Molecular Defense Response of Pine Trees (Pinus spp.) to the Parasitic Nematode Bursaphelenchus xylophilus

Abstract

Pine wilt disease (PWD) is a severe environmental problem in Eastern Asia and Western Europe, devastating large forest areas and causing significant economic losses. This disease is caused by the pine wood nematode (PWN), Bursaphelenchus xylophilus, a parasitic migratory nematode that infects the stem of conifer trees. Here we review what is currently known about the molecular defense response in pine trees after infection with PWN, focusing on common responses in different species. By giving particular emphasis to resistance mechanisms reported for selected varieties and families, we identified shared genes and pathways associated with resistance, including the activation of oxidative stress response, cell wall lignification, and biosynthesis of terpenoids and phenylpropanoids. The role of post-transcriptional regulation by small RNAs in pine response to PWN infection is also discussed, as well as the possible implementation of innovative RNA-interference technologies, with a focus on trans-kingdom small RNAs. Finally, the defense response induced by elicitors applied to pine plants before PWN infection to prompt resistance is reviewed. Perspectives about the impact of these findings and future research approaches are discussed.

Keywords: differential gene expression; migratory nematode; pine wilt disease; post-transcriptional regulation; resistance; small RNAs; susceptibility; trans-kingdom RNA silencing; transcriptomics.

Figure 1

Representation of pine defense response to pinewood nematode (PWN). Pattern-triggered immunity (PTI) is initiated after recognition of nematode-associated molecular patterns (NAMPs), such as BxCDP1, or damage-associated molecular patterns (DAMPs) from damaged plant cells, by cell surface receptor-like kinases (RLKs) or receptor-like proteins (RLPs). PTI leads to a transcriptional reprograming of the plant cell, which includes the activation of hormone pathways, such as jasmonic acid (JA) and salicylic acid (SA) pathways, the expression of pathogenesis-related genes (PR), genes involved in oxidative stress response, and genes encoding enzymes involved in the biosynthesis of secondary metabolites (terpenes and phenylpropanoids). In susceptible plants, it is possible that the activation of the SA pathway inhibits the JA pathway. PWN releases effectors, such as the apoplastic VAP1 and BxSapB1, that repress the plant defense response. These effectors may be recognized by resistance genes, whether directly or indirectly through the monitoring of a co-factor protein that is altered by the effector. Effectors can be recognized by cell surface receptors, when they are apoplastic, or internal nucleotide-binding/leucine-rich-repeat (NLR) receptors, when they are injected into the cytoplasm by the PWN. Recognition of effectors by resistance genes initiates a stronger and more sustained defense response, the effector-triggered immunity (ETI).