Xylella fastidiosa and Drought Stress in Olive Trees: A Complex Relationship Mediated by Soluble Sugars

SIMPLE SUMMARY: Carbohydrates play important roles in tolerance to both biotic and abiotic stressors. Xylella fastidiosa, the causal agent of “Olive Quick Decline Syndrome”, is a quarantine pathogen that induces drought stress in the host, aggravated by eventual water shortage, which is a frequent environmental condition in Mediterranean olive groves. At present, the resistance mechanisms shown by few resistant olive cultivars (e.g., cv Leccino) are not completely known; therefore, the aim of this research is to understand whether sugar metabolism is involved in the cross-talk mechanisms of biotic and abiotic responses. The results show that drought stress response induces effects beneficial to resistance of Xylella fastidiosa in cv Leccino. In the current context of global climate change, this study supports the importance of investigating the complex drought–disease interaction to detect resistance traits and thus find ways to counter the threat of this pathogen in the future. ABSTRACT: Xylella fastidiosa (Xf) subsp. pauca “De Donno” is the etiological agent of “Olive Quick Decline Syndrome” (OQDS) on olive trees (Olea europaea L.); the presence of the bacterium causes xylem vessel occlusions inducing a drought stress and the development of leaf scorch symptoms, which may be worsened by water shortage in summer. In order to evaluate how the two stress factors overlap each other, the carbohydrate content and the expression patterns of genes related to carbohydrate metabolism have been evaluated in two olive cvs trees (Cellina di Nardò, susceptible to Xf, and Leccino, resistant to Xf) reporting transcriptional dynamics elicited by Xf infection, drought, or combined stress (drought/Xf). In the Xf-susceptible Cellina di Nardò plants, Xf and its combination with drought significantly decrease total sugars compared to control (−27.0% and −25.7%, respectively). In contrast, the Xf-resistant Leccino plants show a more limited reduction in sugar content in Xf-positive conditions (−20.1%) and combined stresses (−11.1%). Furthermore, while the amount of glucose decreases significantly in stressed Cellina di Nardò plants (≈18%), an increase was observed in Leccino plants under drought/Xf combined stresses (+11.2%). An opposite behavior among cvs was also observed for sucrose, as an accumulation of the disaccharide was recorded in stressed Leccino plants (≈37%). The different response to combined stress by Xf-resistant plants was confirmed considering genes coding for the sucrose or monosaccharide transporter (OeSUT1, OeMST2), the cell wall or vacuolar invertase (OeINV-CW, OeINV-V), the granule-bound starch synthase I (OeGBSSI) and sucrose synthase (OeSUSY), with a higher expression than at least one single stress (e.g., ≈1-fold higher or more than Xf for OeMST2, OeINV-CW, OeINV-V, OeGBSSI). It is probable that the pathways involved in drought stress response induce positive effects useful for pathogen resistance in cv Leccino, confirming the importance of investigating the mechanisms of cross-talk of biotic and abiotic responses.