Identification of the function of mutualistic root endophytic fungi using the Arabidopsis transcriptome

Ari Jumpponen

Root-associated mutualistic fungi are important determinants of many ecosystem functions because they control community dynamics and net primary productivity of their host plants (Hartnett and Wilson 1999; Newsham et al. 1995). Mycorrhizal fungi are an abundant and relatively well-understood group of such mutualists. Our recent observations challenge the overwhelming abundance of the mycorrhizal root symbionts: non-mycorrhizal endophytes in Konza Prairie Long Term Ecological Research site equal or exceed the mycorrhizal fungi in abundance.  During experiments aiming to determine the host ranges of these endophytes, we discovered that at least two of the endophyte species form functional mutualisms with Arabidopsis thaliana and increase the host’s growth two- to four-fold. This finding is novel: A. thaliana does not associate with mycorrhizal fungi and there is only one prior example of endophyte associations in A. thaliana (Peskan-Berghöfer et al. 2004; Smith and Read 1997). We took advantage of this unique and fortuitous mutualism and tested distribution of A. thaliana responses to endophyte colonization. The results are congruent with the concept of mutualism parasitism continuum: among more than 30 conspecific endophytes, some strains improve host growth, while others are significantly inhibitory. We selected a neutral and a mutualistic strain to further our understanding of fungal mutualisms and are presently using an Affymetrix ATH1 array for A. thaliana to identify differentially up- and downregulated distal gene expression among plants grown endophyte-free or plants grown with a neutral and mutualistic endophytes. Our primary hypotheses are that, similar to mycorrhizal systems, root endophyte mutualisms are a result of 1) systemic host defense that improves the plant resistance against pathogens; 2) improved host nutrient metabolism; and, 3) improved host water use efficiency and drought tolerance. We anticipate that this system is broadly applicable to root symbioses and that the wealth of information available for A. thaliana will allow advances in understanding mycorrhizal and non-mycorrhizal root symbioses alike.

References:

Hartnett DC, Wilson GWT (1999) Mycorrhizae influence plant community structure and diversity in tallgrass prairie. Ecology 80:1187-1195

Newsham KK, Fitter AH, Watkinson AR (1995) Multi-functionality and biodiversity in arbuscular mycorrhizas. TREE 10:407-411

Peskan-Berghöfer T, Shahollari B, Giong PH, Hehl S, Markert C, Blanke V, Kost G, Varma A, Oelm¨ller R (2004) Association of Piriformospora indica with Arabidopsis thaliana roots represents a novel system to study beneficial plant-microbe interactions and involves early plant protein modifications in the endoplasmic reticulum and at the plasma membrane. Physiologia Plantarum 122:465-477

Smith SE, Read DJ (1997) Mycorrhizal symbiosis. Academic Press, London