Complementary effects of biochar, secondary metabolites, and bacteria biocontrol agents rejuvenate ratoon sugarcane traits and stimulate soil fertility

Bacteria biological control agents (BCAs) against diseases and pests are widely deemed a sustainable approach in agriculture. However, the extent to which the multifunctionality of plant secondary metabolites and BC interactions shape soil chemistry (e.g., C and N cycling enzymes) and BCAs communities in complex environments, especially under a cropping system (e.g., ratooning) prone to nutrient depletion, disease, etc., is not well established. Besides, the role metabolites-BCAs-BC interactions play in rejuvenating growth conditions necessary for ratoon sugarcane and suppressing plant pathogens/soil-borne diseases remains unclear. Here, we leveraged high-throughput sequencing and LC–MS/MS analyses to illuminate the regulatory effects of BC and plant secondary metabolites interactions on soil chemistry and BCAs communities. Additionally, we explored the roles metabolites-BCAs-BC interactions play in rejuvenating growth conditions necessary for ratoon sugarcane and suppressing plant pathogens/soil-borne diseases. Our finding revealed a pronounced rejuvenation of sugarcane ratoon traits and edaphic factors under the BC amendment soil, primarily due to the role metabolites-BCAs-BC interactions play in remediating soil fertility and health. We also proved that the BC-amended soils were worthy of enriching essential BCAs communities, including Pseudomonas, Bacillus, Streptomyces, Pantoea, Serratia, Weissella, and Leuconostoc. Abscisic aldehyde had a positive correlation with BCAs genera, including Bacillus, Pseudomonas, Serratia, Pantoea, and Ligilactobacillus. Whereas Pseudomonas, Pseudonocardia, Weissella, Bacillus, and Pantoea responded strongly and positively to jasmonic acid. Additionally, benzoate exhibited a strong positive association with BCAs genera, namely, Pseudomonas, Pseudonocardia, Weissella, Bacillus, Pantoea, and Ligilactobacillus in the different plant tissues. In the rhizosphere zone, BCAs genera such as Pseudomonas and Ligilactobacillus responded strongly to phenyllactic acid. Plant secondary metabolites, including apigenin and naringenin, demonstrated a strong positive relationship with N-cycling enzymes, including urease and phosphatase, respectively. Whereas palmitic acid, jasmonic acid, apiin, and abscisic aldehyde exhibited a significant positive correlation with soil TN, urease, pH, and AP, respectively. BugBase functional analysis confirmed that potentially pathogenic bacterial predicted phenotypes were low in the BC amendment. This work demonstrates how the multifunctionality of plant secondary metabolites-BCAs-BC interactions remediate soil fertility and suppress the presence of pathogens/parasites (e.g., Exserohilum, Aphis gossypii Glover, and Colletotrichum), thereby rejuvenating ratoon sugarcane growth and productivity.