Comparative Transcriptomic Response of Two Pinus Species to Infection with the Pine Wood Nematode Bursaphelenchus xylophilus

Abstract

Pine wilt disease (PWD) caused by pine wood nematode (PWN), Bursaphelenchus xylophilus, is a serious threat to global forest populations of conifers, in particular Pinus spp. Recently, the presence of PWN was reported in dead Yunnan pine (Pinus yunnanensis) trees under natural conditions. To further understand the potential impact caused by PWN in Yunnan pine populations, a transcriptional profiling analysis was performed over different time points (0 hours (h), 6 h, 24 h, 48 h, and 7 days) after PWN inoculation. A total of 9961 differentially expressed genes were identified after inoculation, which suggested a dynamic response against the pathogen, with a more intense pattern at 48 h after inoculation. The results also highlighted a set of biological mechanisms triggered after inoculation that provide valuable information regarding the response of Yunnan pine to PWN infection. When compared with maritime pine (Pinus pinaster), the Yunnan pine response was less complex and involved a smaller number of differentially expressed genes, which may be associated with the increased degree of resistance to PWN displayed by Yunnan pine. These results revealed different strategies to cope with PWN infection by these two pine species, which display contrasting degrees of susceptibility, especially in the timely perception of the infection and response magnitude.

Insights Into the Mechanisms Implicated in Pinus pinaster Resistance to Pinewood Nematode

“…A significant reprogramming of gene expression was observed in P. pinaster plants after inoculation with the PWN. This observation is not surprising, and it is in accordance with previous studies on P. pinaster inoculated with PWN Gaspar et al, 2017Gaspar et al, , 2020 where susceptible plants have been analyzed. However, by focusing on both resistant and susceptible interactions in P. pinaster plants, we show here that although part of the transcriptional response to PWN was shared between both resistant and susceptible groups, significant qualitative and quantitative differences exist in gene expression.…”

“…The first transcriptomic analysis addressing the PWN response in P. pinaster was based on the comparison to P. pinea , described as less susceptible than P. pinaster (Santos et al, 2012 ), while more recent reports in P. pinaster described the transcriptional changes after PWN infection during a susceptible interaction (Gaspar et al, 2017 , 2020 ). However, despite the identification of P. pinaster genotypes considered resistant (Menéndez-Gutiérrez et al, 2017a , b ; Carrasquinho et al, 2018 ), the transcriptional response associated with resistance has not been previously analyzed.…”

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

“…However, a degree of overlap exists between the resistant and susceptible host with regard to the enriched GO terms by the defense response mechanisms, suggesting a similar transcriptional change by F. circinatum infection. Several examples in forest tree pathosystems have shown a delay in the defense response in susceptible interactions [ 34 , 52 , 53 , 54 ], including a Pinus - F. circinatum study [ 45 ]. The early activation of plant defense-related genes requires a straight recognition of pathogen elicitors.…”

“…Several genes encoding PR3 proteins were up-regulated in both pine species; however, a PR2 protein was only induced in P. pinea , suggesting a less effective response of P. radiata at an early stage of the disease. Likewise, the plant PR5 family, known as thaumatin-like protein (TLP), has also shown antifungal properties against several forest tree pathogens [ 27 , 29 , 37 , 54 , 85 ]. Additionally, Carrasco et al [ 38 ] suggested the possible role of PR1 and PR5 in the activation of the SA-dependent pathway, resulting in the induction of systemic induced resistance (SIR) against PPC in P. radiata .…”

Comparative Transcriptome Analysis of Pine Trees Treated with Resistance-Inducing Substances against the Nematode Bursaphelenchus xylophilus

“…Given that studies focussing solely on isolated contributary factors often fail to yield meaningful insights into the important elements of biological processes, we designed the present study with a view towards characterising an integrated environment comprising pine hosts, RISs, and PWNs. Simple treatment using RISs is limited to the detection of general genes (termed pathogenesis-related genes) under SAR conditions [ 67 , 68 ], whereas PWN infection in pine trees predominantly reflects the pathogenic mechanisms within dying cells [ 69 ]. Consequently, the integrated design of the present study enabled us to assess the sequential stages of RIS treatment and infection, as well as the activation of related genes under conditions of SAR induction, thereby facilitating subsequent analyses of the essential mechanisms underlying the protection against and inhibition of PWN.…”