Comparative transcriptomic profile reveals candidate genes manipulated by type III effectors of Pantoea agglomerans pv. betae leading to gall formation in beet

Abstract

Pantoea agglomerans pv. betae (Pab) induces tumor-like galls in beet and gypsophila, a process mediated by the secretion of effector proteins via Pabs type III secretion system (T3SS). The molecular mechanisms underlying Pab-induced gall formation remain largely unexplored. This study delves into the cellular architecture and transcriptional profile of Pab-mediated galls, comparing host responses to wild-type Pab and a T3SS-inactive mutant, hrcC-. Morphological analysis using scanning electron microscopy and cross-sectional visualization of infected beet leaf tissues revealed that Pab-induced gall-like structures are linked to cell hyperplasia and tissue ruptures, contingent on T3SS activity. Comparative transcriptome analysis of wild-type Pab and hrcC- Pab-infected beet leaves at 12 and 48 hours unveiled significant transcriptional reprogramming, with nearly 2,000 differentially expressed genes at 48 hours post inoculation. Enrichment analyses identified the upregulation of pathways related to signal transduction, defense, carbohydrate metabolism, and cell wall modulation in wild-type Pab-infected leaves compared to controls. Particularly notable was the significant upregulation of numerous genes associated with cell wall loosening by wild-type Pab, suggesting an initial rearrangement of cell wall architecture facilitates gall formation. Furthermore, transcriptome analysis demonstrated that wild-type Pab suppresses the expression of the betalain biosynthetic gene DOPA 4,5-DIOXYGENASE, leading to reduced betalain accumulation in infected tissues compared to the mutant strain. These findings offer fresh insights into the transcriptional and physiological manipulation of host tissue during the early stages of Pab-induced gall formation.