Differential transcriptomic landscapes of olive cultivars facing Xylella fastidiosa infection

The bacterium Xylella fastidiosa subsp. pauca (Xfp) is the causal agent of Olive Quick Decline Syndrome (OQDS), a disease characterized by leaf scorch, irregular periderm development, branch desiccation, general growth arrest, and eventual plant death, leading to extensive damage to olive groves (Olea europaea L.) and severely impacting agricultural production in the Apulia region, Italy's leading producer of olive oil. To date, no cure for the disease exists, and most olive germplasm is susceptible, with only a few varieties showing resistance. Among them, the LECCINO cultivar displays resistance to the pathogen, exhibiting little to no symptoms after infection. In contrast, other varieties, such as OLIVA ROSSA, are highly susceptible, while cultivars like DONNA FRANCESCA exhibit an intermediate level of susceptibility. Only limited studies have investigated the genetic basis underlying these differential responses.

Comparative transcriptomic analysis of the above-mentioned olive cultivars revealed distinct and divergent defence strategies. The susceptible OLIVA ROSSA showed a broad but largely ineffective transcriptional reprogramming, including the downregulation of cytoskeleton-related genes. In contrast, the resistant LECCINO displayed a more targeted activation of sulphur assimilation pathways, antioxidant responses, and cell wall-associated proteins, enabling more effective pathogen containment. The cultivar DONNA FRANCESCA exhibited a reduced transcriptional response overall, consistent with its intermediate level of susceptibility. Only 5 of 1,758 differentially expressed genes were shared across all cultivars, highlighting highly cultivar-specific responses and the overall complexity of the host-pathogen interaction. Resistance appears to be associated with a focused and limited transcriptional activation, susceptibility with widespread but ineffective gene reprogramming, and intermediate susceptibility with modest yet efficient transcriptional adjustments.

Each olive cultivar responds to Xfp infection by modulating a distinct set of genes, suggesting that resistance and susceptibility are governed by different molecular mechanisms. This cultivar-specific transcriptional behaviour highlights the complexity of host-pathogen interactions and expanding analyses to additional genotypes could provide further insights into the genetic and molecular bases of these diverse responses.