Eavesdropping roots: Fagus sylvatica detects belowground stress signals from conspecific and heterospecific ( Picea abies ) neighbors, triggering increased shoot VOC emissions

Volatile organic compounds (VOCs) facilitate aboveground plant communication, but belowground signaling remains less understood.

This study explored root-root interactions between Picea abies and Fagus sylvatica saplings in monospecific ( Fagus-Fagus ) and heterospecific ( Picea-Fagus ) pairs (n=6), excluding shoot-level VOC communication. Sender plants were treated with jasmonic acid to simulate herbivory and labeled with ¹³ CO ₂ and ¹⁵ NH ₄ NO ₃ to trace nutrient transfer in a split-root design. VOC emissions and gas exchange were measured over ten days using PTR-TOF-MS and ¹³ CO ₂ -spectroscopy and ¹³ C and ¹⁵ N were analyzed in roots and shoots via EA-IRMS.

Our findings reveal, that (i) JA treatment induced strong de novo terpenoid emissions from P. abies and enhanced emissions of oxygenated VOCs and benzenoids from F. sylvatica , (ii) F. sylvatica receiver plants responded similarly to JA-treated neighbors, indicating belowground signaling, and (iii) responses of receiver plants were more pronounced in the heterospecific treatment. Furthermore, formic acid emissions from soils increased following JA treatment, suggesting altered soil microbial activity. Isotopic analysis revealed C exudation into the rhizosphere and N transfer to receiver plants.

These results suggest that belowground signaling enables early priming of herbivore-induced defenses in neighboring plants, and that the response intensity is modulated by species identity.