Publication

Ethylene and jasmonic acid act as negative modulators during mutualistic symbiosis between Laccaria bicolor and Populus roots Public

Jonthan M. Plett, Amit Khachane, Malika Ouassou,Björn Sundberg,Annegret Kohler,Francis Martin 2014 January 03 New Phytologist 202(1): 270-286

Abstract

  • The plant hormones ethylene, jasmonic acid and salicylic acid have interconnecting roles during the response of plant tissues to mutualistic and pathogenic symbionts. 
  • We used morphological studies of transgenic- or hormone-treated Populus roots as well as whole-genome oligoarrays to examine how these hormones affect root colonization by the mutualistic ectomycorrhizal fungus Laccaria bicolor S238N. 
  • We found that genes regulated by ethylene, jasmonic acid and salicylic acid were regulated in the late stages of the interaction between L. bicolor and poplar. Both ethylene and jasmonic acid treatments were found to impede fungal colonization of roots, and this effect was correlated to an increase in the expression of certain transcription factors (e.g. ETHYLENE RESPONSE FACTOR1) and a decrease in the expression of genes associated with microbial perception and cell wall modification. Further, we found that ethylene and jasmonic acid showed extensive transcriptional cross-talk, cross-talk that was opposed by salicylic acid signaling. 
  • We conclude that ethylene and jasmonic acid pathways are induced late in the colonization of root tissues in order to limit fungal growth within roots. This induction is probably an adaptive response by the plant such that its growth and vigor are not compromised by the fungus.

Highlights

Figure 1. Increased ethylene signaling reduces the development of the Hartig net. (a) Transverse cross-section of a poplar root colonized by Laccaria bicolor under control conditions after 14 d of contact. M, mantle; E, epidermal cell; PC, parenchyma cell; HN, Hartig net. (b) Transverse cross-section of a poplar root colonized without fungal contact. (c) Percentage of roots exhibiting a fungal mantle. (d) Measurements of Hartig net depth of wild-type Populus tremula × Populus tremuloides clone T89 after 14 d of contact with L. bicolor compared with L. bicolor colonization of root systems of plants insensitive to ethylene (35S::Atetr1-1 line 1E and 35S::Atetr1-1 line 3A) or root systems that produce higher levels of 1-aminocyclopropane-1-carboxylic acid (ACC) (35S::PttACO1 line 13 and 35S::PttACO1 line 23). Error bars represent standard error (± SE); significant difference from wild type: *, P < 0.05. (e) Transverse cross-section of a 35S::PttACO1 root colonized by L. bicolor under control conditions after 14 d of contact. (f) Transverse cross-section of a 35S::Atetr1-1 root colonized by L. bicolor under control conditions after 14 d of contact. Bars, 10 μm.

Citation

Plett, J. M., Khachane, A., Ouassou, M., Sundberg, B., Kohler, A. and Martin, F. (2014), Ethylene and jasmonic acid act as negative modulators during mutualistic symbiosis between Laccaria bicolor and Populus roots. New Phytologist. 201(1): 270-286 doi: 10.1111/nph.12655