The response strategies of Colletotrichum gloeosporioides s.s. due to the stress caused by biological control agent Bacillus amyloliquefaciens deciphered by transcriptome analyses

Walnut is cultivated all over the world for its precious woody nut and edible oil. Walnut anthracnose caused by Colletotrichum spp. is a disastrous disease in the walnut plantation. In China, this disease is difficult to control. The efficacies of the traditional preventing and controlling measures are inadequate. It causes serious losses every year. In the interaction systems of ‘antagonistic organism-pathogen’, the response mechanisms of the pathogen to the stress of antagonistic organisms were largely unknown. To understand the response mechanisms of walnut anthracnose pathogen, Colletotrichum gloeosporioides sensu stricto (s.s.) TS-09R was treated with Bacillus amyloliquefaciens, and RNAseq gene expression analyses were performed. A total of 610 genes expressed differentially (DEGs). Among these genes, 387 genes were up-regulated and 223 genes were down-regulated. Gene ontology (GO) analysis showed that 409 DEGs involved in the categories of biological process, and cellular component. The KEGG pathway enrichment analysis showed that all up-regulated DEGs were enriched in amino acid metabolism, biosynthesis of other secondary metabolites, and xenobiotics biodegradation and metabolism. Further analyses indicated that C. gloeosporioides s.s. TS-09R up-expressed significantly some DEGs associated with cell membrane synthesis and, or maintaining stabilization, antioxidant and anti-stress to build the cell membrane, maintain the normal physiological function of cells. At the same time, it improved detoxification efficiency and reduced its sensitivity to the exogenous antimicrobial substance (EAS). It also improved the activity of the efflux pump translocating EAS out of the cells, reduced accumulation, and minimized injuries to cells. C. gloeosporioides s.s. TS-09R also up-expressed significantly genes associated with sporulation to promote spore production for survival in adversity. C. gloeosporioides s.s. TS-09R recruited numerous genes to respond to or resist the biocontrol of B. amyloliquefaciens. The response model was a holistic and complex network involving multiple genes and multiple signaling pathways. Additionally, the glutathione-S-transferases (GST) activities of C. gloeosporioides s.s. TS-09R, TS-09 cultured for 5 days and 9 days were calculated, and the GST activity had a similar change trend to the GST-related gene expression. The result indicated that the hypothetical response strategies were reliable. In this paper, we provided new insights into the onset of the interaction system of ‘C. gloeosporioides s.s. – B. amyloliquefaciens’. The results will contribute to exploring comprehensively the mechanism of B. amyloliquefaciens according to the response mechanisms of C. gloeosporioides s.s.