Understanding pine wilt disease: roles of the pine endophytic bacteria and of the bacteria carried by the disease-causing pinewood nematode

Abstract

Pine wilt disease (PWD) is one of the most destructive diseases in trees of the genus Pinus and is responsible for environmental and economic losses around the world. The only known causal agent of the disease is the pinewood nematode (PWN) Bursaphelenchus xylophilus. Despite that, bacteria belonging to several different genera have been found associated with PWN and their roles in the development of PWD have been suggested. Molecular methodologies and the new era of genomics have revealed different perspectives to the problem, recognizing the manifold interactions between different organisms involved in the disease. Here, we reviewed the possible roles of nematode-carried bacteria in PWD, what could be the definition of this group of microorganisms and questioned their origin as possible endophytes, discussing their relation within the endophytic community of pine trees. The diversity of the nematode-carried bacteria and the diversity of pine tree endophytes, reported until now, is revised in detail in this review. What could signify a synergetic effect with PWN harming the plant, or what could equip bacteria with functions to control the presence of nematodes inside the tree, is outlined as two possible roles of the microbial community in the etiology of this disease. An emphasis is put on the potential revealed by the genomic data of isolated organisms in their potential activities as effective tools in PWD management.

Keywords: Bursaphelenchus xylophilus; bacteria; biocontrol; endophytes; nematodes; pine wilt disease.

Figure 1

Temporal and spatial spreading of pine wilt disease around the world. The PWN is native to North America (light blue) and was spread into Japan (blue); China, Korea, and Taiwan (orange); Nigeria and Mexico (green); and Portugal (continental and Madeira island) and Spain (yellow). ^#Occurrence of the disease in forests in North America is mostly limited to nonnative tree species

Figure 2

Schematic depiction of relationships between B. xylophilus and Monochamus spp. life cycles and pine wilt disease (PWD) development. The insect vector is attracted by healthy trees and releases nematodes during maturation feeding on young pine shoots. The pine trees could be resistant (death of nematodes) or susceptible (development of PWD symptoms, culminating in the death of pine trees). Monochamus spp. are also attracted by dead or dying pine trees for ovoposition. Later, during the larvae development, nematodes are attracted to pupae and (?) indicates that the bacteria maybe carried by nematodes into Monochamus spp. but this remains untested. The cycle restarts by emerging of adult Monochamus spp. carrying nematodes (and probably bacteria). PWD symptom classes: 0—tree without symptoms; I—‹10% brown leaves; II—10‐50% brown leaves; III—50‐80% brown leaves; IV—› 80% brown leaves; V—dead tree without leaves

Figure 3

Comprehensive role of bacteria in pine wilt disease (PWD). Venn diagrams showing common bacteria: i) associated with PWN from Portugal, USA, China, Japan, and Korea; ii) associated with PWN and endophytes from Pinus spp.; and iii) endophytic from P. flexilis, P. contorta, and P. sylvestris. Diagrams illustrate the three known roles of bacteria related with B. xylophilus or pine trees in PWD: i) PWD agents (red circles and red arrows) producing toxins and proteins; ii) nematicidal agents (blue circles and arrows) producing proteases and secretion machinery; and iii) beneficial products for plants (green circles and arrows) such as siderophores, lipases, proteases, acetoin (diacetyl) reductase, and nitrogen fixation genes. Bx ‐ Bursaphelenchus xylophilus