Dual RNA-Sequencing Analysis of Resistant (Pinus pinea) and Susceptible (Pinus radiata) Hosts during Fusarium circinatum Challenge

Abstract

Fusarium circinatum causes one of the most important diseases of conifers worldwide, the pine pitch canker (PPC). However, no effective field intervention measures aiming to control or eradicate PPC are available. Due to the variation in host genetic resistance, the development of resistant varieties is postulated as a viable and promising strategy. By using an integrated approach, this study aimed to identify differences in the molecular responses and physiological traits of the highly susceptible Pinus radiata and the highly resistant Pinus pinea to F. circinatum at an early stage of infection. Dual RNA-Seq analysis also allowed to evaluate pathogen behavior when infecting each pine species. No significant changes in the physiological analysis were found upon pathogen infection, although transcriptional reprogramming was observed mainly in the resistant species. The transcriptome profiling of P. pinea revealed an early perception of the pathogen infection together with a strong and coordinated defense activation through the reinforcement and lignification of the cell wall, the antioxidant activity, the induction of PR genes, and the biosynthesis of defense hormones. On the contrary, P. radiata had a weaker response, possibly due to impaired perception of the fungal infection that led to a reduced downstream defense signaling. Fusarium circinatum showed a different transcriptomic profile depending on the pine species being infected. While in P. pinea, the pathogen focused on the degradation of plant cell walls, active uptake of the plant nutrients was showed in P. radiata. These findings present useful knowledge for the development of breeding programs to manage PPC.

Integrative Analysis of Genes Involved in the Global Response to Potato Wart Formation

“…The induction of nodulin proteins in potato– S. endobioticum interactions has been associated with improvements in pathogen fitness through control over plant transporters. As reported before, the accumulation of transporters for nutrient uptake represents a shift from the biotrophic phase to the necrotrophic phase in hemibiotrophic pathogens due to the rapid growth of secondary hyphae in the late stages of infection ( Zamora-Ballesteros et al, 2021 ).…”

Studying tree response to biotic stress using a multi-disciplinary approach: The pine pitch canker case study

“…However, the authors acknowledged that further physiological measurements (including hormone quantification) and functional studies with F. circinatum mutants are needed. The blocking of JA signalling by F. circinatum has been also proposed by Zamora-Ballesteros et al (2021). Moreover, besides increased levels of JA were found in P. radiata and P. pinaster needles, these species were still susceptible to F. circinatum infection (Amaral et al, 2019a,b).…”

“…The activation of PTI in response to F. circinatum infection in P. pinaster has been proposed due to the early upregulation of genes encoding a lysine motif receptor-like kinase (LysM-RLK), which has been associated to the recognition of fungal chitin (Hernandez-Escribano et al, 2020). Several genes coding for PRR containing domains have also been upregulated in the resistant P. pinea but not in the susceptible P. radiata, which may explain the weak downstream signalling in the latter (Zamora-Ballesteros et al, 2021). Regarding effector-triggered immunity (ETI), a second line of defence activated by the recognition of fungal effector proteins by plant resistance (R) proteins (Hammond-Kosack and Parker, 2003), there is still no evidence of its role in PPC.…”

“…(ii) non-enzymatic components, such as L-ascorbate, glycerol, and vitamin B6 were associated to PPC resistance (Amaral et al, 2019a(Amaral et al, , 2021bZamora-Ballesteros et al, 2021); and (iii) the induction of phenolic compounds seems key in pine antioxidant response to F. circinatum infection (further discussed). The exogenous application of some of these natural compounds or others that induce its biosynthesis could be further explored for the development of environmentally friendly measures to control PPC.…”

“…On the other hand, the importance of hormone-mediate defence responses against F. circinatum infection has been highlighted by recent transcriptomic studies in different pine species (Carrasco et al, 2017;Visser et al, 2019;Hernandez-Escribano et al, 2020;Zamora-Ballesteros et al, 2021). While abscisic acid (ABA) signalling-related genes were part of the second most relevant category of genes differentially expressed in P. radiata upon inoculation (Carrasco et al, 2017) and ABA catabolism seems to be activated (Zamora-Ballesteros et al, 2021); a complex integration and coordination of SA, jasmonic acid (JA), and ethylene (ET), and auxins signalling is suggested to be involved in the resistance of P. tecunumanii and P. pinea to PPC (Visser et al, 2019;Zamora-Ballesteros et al, 2021), as well as the moderate resistance shown by P. pinaster at early stages of infection (Hernandez-Escribano et al, 2020). In particular, lncRNAPiRa.85000.6 has been suggested as a key regulator of ET levels after infection: while P. pinaster presents a fine-tuned ET response against F. circinatum, this does not occur in P. radiata likely due to the influence of this lncRNA located upstream of its transcription (Zamora-Ballesteros et al, 2022).…”