NGS transcriptomic analysis uncovers the possible resistance mechanisms of olive to Spilocea oleagina leaf spot infection

Abstract

Spilocea oleagina is a dangerous obligate fungal pathogen of olive, feared in the Mediterranean countries, causing Peacock’s eye or leaf spot infection, which can lead to a serious yield loss of approximately 20% or higher depending on climatic conditions. Coping with this disease is much more problematic for organic farms. To date, knowledge on the genetic control of possible mechanisms of resistance/low susceptibility is quite limited. In this work, comparative transcriptomic analysis (RNA-seq) was conducted in leaf tissues of a low susceptible cultivar Koroneiki and a high susceptible cultivar Nocellara del Belice, both tested in the field using the NaOH test, considering two stages—”zero sign of disease” and “evident sign of infection”. Cultivars showed a very large number of differentially expressed genes (DEGs) in both stages. ‘Koroneiki’ showed an extensive hormonal crosstalk, involving Abscisic acid (ABA) and ethylene synergistically acting with Jasmonate, with early signaling of the disease and remarkable defense responses against Spilocea through the over-expression of many resistance gene analogs or pathogenesis-related (PR) genes: non-specific lipid-transfer genes (nsLTPs), LRR receptor-like serine/threonine-protein kinase genes, GDSL esterase lipase, defensin Ec-AMP-D2-like, pathogenesis-related leaf protein 6-like, Thaumatin-like gene, Mildew resistance Locus O (MLO) gene, glycine-rich protein (GRP), MADS-box genes, STH-21-like, endochitinases, glucan endo-1,3-beta-glucosidases, and finally, many proteinases. Numerous genes involved in cell wall biogenesis, remodeling, and cell wall-based defense, including lignin synthesis, were also upregulated in the resistant cultivar, indicating the possible role of wall composition in disease resistance. It was remarkable that many transcription factors (TS), some of which involved in Induced Systemic Resistance (ISR), as well as some also involved in abiotic stress response, were found to be uniquely expressed in ‘Koroneiki’, while ‘Nocellara del Belice’ was lacking an effective system of defense, expressing genes that overlap with wounding responses, and, to a minor extent, genes related to phenylpropanoid and terpenoid pathways. Only a Thaumatin-like gene was found in both cultivars showing a similar expression. In this work, the genetic factors and mechanism underlying the putative resistance trait against this fungal pathogen were unraveled for the first time and possible target genes for breeding resistant olive genotypes were found.

Adaptation Mechanisms of Olive Tree under Drought Stress: The Potential of Modern Omics Approaches

“…Apart from the aforementioned studies, the transcriptome of the olive tree has also been investigated under various biotic and abiotic stresses (Table 2). Regarding the biotic stressors, Marchese et al (2023) worked on a comparative transcriptomic analysis (RNA-seq) of leaf tissues from two varieties, Koroneiki (low susceptible) and Nocellara del Belice (high susceptible), infected by the obligate fungal pathogen Spilocea oleagina [94]. In their study, they reported significant differences between the two varieties including the early signaling and defense responses of Koroneiki and the expression of unique genes compared to Nocellara del Belice [94].…”

“…Regarding the biotic stressors, Marchese et al (2023) worked on a comparative transcriptomic analysis (RNA-seq) of leaf tissues from two varieties, Koroneiki (low susceptible) and Nocellara del Belice (high susceptible), infected by the obligate fungal pathogen Spilocea oleagina [94]. In their study, they reported significant differences between the two varieties including the early signaling and defense responses of Koroneiki and the expression of unique genes compared to Nocellara del Belice [94]. Another research group examined the Verticillium wilt of two olive varieties, Frantoio (tolerant) and Picual (susceptible), in the root tissue, resulting in significant differences in both varieties in the absence and presence of the pathogen [95].…”