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Publications - Cell and Metabolic Biology

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Publications

Krajinski, F.; Courty, P.-E.; Sieh, D.; Franken, P.; Zhang, H.; Bucher, M.; Gerlach, N.; Kryvoruchko, I.; Zoeller, D.; Udvardi, M.; Hause, B.; The H+-ATPase HA1 of Medicago truncatula Is Essential for Phosphate Transport and Plant Growth during Arbuscular Mycorrhizal Symbiosis Plant Cell 26, 1808-1817, (2014) DOI: 10.1105/tpc.113.120436

A key feature of arbuscular mycorrhizal symbiosis is improved phosphorus nutrition of the host plant via the mycorrhizal pathway, i.e., the fungal uptake of Pi from the soil and its release from arbuscules within root cells. Efficient transport of Pi from the fungus to plant cells is thought to require a proton gradient across the periarbuscular membrane (PAM) that separates fungal arbuscules from the host cell cytoplasm. Previous studies showed that the H+-ATPase gene HA1 is expressed specifically in arbuscule-containing root cells of Medicago truncatula. We isolated a ha1-2 mutant of M. truncatula and found it to be impaired in the development of arbuscules but not in root colonization by Rhizophagus irregularis hyphae. Artificial microRNA silencing of HA1 recapitulated this phenotype, resulting in small and truncated arbuscules. Unlike the wild type, the ha1-2 mutant failed to show a positive growth response to mycorrhizal colonization under Pi-limiting conditions. Uptake experiments confirmed that ha1-2 mutants are unable to take up phosphate via the mycorrhizal pathway. Increased pH in the apoplast of abnormal arbuscule-containing cells of the ha1-2 mutant compared with the wild type suggests that HA1 is crucial for building a proton gradient across the PAM and therefore is indispensible for the transfer of Pi from the fungus to the plant.
Publications

Bucher, M.; Hause, B.; Krajinski, F.; Küster, H.; Through the doors of perception to function in arbuscular mycorrhizal symbioses New Phytol. 204, 833-840, (2014) DOI: 10.1111/nph.12862

The formation of an arbuscular mycorrhizal (AM) symbiosis is initiated by the bidirectional exchange of diffusible molecules. While strigolactone hormones, secreted from plant roots, stimulate hyphal branching and fungal metabolism, fungal short‐chain chitin oligomers as well as sulfated and nonsulfated lipochitooligosaccharides (s/nsMyc‐LCOs) elicit pre‐symbiosis responses in the host. Fungal LCO signals are structurally related to rhizobial Nod‐factor LCOs. Genome‐wide expression studies demonstrated that defined sets of genes were induced by Nod‐, sMyc‐ and nsMyc‐LCOs, indicating LCO‐specific perception in the pre‐symbiosis phase. During hyphopodium formation and the subsequent root colonization, cross‐talk between plant roots and AM fungi also involves phytohormones. Notably, gibberellins control arbuscule formation via DELLA proteins, which themselves serve as positive regulators of arbuscule formation. The establishment of arbuscules is accompanied by a substantial transcriptional and post‐transcriptional reprogramming of host roots, ultimately defining the unique protein composition of arbuscule‐containing cells. Based on cellular expression profiles, key checkpoints of AM development as well as candidate genes encoding transcriptional regulators and regulatory microRNAs were identified. Detailed functional analyses of promoters specified short motifs sufficient for cell‐autonomous gene regulation in cells harboring arbuscules, and suggested simultaneous, multi‐level regulation of the mycorrhizal phosphate uptake pathway by integrating AM symbiosis and phosphate starvation response signaling.
Publications

Breuillin, F.; Schramm, J.; Hajirezaei, M.; Ahkami, A.; Favre, P.; Druege, U.; Hause, B.; Bucher, M.; Kretzschmar, T.; Bossolini, E.; Kuhlemeier, C.; Martinoia, E.; Franken, P.; Scholz, U.; Reinhardt, D.; Phosphate systemically inhibits development of arbuscular mycorrhiza in Petunia hybrida and represses genes involved in mycorrhizal functioning Plant J. 64, 1002-1017, (2010) DOI: 10.1111/j.1365-313X.2010.04385.x

Most terrestrial plants form arbuscular mycorrhiza (AM), mutualistic associations with soil fungi of the order Glomeromycota. The obligate biotrophic fungi trade mineral nutrients, mainly phosphate (Pi), for carbohydrates from the plants. Under conditions of high exogenous phosphate supply, when the plant can meet its own P requirements without the fungus, AM are suppressed, an effect which could be interpreted as an active strategy of the plant to limit carbohydrate consumption of the fungus by inhibiting its proliferation in the roots. However, the mechanisms involved in fungal inhibition are poorly understood. Here, we employ a transcriptomic approach to get insight into potential shifts in metabolic activity and symbiotic signalling, and in the defence status of plants exposed to high Pi levels. We show that in mycorrhizal roots of petunia, a similar set of symbiosis‐related genes is expressed as in mycorrhizal roots of Medicago, Lotus and rice. Pi acts systemically to repress symbiotic gene expression and AM colonization in the root. In established mycorrhizal roots, Pi repressed symbiotic gene expression rapidly, whereas the inhibition of colonization followed with a lag of more than a week. Taken together, these results suggest that Pi acts by repressing essential symbiotic genes, in particular genes encoding enzymes of carotenoid and strigolactone biosynthesis, and symbiosis‐associated phosphate transporters. The role of these effects in the suppression of symbiosis under high Pi conditions is discussed.
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