Characterization of a carbohydrate transporter from symbiotic glomeromycotan fungi

Abstract

The symbiotic relationships between mycorrhizal fungi and plants have an enormous impact on terrestrial ecosystems. Most common are the arbuscular mycorrhizas, formed by fungi belonging to the phylum Glomeromycota. Arbuscular mycorrhizal fungi facilitate the uptake of soil nutrients by plants and in exchange obtain carbohydrates, thus representing a large sink for atmospheric plant-fixed CO(2). However, how carbohydrates are transported through the symbiotic interface is still unknown. Here we report the characterization of the first known glomeromycotan monosaccharide transporter, GpMST1, by exploiting the unique symbiosis of a glomeromycotan fungus (Geosiphon pyriformis) with cyanobacteria. The GpMST1 gene has a very low GC content and contains six introns with unusual boundaries. GpMST1 possesses twelve predicted transmembrane domains and functions as a proton co-transporter with highest affinity for glucose, then mannose, galactose and fructose. It belongs to an as yet uncharacterized phylogenetic monosaccharide transporter clade. This initial characterization of a new transporter family involved in fungal symbiosis will lead to a better understanding of carbon flows in terrestrial environments.

Sugar transport in arbuscular mycorrhizal symbiosis

“…The plant cell wall in the interface space of arbuscular mycorrhizae was shown to be amorphous, very thin, and containing sugar mainly as glucose, mannose, galactose and xylose (Bonfante 2001). It was speculated, therefore, that at least a portion of the monosaccharides could be liberated from plant extracellular polysaccharides and taken up by arbuscular mycorrhizal fungi (AMF) (Schu¨ßler et al 2006). To illustrate the location and the forms of sugar and Pi transported at the arbuscule-cortical cell interface in the AM symbiosis, we incorporated those elucidated in recent publications in Fig.…”

“…Isotopic labeling and radio-respirometry (Solaiman and Saito 1997) have been used to show that sucrose allocated to the symbiotic interfaces through the apoplast and symplast pathways (Hause and Fester 2005;Bu¨cking and Shachar-Hill 2004) is hydrolyzed to glucose and fructose by a cellwall-bound invertase, and these monosaccharides are taken up by the fungi (Schubert et al 2004). Schu¨ßler et al (2006) demonstrated recently that there might be sugars other than glucose and fructose that are transported at the arbuscule-cortical cell interfaces. Glomeromycotan monosaccharide transporter (GpMST1) functions as a proton co-transporter in transporting monosaccharides, with rates in the following order: glucose mannose galactose fructose (Schu¨ßler et al 2006).…”

“…Schu¨ßler et al (2006) demonstrated recently that there might be sugars other than glucose and fructose that are transported at the arbuscule-cortical cell interfaces. Glomeromycotan monosaccharide transporter (GpMST1) functions as a proton co-transporter in transporting monosaccharides, with rates in the following order: glucose mannose galactose fructose (Schu¨ßler et al 2006). The plant cell wall in the interface space of arbuscular mycorrhizae was shown to be amorphous, very thin, and containing sugar mainly as glucose, mannose, galactose and xylose (Bonfante 2001).…”

“…Only one fungal gene putatively encoding a sugar transporter has been characterized in AMF. Dissecting a unique symbiosis between a glomeromycotan fungus (G. pyriformis) and a cyanobacterium (Nostoc punctiforme) led Schu¨ßler et al (2006) to isolate the AMF sugar transporter gene, GpMST1. The predicted protein possesses twelve transmembrane domains.…”

Dierential Gene Expression in Incompatible Interaction between Wheat and Stripe Rust Fungus Revealed by Cdna-AFLP and Comparison to Compatible Interaction

“…Electrophysiological studies showed its substrate specificity, whereas cytological analysis showed that it is very specifically localised at the haustorial plasma membrane. Similarly, the mycorrhizal fungus Geosiphon pyriformis, which forms a symbiotic relationship with plant roots allowing them to acquire nutrients more efficiently from soil, possesses a novel hexose transporter with highest affinity for glucose (followed by mannose, galactose, and fructose), which may be involved in the fungus-root cell mutualistic symbiosis that is of such importance to plant growth in diverse terrestrial ecosystems [20]. However, the role of these transporters in each respective plant-fungal interaction could not be determined by gene functional analysis because both U. fabae and G. pyriformis are obligate symbionts, which cannot be cultured away from their plant hosts, so the significance of these Figure 1.…”