Ectomycorrhizal symbiosis with Tuber spp. Enhances host performances in Pinus and Carya and induces host-specific patterns in defense-related regulation in the leaf transcriptomes.

Ectomycorrhizal fungi (EMF) colonize roots to establish symbiotic associations with plants. Sporocarps of the EMF Tuber spp. are considered as a delicacy in numerous countries and is a kind of EMF of great economic and social importance. Elucidating host responses to Tuber colonization would facilitate the exploration of symbiotic interactions and contribute to truffle cultivation. Tuber indicum and T. panzhihuanense, two primary commercial truffle species in China, were selected to colonize Pinus armandii and Carya illinoinensis in a two-and-a-half-year symbiosis experiment. Host performances, including growth, nutrient uptake, and physiological characteristics, were dynamically monitored. The molecular response of host leaf to Tuber symbiosis was further analyzed using RNA-seq. Tuber indicum and T. panzhihuanense exhibited superior colonization of P. armandii compared to that of C. illinoinensis. Both Tuber species enhanced the performance of the two hosts by increasing their height, stem circumference, and biomass. Phosphorus levels and activities of peroxidase and catalase in hosts were observed to increase during Tuber symbiosis. The results confirmed that Tuber colonization led to significant alterations in leaf transcriptomic profiles of the two trees. Tuber indicum and T. panzhihuanense both elicited defense-related regulation in host leaves, such as secondary metabolism, cell wall biogenesis, plant hormone signal transduction, and plant-pathogen interaction, with distinct patterns in P. armandii and C. illinoinensis. Our study provides an evaluation of host performance during truffle symbiosis and highlights the diverse patterns of Tuber-induced systematic defense regulation in hosts, offering insights into the specific symbiotic traits of Tuber-host pairs.