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Xylem cavitation susceptibility and refilling mechanisms in olive trees infected by Xylella fastidiosa.

ABSTRACT: In olive trees, Xylella fastidiosa colonizes xylem vessels and compromises water transport causing the olive quick decline syndrome (OQDS). The loss of hydraulic conductivity could be attributed to vessel occlusions induced both by the bacteria biofilm and by plant responses (tyloses, gums, etc.) that could trigger embolism. The ability of the infected plants to detect embolism and to respond, by activating mechanisms to restore the hydraulic conductivity, can influence the severity of the disease symptomatology. In order to investigate these mechanisms in the X. fastidiosa-resistant olive cultivar Leccino and in the susceptible Cellina di Nardò, sections of healthy olive stems were analysed by laser scanning microscope to calculate the cavitation vulnerability index. Findings indicated that the cultivar Leccino seems to be constitutively less susceptible to cavitation than the susceptible one. Among the vascular refilling mechanisms, starch hydrolysis is a well-known strategy to refill xylem vessels that suffered cavitation and it is characterized by a dense accumulation of starch grains in the xylem parenchima; SEM-EDX analysis of stem cross-sections of infected plants revealed an aggregation of starch grains in the Leccino xylem vessels. These observations could indicate that this cultivar, as well as being anatomically less susceptible to cavitation, it also could be able to activate more efficient refilling mechanisms, restoring vessel's hydraulic conductivity. In order to verify this hypothesis, we analysed the expression levels of some genes belonging to families involved in embolism sensing and refilling mechanisms: aquaporins, sucrose transporters, carbohydrate metabolism and enzymes related to starch breakdown, alpha and beta-amylase. The obtained genes expression patterns suggested that the infected plants of the cultivar Leccino strongly modulates the genes involved in embolism sensing and refilling.

SUBMITTER: Sabella E

PROVIDER: S-EPMC6610111 | biostudies-literature | 2019 Jul

REPOSITORIES: biostudies-literature

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Xylem cavitation susceptibility and refilling mechanisms in olive trees infected by Xylella fastidiosa.

Sabella Erika E Aprile Alessio A Genga Alessandra A Siciliano Tiziana T Nutricati Eliana E Nicolì Francesca F Vergine Marzia M Negro Carmine C De Bellis Luigi L Luvisi Andrea A

Scientific reports 20190703 1

In olive trees, Xylella fastidiosa colonizes xylem vessels and compromises water transport causing the olive quick decline syndrome (OQDS). The loss of hydraulic conductivity could be attributed to vessel occlusions induced both by the bacteria biofilm and by plant responses (tyloses, gums, etc.) that could trigger embolism. The ability of the infected plants to detect embolism and to respond, by activating mechanisms to restore the hydraulic conductivity, can influence the severity of the disea ...[more]

PMID: 31270378

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Project description: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.

Project description:Xylella fastidiosa represents a major threat to important crops worldwide including almond, citrus, grapevine, and olives. Nowadays, there are no efficient control measures for X. fastidiosa, and the use of preventive measures and host resistance represent the most practical disease management strategies. Research on vessel-associated microorganisms is gaining special interest as an innate natural defense of plants to cope against infection by xylem-inhabiting pathogens. The objective of this research has been to characterize, by next-generation sequencing (NGS) analysis, the microbial communities residing in the xylem sap of almond trees affected by almond leaf scorch disease (ALSD) in a recent X. fastidiosa outbreak occurring in Alicante province, Spain. We also determined community composition changes and network associations occurring between xylem-inhabiting microbial communities and X. fastidiosa. For that, a total of 91 trees with or without ALSD symptoms were selected from a total of eight representative orchards located in five municipalities within the X. fastidiosa-demarcated area. X. fastidiosa infection in each tree was verified by quantitative polymerase chain reaction (qPCR) analysis, with 54% of the trees being tested X. fastidiosa-positive. Globally, Xylella (27.4%), Sphingomonas (13.9%), and Hymenobacter (12.7%) were the most abundant bacterial genera, whereas Diplodia (30.18%), a member of the family Didymellaceae (10.7%), and Aureobasidium (9.9%) were the most predominant fungal taxa. Furthermore, principal coordinate analysis (PCoA) of Bray-Curtis and weighted UniFrac distances differentiated almond xylem bacterial communities mainly according to X. fastidiosa infection, in contrast to fungal community structure that was not closely related to the presence of the pathogen. Similar results were obtained when X. fastidiosa reads were removed from the bacterial data set although the effect was less pronounced. Co-occurrence network analysis revealed negative associations among four amplicon sequence variants (ASVs) assigned to X. fastidiosa with different bacterial ASVs belonging to 1174-901-12, Abditibacterium, Sphingomonas, Methylobacterium-Methylorubrum, Modestobacter, Xylophilus, and a non-identified member of the family Solirubrobacteraceae. Determination of the close-fitting associations between xylem-inhabiting microorganisms and X. fastidiosa may help to reveal specific microbial players associated with the suppression of ALSD under high X. fastidiosa inoculum pressure. These identified microorganisms would be good candidates to be tested in planta, to produce almond plants more resilient to X. fastidiosa infection when inoculated by endotherapy, contributing to suppress ALSD.

Dataset Information

Xylem cavitation susceptibility and refilling mechanisms in olive trees infected by Xylella fastidiosa.

Publications

Xylem cavitation susceptibility and refilling mechanisms in olive trees infected by Xylella fastidiosa.

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