A Versatile Monosaccharide Transporter That Operates in the Arbuscular Mycorrhizal FungusGlomussp Is Crucial for the Symbiotic Relationship with Plants  

Abstract

For more than 400 million years, plants have maintained a mutualistic symbiosis with arbuscular mycorrhizal (AM) fungi. This evolutionary success can be traced to the role of these fungi in providing plants with mineral nutrients, particularly phosphate. In return, photosynthates are given to the fungus, which support its obligate biotrophic lifestyle. Although the mechanisms involved in phosphate transfer have been extensively studied, less is known about the reciprocal transfer of carbon. Here, we present the high-affinity Monosaccharide Transporter2 (MST2) from Glomus sp with a broad substrate spectrum that functions at several symbiotic root locations. Plant cell wall sugars can efficiently outcompete the Glc uptake capacity of MST2, suggesting they can serve as alternative carbon sources. MST2 expression closely correlates with that of the mycorrhiza-specific Phosphate Transporter4 (PT4). Furthermore, reduction of MST2 expression using host-induced gene silencing resulted in impaired mycorrhiza formation, malformed arbuscules, and reduced PT4 expression. These findings highlight the symbiotic role of MST2 and support the hypothesis that the exchange of carbon for phosphate is tightly linked. Unexpectedly, we found that the external mycelium of AM fungi is able to take up sugars in a proton-dependent manner. These results imply that the sugar uptake system operating in this symbiosis is more complex than previously anticipated.

The expression of GintPT, the phosphate transporter of Rhizophagus irregularis, depends on the symbiotic status and phosphate availability

“…We wondered whether our data could fit to the emerging model of the reciprocal rewards in which the cooperation between partners in the AM symbiosis is at the basis of the nutrient transfer (Kiers et al 2011;Selosse and Rousset 2011;Fellbaum et al 2012). In our experiments the regulation of the only available marker of a C flux from the fungus to the plants, the fungal hexose transporter GintMST2 (Helber et al 2011), was not in line with the model since an up-regulation of the GintMST2 in arbusculated cells of roots grown at 320 μM Pi compared to 32 μM was not observed (Fig. 4b).…”

“…AY116211) (Zocco et al 2011), and MST2 (accession no. HM143864) (Helber et al 2011). A melting curve was obtained as described above.…”

“…5). Since it has been proposed that the exchange of Pi versus carbon compounds in AM symbiosis is interconnected (Kiers et al 2011), we also investigated the expression profile of GintMST2, the R. irregularis hexose transporter recently characterized by Helber et al (2011) in arbusculated cells. The gene is in fact possibly involved in the uptake of hexoses released by the plant in the periarbuscular space.…”

“…4b). However, it is worth noting that GintMST2 transcripts were detected not only in arbuscules but also in intercellular hyphae (Helber et al 2011), suggesting that the periarbuscular space may not be the only site in which the exchange of P for C occurs. In addition, we could envisage that other sugar transporters may be involved in supplying C to the fungus in mycorrhizal roots, or that GintMST2 is not the only one controlling the P versus C exchanges in arbusculated cells.…”

“…We therefore investigated the MtPT4 gene, encoding a phosphate transporter of Medicago truncatula, which is expressed in arbuscule-containing cells and is responsible for the uptake of Pi released by the fungus in the periarbuscular space (Harrison et al 2002;Javot et al 2007). We also investigated the MST2 gene, the fungal hexose transporter which is possibly involved in C uptake (Helber et al 2011). Our results conclusively demonstrate that, under controlled conditions, the AM fungus constitutively expresses GintPT, and that a connection with the host plant is required to support high expression levels in the extraradical hyphae.…”