Carbon Export from Arbuscular Mycorrhizal Roots Involves the Translocation of Carbohydrate as well as Lipid

Abstract

(J.W.A., Y.S.-H.) Arbuscular mycorrhizal (AM) fungi take up photosynthetically fixed carbon from plant roots and translocate it to their external mycelium. Previous experiments have shown that fungal lipid synthesized from carbohydrate in the root is one form of exported carbon. In this study, an analysis of the labeling in storage and structural carbohydrates after 13 C 1 glucose was provided to AM roots shows that this is not the only pathway for the flow of carbon from the intraradical to the extraradical mycelium (ERM). Labeling patterns in glycogen, chitin, and trehalose during the development of the symbiosis are consistent with a significant flux of exported glycogen. The identification, among expressed genes, of putative sequences for glycogen synthase, glycogen branching enzyme, chitin synthase, and for the first enzyme in chitin synthesis (glutamine fructose-6-phosphate aminotransferase) is reported. The results of quantifying glycogen synthase gene expression within mycorrhizal roots, germinating spores, and ERM are consistent with labeling observations using 13 C-labeled acetate and glycerol, both of which indicate that glycogen is synthesized by the fungus in germinating spores and during symbiosis. Implications of the labeling analyses and gene sequences for the regulation of carbohydrate metabolism are discussed, and a 4-fold role for glycogen in the AM symbiosis is proposed: sequestration of hexose taken from the host, long-term storage in spores, translocation from intraradical mycelium to ERM, and buffering of intracellular hexose levels throughout the life cycle.The arbuscular mycorrhizal (AM) symbiosis is important because it benefits most land plants. AM plants show enhanced growth, increased resistance to biotic and abiotic stresses, and greater ecological diversity (for review, see Smith and Read, 1997). AMs are also responsible for directing the movement of huge quantities of photosynthate to the soil (for review, see Douds et al., 2000; Graham, 2000). Carbon in the root flows from plant to fungus in the form of sugars (Shachar-Hill et al., 1995; Solaiman and Saito, 1997), and together with the transfer of mineral nutrients from fungus to root (Koide and Schreiner, 1992; George et al., 1995; Jakobsen, 1995), this is the nutritional mainstay of what is arguably the world's most important mutualistic symbiosis.Rather little was known about the forms and pathways through which carbon flows in the AM symbiosis until recently (Jennings, 1995; Smith and Read, 1997). The development of in vitro monoxenic AM root cultures (Mugnier and Mosse, 1987) with separate host and fungal compartments (St. Arnaud et al., 1996) has facilitated the application of stable isotope labeling (Pfeffer et al., 1999), gene expression analysis (Lammers et al., 2001; Bago et al., 2002), in vivo microscopy (Bago et al., 2002), and other methods (for review, see Fortin et al., 2002). Together with previous work on enzyme activities and analysis of metabolites, these approaches have begun to illuminate the metabo...

Influence of arbuscular mycorrhizal colonization on whole‐plant respiration and thermal acclimation of tropical tree seedlings

“…Additionally, rapid turnover of fungal structures and cellular costs of colonization have the potential to increase root respiration (Bago et al. 2003; Staddon et al. 2003).…”

Nuclear-Localized and Deregulated Calcium- and Calmodulin-Dependent Protein Kinase Activates Rhizobial and Mycorrhizal Responses in Lotus japonicus

“…In the arbuscule, nutrients are exchanged across the fungal and plant membranes by transporters (Harrison and van Buuren, 1995;Bago et al, 2003).…”

Effects of Exogenous Putrescine on Mycorrhiza, Root System Architecture, and Physiological Traits of Glomus mosseae-Colonized Trifoliate Orange Seedlings

“…Effects of exogenous Put on sucrose and glucose contents in leaf and root of trifoliate orange seedlings colonized by Glomus mosseae. Data (means ± SE, n=3) followed by the same letter above the bars are not significant difference between various treatments at 5% level to sustain its growth and development (Bago et al, 2003). Through the phloem shoot sucrose is transported down to reach the roots, where the sucrose is rapidly hydrolysed to glucose and fructose (Hammond and White, 2008).…”