Regulation of Arbuscular Mycorrhization by Carbon. The Symbiotic Interaction Cannot Be Improved by Increased Carbon Availability Accomplished by Root-Specifically Enhanced Invertase Activity

Abstract

The mutualistic interaction in arbuscular mycorrhiza (AM) is characterized by an exchange of mineral nutrients and carbon. The major benefit of AM, which is the supply of phosphate to the plant, and the stimulation of mycorrhization by low phosphate fertilization has been well studied. However, less is known about the regulatory function of carbon availability on AM formation. Here the effect of enhanced levels of hexoses in the root, the main form of carbohydrate used by the fungus, on AM formation was analyzed. Modulation of the root carbohydrate status was performed by expressing genes encoding a yeast (Saccharomyces cerevisiae)-derived invertase, which was directed to different subcellular locations. Using tobacco (Nicotiana tabacum) alcTcwINV plants, the yeast invertase was induced in the whole root system or in root parts. Despite increased hexose levels in these roots, we did not detect any effect on the colonization with Glomus intraradices analyzed by assessment of fungal structures and the level of fungus-specific palmitvaccenic acid, indicative for the fungal carbon supply, or the plant phosphate content. Roots of Medicago truncatula, transformed to express genes encoding an apoplast-, cytosol-, or vacuolar-located yeastderived invertase, had increased hexose-to-sucrose ratios compared to b-glucuronidase-transformed roots. However, transformations with the invertase genes did not affect mycorrhization. These data suggest the carbohydrate supply in AM cannot be improved by root-specifically increased hexose levels, implying that under normal conditions sufficient carbon is available in mycorrhizal roots. In contrast, tobacco rolCTppa plants with defective phloem loading and tobacco pyk10TInvInh plants with decreased acid invertase activity in roots exhibited a diminished mycorrhization.Arbuscular mycorrhiza (AM) represents a widespread mutualistic association between soil-born fungi of the phylum Glomeromycota and most land plants. The AM interaction enables the plant to improve its supply of water and mineral nutrients, mainly phosphate. In return, the obligate biotrophic AM fungi are provided with carbon. In the Arum-type interaction, as analyzed here between Glomus sp. and tobacco (Nicotiana tabacum) or Medicago truncatula, the AM fungus colonizes the cortical cells by formation of intra-and intercellular hyphae and very characteristic haustorialike structures, the highly branched intracellular arbuscules. When the carbon supply is sufficient, lipid-rich vesicles are formed intercellularly within the cortex, as fungal storage organs. Intracellular fungal structures are separated from the plant cytoplasm by an extension of the plasma membrane, forming the periarbuscular membrane surrounding the arbuscule. The greatly increased surfaces of host and arbuscule plasma membranes offers optimized conditions for effective nutrient exchange via the established symbiotic interface (for review, see Gianinazzi-Pearson et al., 1996;Harrison, 1999).The exchange of phosphate via the periarbuscular interface and th...

Constitutive overexpression of the sucrose transporter SoSUT1 in potato plants increases arbuscular mycorrhiza fungal root colonization under high, but not under low, soil phosphorus availability

“…The observation that SUT1antisense plants did not differ in their extent of AM fungal root colonization from corresponding WT plants in our study is in disagreement with earlier findings of Schaarschmidt et al (2007a), who observed a decrease in the extent of AM fungal root colonization in tobacco plants with impaired pyrophosphate-dependent uptake of sucrose into the phloem. Since different plant species and different approaches to impairing plant phloem loading of sucrose were used in the two studies, it is possible that overall sucrose flux from source to sink organs was different between the transformants used in the two experiments, e.g.…”

“…The absence of differences in extra-and intraradical development between SUT1sense and WT plants grown under Low P supply, suggests that under conditions where the host plant relies on the AM symbiosis for P uptake, SUT1sense and WT plants did not differ in the amount of C transferred to the AM symbiosis. Similarly, Schaarschmidt et al (2007a) could not improve AM fungal performance by increasing hexose concentrations in the root apoplast of transgenic tobacco plants with root-specifically enhanced invertase activity. The authors concluded that under conditions of limited plant P availability, WT plant C supply to the AM fungus may already be sufficient for optimal AM development.…”

“…Plants may also exert control over AM fungal development through mechanisms that serve the defense against microbial root invasion, such as the synthesis of antifungal enzymes and metabolites (Garcìa-Garrido and Ocampo, 2002). In addition, plant control of AM development by the amounts of C transferred to the AM fungus has frequently been proposed (Thomson et al, 1986;Graham and Eissenstat, 1994;Olsson et al, 2002;Schaarschmidt et al, 2007a). When AM symbioses established under low P fertilization levels were supplied with additional P, concentrations of AM fungal storage lipids decreased in roots and soil compared with the nonfertilized controls within only three days (Olsson et al, 2010).…”

Photochemical processes, carbon assimilation and RNA accumulation of sucrose transporter genes in tomato arbuscular mycorrhiza

“…Genes encoding apoplastic invertases as well as sucrose synthases are induced in mycorrhized plants and the gene products could be localised in regions of the root cortex where cells are colonised by the fungus (Blee and Anderson, 2002;Hohnjec et al, 2003;Schaarschmidt et al, 2006). Moreover, down regulation of such genes resulted in decreased formation of AM fungal structures in the roots (Schaarschmidt et al, 2007;Baier et al, 2010). Comparison of mycorrhizal with control roots revealed that fructose contents were increased, while glucose contents were not different.…”

Bioactive Molecules in Soil Ecosystems: Masters of the Underground

“…In return, up to 20% of the plant-fixed carbon is transferred to the fungus [27]. Hexoses formed from carbon taken up by the root were found to be the major form of carbohydrates by AMF [45]; however, triacylglycerol is the main form of stored carbon utilized by the mycobiont during all stages of its life cycle [93]. …”