Abstract
Microbial symbionts are known to assist exotic pests in their colonization of new host plants. However, there has been little evidence linking symbiotic invasion success to mechanisms for mitigation of native plant resistance. The red turpentine beetle (RTB) was introduced with a fungus, Leptographium procerum, to China from the United States and became a destructively invasive symbiotic complex in natural Pinus tabuliformis forests. Here, we report that three Chinese-resident fungi, newly acquired by RTB in China, induce high levels of a phenolic defensive chemical, naringenin, in pines. This invasive beetle-fungus complex is suppressed by elevated levels of naringenin. However, cryptic microbiotas in RTB galleries strongly degrade naringenin, and pinitol, the main soluble carbohydrate of P. tabuliformis, is retained in L. procerum-infected phloem and facilitate naringenin biodegradation by the microbiotas. These results demonstrate that cryptic microbiota mitigates native host plant phenolic resistance to an invasive symbiotic complex, suggesting a putative mechanism for reduced biotic resistance to symbiotic invasion.
Highlights
Microbial symbionts are known to assist exotic pests in their colonization of new host plants
Cryptic microbiotas in red turpentine beetle (RTB) galleries strongly degrade naringenin, and pinitol, the main soluble carbohydrate of P. tabuliformis, is retained in L. procerum-infected phloem and facilitate naringenin biodegradation by the microbiotas. These results demonstrate that cryptic microbiota mitigates native host plant phenolic resistance to an invasive symbiotic complex, suggesting a putative mechanism for reduced biotic resistance to symbiotic invasion
The rest of fungi were associated with RTB both in China and US: Leptographium procerum is the primary fungal associate of Chinese RTB, which had all alleles shared by US RTB-associated L. procerum, with no allele unique in Chinese populations, this demonstrating that L. procerum associated with RTB in China originated from those with RTB in US and is referred to as “Chinese-invasive”; the other species that had no population genetic evidence yet are temporarily classified as “shared” fungal species
Summary
Microbial symbionts are known to assist exotic pests in their colonization of new host plants. We report that three Chinese-resident fungi, newly acquired by RTB in China, induce high levels of a phenolic defensive chemical, naringenin, in pines This invasive beetle-fungus complex is suppressed by elevated levels of naringenin. Cryptic microbiotas in RTB galleries strongly degrade naringenin, and pinitol, the main soluble carbohydrate of P. tabuliformis, is retained in L. procerum-infected phloem and facilitate naringenin biodegradation by the microbiotas These results demonstrate that cryptic microbiota mitigates native host plant phenolic resistance to an invasive symbiotic complex, suggesting a putative mechanism for reduced biotic resistance to symbiotic invasion. Studies have reported that compromised plant defences have contributed to the success of invasive insect pests on their new hosts[11,12,13] Even though it is considered as an important barrier for colonization, the role of plant chemical defence as mediated by an invader’s microbial symbionts has received little attention. The fungal community composition has shifted from species associated with RTB in the United States to species newly acquired in China (See Supplementary Table S1)
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