In Planta Transcriptomics of <i>Xanthomonas albilineans</i> Reveals Early Adaptations to the Nutrient-Limited Xylem Environment of Sugarcane

<i>Xanthomonas albilineans</i> causes leaf scald disease in sugarcane, leading to white streaks on leaves, stunted growth, and potentially plant death. With the smallest genome in the genus, its compact size likely reflects adaptation to a specialized lifestyle. Here, we present the first in planta transcriptome of <i>X. albilineans</i>, obtained 48 hours post-inoculation using dual RNA-Seq-a technically demanding approach due to minimal bacterial load relative to host material. Despite only 0.05% of the more than forty billion sequenced bases corresponding to the bacterial cells, we successfully recovered and analyzed its gene expression. Compared to the transcriptome in vitro, we found that during early infection, the bacteria targets sugarcane-specific cell wall components, facilitating tissue invasion. Notably, transcriptomic data suggest that <i>X. albilineans</i> may utilize a distinct metabolic route for the catabolism of lignin-derived compounds, funneling aromatic intermediates into central metabolism through the protocatechuate pathway. This may represent an adaptation to plant-derived aromatic substrates not previously described in other <i>Xanthomonas</i> species. The upregulation of chemotaxis and motility genes indicates active systemic colonization, while phosphorelay systems enhance environmental adaptation. Bacterial fitness is also supported by production of albicidin and upregulation of type IV secretion system (T4SS) and some T5SS genes, whereas T3SS SPI-1 is inactive during early infection. These findings underscore the bacterium's reliance on specific metabolic genes to degrade sugarcane's recalcitrant wall, thrive in the xylem, and migrate to other tissues. Understanding its genomic arsenal and gene expression in sugarcane provides valuable insights for managing leaf scald disease and mitigating impact on production.