Haustorium connection between parasitic Santalum album (sandalwood) and herbivore-damaged Dalbergia odorifera mediates the associational effect to an enhanced herbivory resistance in neighboring sandalwood

Parasitic plants withdraw water, nutrients and metabolites from other plants through haustoria, establishing intimate physiological connections with their host plants. However, the associational effects of herbivore-attacked host plants on parasite defense against other enemies, and especially whether the haustorium transmits defense signals, have not yet been examined. Under greenhouse conditions, we investigated how rosewood ( Dalbergia odorifera ) fed by Plecoptera oculata could affect chemical defenses in parasite sandalwood ( Santalum album ). Variables, including herbivore-induced plant volatiles (HIPVs), phytohormones, gene expression and transcriptomes were measured in both rosewood and sandalwood. A bioassay was also performed to evaluate defenses against herbivores ( P. oculata for rosewood and Delias aglaia for sandalwood) using several typical HIPVs. Volatile compound analyses revealed that when parasitized rosewood were fed on by P. oculata , there was a marked increase in the relative abundance of HIPVs in damaged rosewood and attached sandalwood. Attached sandalwood increased levels of jasmonic acid (JA) and gene expression ( AOC and LOX ), and enriched the arachidonic acid pathway after P. oculata feeding on host rosewood, suggesting that the defense signal did translocate through the haustoria. Individual volatile compound exposure experiments showed that DMNT, β-ocimene, and hexadecane in rosewood as well as hexadecane in sandalwood strongly repelled the feeding of P. oculata and D. aglaia , respectively, which can be considered as induced defenses. These results demonstrated that sandalwood had directly and indirectly affected by rosewood-associational effects, primarily with a defense signal transmission through haustoria connections. Our findings have potential importance for the development of pest control strategies in mixed plantations with parasite species. • Haustoria translocate defense signal from host to parasite. • Herbivore-damaged induces defense responses of rosewood and attached sandalwood. • HIPVs elevate the resistance to herbivore attacks.