The mutualism effector MiSSP7 of Laccaria bicolor alters the interactions between the poplar JAZ6 protein and its associated proteins

Yohann Daguerre,Laura Meyer,Romain Schellenberger,Jonathan M Plett,Claire Veneault-Fourrey,Sebastian Hartmann-Wittulski,Justine Bailly,Annegret Kohler,Francis Martin,Veronica Basso

doi:10.1038/s41598-020-76832-6

Abstract

Despite the pivotal role of jasmonic acid in the outcome of plant-microorganism interactions, JA-signaling components in roots of perennial trees like western balsam poplar (Populus trichocarpa) are poorly characterized. Here we decipher the poplar-root JA-perception complex centered on PtJAZ6, a co-repressor of JA-signaling targeted by the effector protein MiSSP7 from the ectomycorrhizal basidiomycete Laccaria bicolor during symbiotic development. Through protein–protein interaction studies in yeast we determined the poplar root proteins interacting with PtJAZ6. Moreover, we assessed via yeast triple-hybrid how the mutualistic effector MiSSP7 reshapes the association between PtJAZ6 and its partner proteins. In the absence of the symbiotic effector, PtJAZ6 interacts with the transcription factors PtMYC2s and PtJAM1.1. In addition, PtJAZ6 interacts with it-self and with other Populus JAZ proteins. Finally, MiSSP7 strengthens the binding of PtJAZ6 to PtMYC2.1 and antagonizes PtJAZ6 homo-/heterodimerization. We conclude that a symbiotic effector secreted by a mutualistic fungus may promote the symbiotic interaction through altered dynamics of a JA-signaling-associated protein–protein interaction network, maintaining the repression of PtMYC2.1-regulated genes.

Highlights

As an adaptation to nitrogen- and phosphorous -limiting conditions, the root systems of forest trees interact with the hyphae of mutualistic ectomycorrhizal (ECM) fungi to form a hybrid organ called the ectomycorrhizal root tip
TRP1 and LEU2 served as transformation markers for vectors whereas HIS3, URA3 and β-galactosidase LacZ (X-Gal) were used as reporter genes. (c) Live-cell imaging of PtJAZ6:GFP and transcription factors (TFs):RFP transiently expressed in Nicotiana benthamiana epidermal leaf cells transformed by agroinfiltration, using a laser-scanning confocal microscope in a sequential scanning mode
We identified PtJAZ6 (Potri.003G068900), MiSSP7 and a basic-helix-loop-helix transcription factors similar to Arabidopsis JAM1/2, that we named PtJAM1.1

Summary

Introduction

As an adaptation to nitrogen- and phosphorous -limiting conditions, the root systems of forest trees interact with the hyphae of mutualistic ectomycorrhizal (ECM) fungi to form a hybrid organ called the ectomycorrhizal root tip. MiSSP7 physically interacts with the Populus JAZ6 (PtJAZ6) protein in nuclei of host cells. This interaction inhibits the degradation of PtJAZ6 in the presence of JA and suppresses JA-dependent responses allowing in planta fungal colonization. The majority of these studies on JA pathways have been performed on the leaves of Arabidopsis, tomato, or rice In these well-studied model systems, the bioactive JA-hormone (i.e., (+)-7-iso-jasmonoyl-L-Ile)[25], is perceived by a co-receptor complex consisting of dimerized JASMONATE ZIM-DOMAIN (JAZ) proteins, which form part of a transcription factor (TF) repression complex, and the F-box protein CORONATIN INSENSITIVE1 (COI1), which is part of a Skp1/Cullin/F-box E3 ubiquitin ligase[26]. JAZ proteins interact with a wide range of transcription factors (TFs) and are major hubs integrating environmental and developmental cues in order to modulate several developmental and physiological processes on the basis of a growth-to-defense energetic trade-off[23,27,28]

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