Many plants have the capacity to obtain phosphate via a symbiotic association with arbuscular mycorrhizal (AM) fungi. In AM associations, the fungi release phosphate from differentiated hyphae called arbuscules, that develop within the cortical cells, and the plant transports the phosphate across a symbiotic membrane, called the periarbuscular membrane, into the cortical cell. In Medicago truncatula , a model legume used widely for studies of root symbioses, it is apparent that the phosphate transporters known to operate at the root-soil interface do not participate in symbiotic phosphate transport. EST database searches with short sequence motifs shared by known phosphate transporters enabled the identification of a novel phosphate transporter from M. truncatula , MtPT4. MtPT4 is significantly different from the plant root phosphate transporters cloned to date. Complementation of yeast phosphate transport mutants indicated that MtPT4 functions as a phosphate transporter, and estimates of the K m suggest a relatively low affinity for phosphate. MtPT4 is expressed only in mycorrhizal roots, and the MtPT4 promoter directs expression exclusively in cells containing arbuscules. MtPT4 is located in the membrane fraction of mycorrhizal roots, and immunolocalization revealed that MtPT4 colocalizes with the arbuscules, consistent with a location on the periarbuscular membrane. The transport properties and spatial expression patterns of MtPT4 are consistent with a role in the acquisition of phosphate released by the fungus in the AM symbiosis.

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The formation of symbiotic associations with arbuscular mycorrhizal (AM) fungi is a phenomenon common to the majority of vascular flowering plants. Here, we used cDNA arrays to examine transcript profiles in Medicago truncatula roots during the development of an AM symbiosis with Glomus versiforme and during growth under differing phosphorus nutrient regimes. Three percent of the genes examined showed significant changes in transcript levels during the development of the symbiosis. Most genes showing increased transcript levels in mycorrhizal roots showed no changes in response to high phosphorus, suggesting that alterations in transcript levels during symbiosis were a consequence of the AM fungus rather than a secondary effect of improved phosphorus nutrition. Among the mycorrhiza-induced genes, two distinct temporal expression patterns were evident. Members of one group showed an increase in transcripts during the initial period of contact between the symbionts and a subsequent decrease as the symbiosis developed. Defense- and stress-response genes were a significant component of this group. Genes in the second group showed a sustained increase in transcript levels that correlated with the colonization of the root system. The latter group contained a significant proportion of new genes similar to components of signal transduction pathways, suggesting that novel signaling pathways are activated during the development of the symbiosis. Analysis of the spatial expression patterns of two mycorrhiza-induced genes revealed distinct expression patterns consistent with the hypothesis that gene expression in mycorrhizal roots is signaled by both cell-autonomous and cell-nonautonomous signals.

SummaryIn natural ecosystems, the roots of many plants exist in association with arbuscular mycorrhizal (AM) fungi, and the resulting symbiosis has profound effects on the plant. The most frequently documented response is an increase in phosphorus nutrition; however, other effects have been noted, including increased resistance to abiotic and biotic stresses. Here we used a 16 000-feature oligonucleotide array and real-time quantitative RT-PCR to explore transcriptional changes triggered in Medicago truncatula roots and shoots as a result of AM symbiosis. By controlling the experimental conditions, phosphorus-related effects were minimized, and both local and systemic transcriptional responses to the AM fungus were revealed. The transcriptional response of the roots and shoots differed in both the magnitude of gene induction and the predicted functional categories of the mycorrhiza-regulated genes. In the roots, genes regulated in response to three different AM fungi were identified, and, through split-root experiments, an additional layer of regulation, in the colonized or noncolonized sections of the mycorrhizal root system, was uncovered. Transcript profiles of the shoots of mycorrhizal plants indicated the systemic induction of many genes predicted to be involved in stress or defense responses, and suggested that mycorrhizal plants might display enhanced disease resistance. Experimental evidence supports this prediction, and mycorrhizal M. truncatula plants showed increased resistance to a virulent bacterial pathogen, Xanthomonas campestris. Thus, the symbiosis is accompanied by a complex pattern of local and systemic changes in gene expression, including the induction of a functional defense response.