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

Inês Modesto; Lieven Sterck; Vicent Arbona; Aurelio Gómez-Cadenas; Isabel Carrasquinho; Yves Van de Peer; Célia M Miguel

doi:10.3389/fpls.2021.690857

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

Front Plant Sci. 2021 Jun 10:12:690857. doi: 10.3389/fpls.2021.690857. eCollection 2021.

Authors

Inês Modesto^{1

2

3}, Lieven Sterck^{3

4}, Vicent Arbona⁵, Aurelio Gómez-Cadenas⁵, Isabel Carrasquinho^{6

7}, Yves Van de Peer^{3

4

8}, Célia M Miguel^{2

9}

Affiliations

¹ Instituto de Tecnologia Química e Biológica, Universidade Nova de Lisboa, Oeiras, Portugal.
² Instituto de Biologia e Tecnologia Experimental, Oeiras, Portugal.
³ Department of Plant Biotechnology and Bioinformatics, Ghent University, Ghent, Belgium.
⁴ VIB-UGent Center for Plant Systems Biology, Ghent, Belgium.
⁵ Departament de Ciències Agràries i del Medi Natural, Universitat Jaume I, Castelló de la Plana, Spain.
⁶ Instituto Nacional Investigaciao Agraria e Veterinaria, Oeiras, Portugal.
⁷ Linking Landscape, Environment, Agriculture and Food, Instituto Superior de Agronomia, Universidade de Lisboa, Lisbon, Portugal.
⁸ Department of Biochemistry, Genetics and Microbiology, University of Pretoria, Pretoria, South Africa.
⁹ Biosystems and Integrative Sciences Institute, Faculdade de Ciências, Universidade de Lisboa, Lisbon, Portugal.

Abstract

Pine wilt disease (PWD), caused by the plant-parasitic nematode Bursaphelenchus xylophilus, has become a severe environmental problem in the Iberian Peninsula with devastating effects in Pinus pinaster forests. Despite the high levels of this species' susceptibility, previous studies reported heritable resistance in P. pinaster trees. Understanding the basis of this resistance can be of extreme relevance for future programs aiming at reducing the disease impact on P. pinaster forests. In this study, we highlighted the mechanisms possibly involved in P. pinaster resistance to PWD, by comparing the transcriptional changes between resistant and susceptible plants after infection. Our analysis revealed a higher number of differentially expressed genes (DEGs) in resistant plants (1,916) when compared with susceptible plants (1,226). Resistance to PWN is mediated by the induction of the jasmonic acid (JA) defense pathway, secondary metabolism pathways, lignin synthesis, oxidative stress response genes, and resistance genes. Quantification of the acetyl bromide-soluble lignin confirmed a significant increase of cell wall lignification of stem tissues around the inoculation zone in resistant plants. In addition to less lignified cell walls, susceptibility to the pine wood nematode seems associated with the activation of the salicylic acid (SA) defense pathway at 72 hpi, as revealed by the higher SA levels in the tissues of susceptible plants. Cell wall reinforcement and hormone signaling mechanisms seem therefore essential for a resistance response.

Keywords: Bursaphelenchus xylophilus; cell wall lignification; jasmonate; maritime pine; pine wilt disease; resistance genes; secondary metabolism; transcriptome.