Multitrophic Interactions with Oaks
Plant Physiology
Final Report Abstract
The TrophinOak project aimed at answering the general question how long lived forest trees harmonize their own development and the diversity of beneficial and detrimental interactions with organisms associated to their above- or belowground parts. We focused on gene regulation and resource allocation in the common oak (Quercus robur L.), a foundation forest tree species with large distribution in Europe, which harbours one of the highest level and diversity of multitrophic interactions. Oaks typically display an Endogenous Rhythmic Growth (ERG) characterized by alternating shoot flushes (SF) and root flushes (RF). The project used the micro-propagated oak clone DF159 to produce genetically identical micro-cuttings, and a controlled microcosm system to synthesize ectomycorrhizal symbioses with the fungus Piloderma croceum in combination with six further biotrophic interactors: the root pathogenic fungus Phytophthora quercina (Subproject RootPatho-EMF), the root herbivore nematode Pratylenchus penetrans and the rhizosphere consumer Collembola Protaphorura fimata (Subproject RootCons), the leaf pathogen powdery mildew Microsphaera alphitoides and a mycorrhiza helper bacterium Streptomyces AcH 505 (Subproject Leafpatho-MHB), the leaf herbivore Lymantria dispar (Subproject LeafCons). All subprojects used a Joint Experimental Platform (JEP) based on the microcosm system for double and triple biotrophic associations with DF159. The JEP also constructed a chamber to label plants with 13C and 15N toward the end of each experiment to quantify fluctuations in carbon and nitrogen allocation between below and above plant parts during SF vs. RF. The JEP also constructed a specific gene library with 70,000 contigs (OakCOntigDF159.1) to support annotation of the plant genes regulated in roots and shoots of DF159 during the different combinations of biotrophic interactions and ERG phases. The JEP enabled us to show that the ERG is paralleled with upward and downward shifts in plant resource allocation during SF and RF, respectively. A mycorrhizal inoculation enhanced the total C and N resources of the tree but influenced neither the resource oscillations nor the period of the ERG. The gene expression analyses showed that the ERG is internally controlled by mechanisms otherwise described in relation to circadian processes. Combining beneficial vs. detrimental interactions on roots or shoot with ectomycorrhizal infection enabled us to better understand the function of this ecologically obligate symbiosis. Obviously mycorrhiza helps oaks to overcome their most critical development phase, i.e. the production of new shoot units. It reduces plant defence but enhances stress tolerance, which minors the tree susceptibility to detrimental root herbivores and rhizosphere consumers. Another effect is the re-shifting of plant internal resources determined by the ERG, which reduced susceptibility to leaf pathogenic fungi during SF but temporarily enhanced it against root fungal pathogens during RF. In addition we found that gene regulation patterns during the ERG of plants faced separately with two interaction partners are not predictive of those observed after double inoculation. Depending on the interaction partner, the differential gene expression was higher either during the RF or the SF as well in the root as in the shoot; however these two patterns did not depend on whether the partner is beneficial or detrimental or interacts on root or shoot. The ERG trait was highly helpful to tackle mechanisms controlling the interplay between tree multitrophic interactions and growth. The regulation is often driven distantly from the distal plant part to the one growing or involved in a detrimental interaction. Symbiotic fungi or helper bacteria support such distance effects. Thanks to TrophinOak we took part to an international oak genome sequencing initiative, and initiated the PhytOakmeter project, in which we release saplings of DF159 along field catena in Central Germany and Europe to tackle the impact of global change on oak trees.
