Truffles regulate plant root morphogenesis via the production of auxin and ethylene.
Truffles are symbiotic fungi that form ectomycorrhizas with plant roots. Here we present evidence that at an early stage of the interaction, i.e. prior to physical contact, mycelia of the white truffle Tuber borchii and the black truffle Tuber melanopsorum induce alterations in root morphology of the host Cistus incanus and the nonhost Arabidopsis (Arabidopsis thaliana; i.e. primary root shortening, lateral root formation, root hair stimulation). This was most likely due to the production of indole-3-acetic acid (IAA) and ethylene by the mycelium. Application of a mixture of the ethylene precursor 1-aminocyclopropane-1-carboxylic acid and IAA fully mimicked the root morphology induced by the mycelium for both host and nonhost plants. Application of the single hormones only partially mimicked it. Furthermore, primary root growth was not inhibited in the Arabidopsis auxin transport mutant aux1-7 by truffle metabolites while root branching was less effected in the ethylene-insensitive mutant ein2-LH. The double mutant aux1-7;ein2-LH displayed reduced sensitivity to fungus-induced primary root shortening and branching. In agreement with the signaling nature of truffle metabolites, increased expression of the auxin response reporter DR5GFP in Arabidopsis root meristems subjected to the mycelium could be observed, confirming that truffles modify the endogenous hormonal balance of plants. Last, we demonstrate that truffles synthesize ethylene from l-methionine probably through the alpha-keto-gamma-(methylthio)butyric acid pathway. Taken together, these results establish the central role of IAA and ethylene as signal molecules in truffle/plant interactions.
Splivallo
Richard
R
Department of Crop Sciences, Molecular Phytopathology and Mycotoxin Research , Georg-August University, D-37077 Goettingen, Germany. ricsi17@hotmail.com
Fischer
Urs
U
Göbel
Cornelia
C
Feussner
Ivo
I
Karlovsky
Petr
P
D000598:Amino Acids, Cyclic / Q000494:pharmacology; D017360:Arabidopsis / Q000187:drug effects / Q000378:metabolism / Q000382:microbiology; D001203:Ascomycota / Q000187:drug effects / Q000502:physiology*; D001681:Biological Assay; D020148:Butyric Acid / Q000378:metabolism; D003470:Culture Media; D005030:Ethylenes / Q000096:biosynthesis*; D054884:Host-Pathogen Interactions / Q000187:drug effects; D007210:Indoleacetic Acids / Q000378:metabolism* / Q000494:pharmacology; D053858:Metabolic Networks and Pathways / Q000187:drug effects; D009024:Morphogenesis / Q000187:drug effects; D009154:Mutation / Q000235:genetics; D018517:Plant Roots / Q000033:anatomy & histology / Q000187:drug effects / Q000196:embryology* / Q000382:microbiology*; D015398:Signal Transduction / Q000187:drug effects
D000598:Amino Acids, Cyclic; D003470:Culture Media; D005030:Ethylenes; D007210:Indoleacetic Acids; D020148:Butyric Acid; C023863:1-aminocyclopropane-1-carboxylic acid; C030737:indoleacetic acid; C036216:ethylene