Cell wall degrading enzymes originating from Rhizoctonia solani increase sugar beet root damage in the presence of Leuconostoc mesenteroides

Authors: Majumdar, Raj; Strausbaugh, Carl; Galewski, Paul; MINOCHA, RAKESH - Us Forest Service (FS); Rogers, Christopher

Submitted to: International Journal of Molecular Sciences
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/21/2022
Publication Date: 1/25/2022
Citation: Majumdar, R., Strausbaugh, C.A., Galewski, P.J., Minocha, R., Rogers, C.W. 2022. Cell wall degrading enzymes originating from Rhizoctonia solani increase sugar beet root damage in the presence of Leuconostoc mesenteroides. International Journal of Molecular Sciences. 23(3). Article 1366. https://doi.org/10.3390/ijms23031366.
DOI: https://doi.org/10.3390/ijms23031366

Interpretive Summary: Sugar beet is highly susceptible to the soil borne fungus Rhizoctonia solani (R. solani) and this fungal pathogen causes root rot and reduces sugar yield. Root rot is greatly increased if this fungus is in close association with Leuconostoc mesenteroides (L. mesenteroides), a free-living bacterium in the soil. Interestingly L. mesenteroides in absence of R. solani has minimum effect on sugar beet root rot. The current study was undertaken to identify potential R. solani derived factors that contribute to increased root rot. Using a multidisciplinary approach, we demonstrate that R. solani derived specific plant cell wall degrading enzymes are the key players that increase root rot in the presence of L. mesenteroides. The knowledge obtained from this study will help in designing novel mitigation strategies to minimize sugar beet root rot and maximize sugar yield caused by both these fungal and bacterial pathogens.

Technical Abstract: Sugar beet crown and root rot caused by Rhizoctonia solani is a major yield constraint. Root rot is highly increased when R. solani and Leuconostoc mesenteroides co-infect roots. We hypothesized that the absence of plant cell wall degrading enzymes in L. mesenteroides and their supply by R. solani during close contact, causes increased damage. In planta root inoculation with or without cell wall degrading enzymes showed greater rot when L. mesenteroides was combined with cellulase (49 mm rot), polygalacturonase (48 mm), and pectin lyase (35 mm) versus these enzymes (0–11 mm), R. solani (13 mm), and L. mesenteroides (22 mm) individually. Carbohydrate analysis revealed increase in simpler carbohydrates namely glucose + galactose, and fructose in the infected roots versus mock control, possibly due to the degradation of complex cell wall carbohydrates. Expression of R. solani cellulase, polygalacturonase, and pectin lyase genes during root infection corroborated well with the enzyme data. Global mRNAseq analysis identified candidate genes and highly co-expressed gene clusters (in all 3 organisms) that might be critical in host plant defense and pathogenesis. Future targeting of R. solani cell wall degrading enzymes could be an effective strategy to mitigate root damage during interaction with L. mesenteroides.