens, and indicates that adding bacteria to fungal inoculum could have a remarkable impact on the plantS. indica symbiosis.

Presence of the Weakly Pathogenic Fusarium poae in the Fusarium Head Blight Disease Complex Hampers Biocontrol and Chemical Control of the Virulent Fusarium graminearum Pathogen

“…When a plant is infected by a pathogen, a complex interaction between plant, pathogen and the residing microbial community starts (e.g., del Barrio-Duque et al, 2020 ). The outcome of this interaction is then typically determined by the mutual interplay of plant, microbial and plant pathogen-derived signals and pathways.…”

miCROPe 2019 – emerging research priorities towards microbe-assisted crop production

“…For instance, del Barrio Duque et al . ( 2019 , 2020 ) revealed synergistic effects between fungal and bacterial strains to promote plant growth and to suppress root pathogens. In particular, the combination between Serendipita indica , a well-known plant beneficial fungus, and Mycolicibacterium strains, all isolated from plants, enhanced the growth-promoting effect of the fungus when tested on tomato plants.…”

The Free-Living Stage Growth Conditions of the Endophytic Fungus Serendipita indica May Regulate Its Potential as Plant Growth Promoting Microbe

“…The lack of these studies, especially the lack of field trials, limits our study’s contribution to the development of efficient S. indica -based PGPM, either S. indica alone or in consortium with bacteria. Indeed, studies demonstrating interactions between S. indica and soil bacteria are accumulating in recent years: (i) S. indica -bacteria interactions can benefit ( Jiang et al, 2018 ; Alabid et al, 2019 ) or affect ( Leyva-Rojas et al, 2020 ) S. indica ’s growth during the free-living stage; and (ii) S. indica -bacteria interactions have been shown to enhance crop production ( Guo et al, 2017 ; del Barrio-Duque et al, 2019 ; Dabral et al, 2020 ) and resistance to phytopathogens ( del Barrio-Duque et al, 2019 , 2020 ) and salt stress ( Heidarianpour et al, 2020 ). This recent trend further reinforces the need for synergy between fungal and bacterial endophyte research efforts ( Le Cocq et al, 2017 ), especially taking into consideration the bacteria intimately associated with S. indica ( Sharma et al, 2008 ; Guo et al, 2017 ; del Barrio-Duque et al, 2020 ).…”