Interspecific communication between pinewood nematode, its insect vector, and associated microbes

•The pinewood nematode (PWN) forms a symbiotic partnership with its insect vector and associated microbes. •Chemical signals produced by Monochamus beetle and fungi promote the spread of PWN. •Horizontal gene transfer has contributed to the plasticity and pathogenicity of PWN. Pine wilt disease (PWD) is perhaps the most serious threat to pine forests worldwide. The causative agent of PWD, the pinewood nematode (PWN), engages in a symbiotic partnership with its insect vector, the Monochamus beetle, as well as associated bacteria and ophiostomatoid fungi, in order to successfully infect and kill its host pine tree. This review focuses on the interspecific communication between PWN and its associated partners, and the potential role of this communication in promoting pathogenicity and invasiveness of PWN. We describe the chemical and molecular signals positively influencing the survival, reproduction, and spread of PWN. Knowledge of these signals could potentially be used to interfere with the proliferation and dispersal of PWN. Pine wilt disease (PWD) is perhaps the most serious threat to pine forests worldwide. The causative agent of PWD, the pinewood nematode (PWN), engages in a symbiotic partnership with its insect vector, the Monochamus beetle, as well as associated bacteria and ophiostomatoid fungi, in order to successfully infect and kill its host pine tree. This review focuses on the interspecific communication between PWN and its associated partners, and the potential role of this communication in promoting pathogenicity and invasiveness of PWN. We describe the chemical and molecular signals positively influencing the survival, reproduction, and spread of PWN. Knowledge of these signals could potentially be used to interfere with the proliferation and dispersal of PWN. a pair of chemosensory organs in the nematode head that are open to the environment enabling the detection of chemical cues. water-soluble, small-molecule pheromones that mediate developmental diapause, aggregation, and mating attraction in nematodes. These pheromones are derivatives of the dideoxy-L-sugar ascarylose, which are linked to fatty acid-derived side chains of varying lengths and are often decorated further with building blocks derived from amino acids, folate, and other primary metabolites. a family of secreted peptide ligands that play important roles in plant growth and development. They share a putative N-terminal signal peptide and a conserved C-terminal 14-amino acid CLE motif. nematodes belonging to the genus Globodera, including the soybean cyst nematode and potato cyst nematode that attack plant roots. a nuclear hormone receptor that is downstream of the insulin/IGF-1 and transforming growth factor (TGF)-β pathways and that regulates dauer diapause in many nematode species. 4-hydroxy-4-methyl-2-pentanone, a clear liquid with fragrance. juveniles that are specialized for dispersal to and infection of a new host. the molting and emergence of an adult insect from its pupal case. the irreversible change at the genetic level of biological populations over successive generations over a long period of time. naturally occurring genetic differences both within populations of the same species and between populations of different species. the transmission of DNA (deoxyribonucleic acid) encoding genes between different genomes. This phenomenon occurs, especially, frequently in single celled organisms. biological signaling pathways that enable an organism to respond to biological infections or invasions. a neuroendocrine pathway in nematodes that controls dauer diapause, metabolism, and lifespan. Protein hormones called insulin promote growth by binding to the insulin/IGF-1 receptor and promoting downstream signaling by the DAF-12 and other pathways. the use of proteins by a pathogen that are similar to host proteins to mimic those proteins in order to interfere with biological signaling in the host and to benefit the pathogen; these proteins are often initially acquired by the pathogen through HGT of the corresponding gene from the host. a polyphyletic group of morphologically similar genera of ascomycetes, including Ophiostoma, Grosmannia, and Ceratocystis species. They are commonly associated with bark beetles and cause a blue stain in freshly cut logs, especially on softwoods. They are not pathogenic to the pine trees themselves but benefit the associated beetles by decreasing tree vigor or by providing a food source to the bark beetles. a heterogeneous group of proteins induced in plants by pathogen infection and exogenous chemicals. the adaptability of an organism to environmental changes. infochemicals used among individuals for communication in animals. It can be secreted or excreted by an organism to trigger responses/behavior of others of the same species (animals include insects). juveniles belonging to the propagative part of the life cycle of nematodes in which the nematode reproduces. In the context of PWN, the propagative stages multiply inside the pine tree host, feeding on it, and leading to its demise. a hollowed out space in the xylem of the pine tree that is created by the chewing action of the Monochamus beetle larvae and that serves to protect the beetle as it pupates. intercellular canals in a woody stem or a leaf, lined with glandular epithelium that secretes resins. a hollow mouth spear in a plant parasitic nematode that the nematode pushes into plant cells in order to inject digestive enzymes. The stylet is then used by the nematode to suck and consume the liquefied contents of the plant cell. a class of volatile, nonpolar secondary metabolites that are structurally related to isoprene and that are produced by plants and some insects primarily as chemical signals. a foreign chemical or substance found in an organism or biological system that is not produced by that organism, but originated from another source; often toxic and must be destroyed and/or excreted by the organism. part of the vascular system in a plant that transports water and dissolved minerals from the roots to the rest of the plant; the interior parts of a tree that include the protoxylem and metaxylem.