Rhizobacteria-induced priming against Fusarium crown rot and desiccation stress in Sorghum bicolor

Abstract

Untargeted ultra-high performance liquid chromatography-high definition mass spectrometry (UHPLC-HDMS) based metabolomics was applied to elucidate the metabolomic changes in Sorghum bicolor seedlings that attribute to rhizobacteria-induced systemic resistance (ISResistance) against biotic stress (Fusarium pseudograminearum crown rot), rhizobacteria-induced systemic tolerance (ISTolerance) against abiotic stress (desiccation) and rhizobacteria-induced systemic resilience (ISResilience) against combined biotic- and abiotic stress. In order to elucidate the biochemical mechanisms of defence priming in S. bicolor during rhizobacteria-ISResistance the differential metabolic reprogramming in naïve versus Paenibacillus alvei-primed S. bicolor seedlings in response to F. pseudograminearum infection was investigated by applying UHPLC-HDMS based metabolomics. An enhanced defensive response in P. alvei NAS-6G6-primed S. bicolor plants was attributed to an early, enhanced upregulation of phytohormone-, amino acid-, flavonoid-, phenylpropanoid- and lipid metabolism. Secondary metabolites identified as discriminatory biomarkers (some with reported antimicrobial phytoalexin activity), included apigenin, caffeic acid, caffeoylquinate, cinnamic acid, coumaroylshikimate, epicatechin, hesperetin, kaempferol, leucocyanidin, naringenin, neohesperidin and shikimic acid giving rise to a significant reduction in crown rot disease incidence and resultant plant growth promotion. In order to elucidate the biochemical mechanisms of rhizobacteria-induced desiccation stress tolerance in S. bicolor, a large group of new rhizobacterial isolates (isolated from the rhizosphere of seven grass species collected from the Nylsvlei Nature Reserve in South Africa) were screened for their ability to elicit ISTolerance against desiccation stress. The best-performing rhizobacterial isolates (Bacillus methylotrophicus N18, B. safensis A28, Pseudomonas taiwanensis N66 and B. pumilus N52) and one semi-commercial strain (P. alvei NAS-6G6), were subsequently included in an UHPLC-HDMS based metabolomics study. The enhanced desiccation stress tolerance in rhizobacteria-primed S. bicolor seedlings was attributed to augmented (1) antioxidant capacity; (2) growth promotion and root architecture modification as a result of the upregulation of the hormones gibberellic acid, indole acetic acid and cytokinin; (3) activation of ISTolerance through the signalling hormones brassinolides, salicylic acid and jasmonic acid and signaling molecules sphingosine and psychosine; (4) osmoregulation resulting from the production of the osmolytes proline, glutamic acid and choline; (5) production of the epicuticular wax docosanoic acid and (6) 1-aminocyclopropane-1-carboxylate (ACC) deaminase activity and lowered ethylene levels. The enhanced desiccation stress tolerance elicited by P. taiwanensis N66, points to an important role of ACC deaminase activity in rhizobacteria-induced desiccation stress tolerance. In order to elucidate the biochemical mechanisms of defence priming in S. bicolor during rhizobacteria-ISResilience against combined stress, a large group of new rhizobacterial isolates were screened for ISResilience and the best performing isolate (B. velezensis N54) was selected for an UHPLC-HDMS based metabolomics study which investigated the best-performing isolates selected for ISResistance, ISTolerance and ISResilience. This study reports on new findings pertaining to the metabolic changes in S. bicolor seedlings elicited by P. alvei NAS-6G6, P. taiwanensis N66 and B. velezensis N54 and the resultant defensive response against biotic- (F. pseudograminearum crown rot), abiotic-(desiccation) and combined stress. The findings from this work provide novel understanding of rhizobacteria-induced priming and the resultant protection elicited in S. bicolor seedlings upon exposure to biotic-, abiotic- and combined stress.