Intracellular arbuscular mycorrhiza symbiosis between plants and glomeromycotan fungi leads to formation of highly branched fungal arbuscules that release mineral nutrients to the plant host. Their development is regulated in plants by a mechanistically unresolved interplay between symbiosis, nutrient, and hormone (gibberellin) signaling. Using a positional cloning strategy and a retrotransposon insertion line, we identify two novel alleles of Lotus japonicus REDUCED ARBUSCULAR MYCORRHIZA1 (RAM1) encoding a GRAS protein. We confirm that RAM1 is a central regulator of arbuscule development: arbuscule branching is arrested in L. japonicus ram1 mutants, and ectopic expression of RAM1 activates genes critical for arbuscule development in the absence of fungal symbionts. Epistasis analysis places RAM1 downstream of CCaMK, CYCLOPS, and DELLA because ectopic expression of RAM1 restores arbuscule formation in cyclops mutants and in the presence of suppressive gibberellin. The corresponding proteins form a complex that activates RAM1 expression via binding of CYCLOPS to a cis element in the RAM1 promoter. We thus reveal a transcriptional cascade in arbuscule development that employs the promoter of RAM1 as integrator of symbiotic (transmitted via CCaMK and CYCLOPS) and hormonal (gibberellin) signals.
Arbuscular mycorrhiza (AM) is a widespread symbiosis between roots of the majority of land plants and Glomeromycotina fungi. AM is important for ecosystem health and functioning as the fungi critically support plant performance by providing essential mineral nutrients, particularly the poorly accessible phosphate, in exchange for organic carbon. AM fungi colonize the inside of roots and this is promoted at low but inhibited at high plant phosphate status, while the mechanistic basis for this phosphate-dependence remained obscure. Here we demonstrate that a major transcriptional regulator of phosphate starvation responses in rice PHOSPHATE STARVATION RESPONSE 2 (PHR2) regulates AM. Root colonization of phr2 mutants is drastically reduced, and PHR2 is required for root colonization, mycorrhizal phosphate uptake, and yield increase in field soil. PHR2 promotes AM by targeting genes required for pre-contact signaling, root colonization, and AM function. Thus, this important symbiosis is directly wired to the PHR2-controlled plant phosphate starvation response.
Phosphate (P i ) is indispensable for life on this planet. However, for sessile land plants it is poorly accessible. Therefore, plants have developed a variety of strategies for enhanced acquisition and recycling of P i . The mechanisms to cope with P i limitation as well as direct uptake of P i from the substrate via the root epidermis are regulated by a conserved P i starvation response (PSR) system based on a family of key transcription factors (TFs) and their inhibitors. Furthermore, plants obtain P i indirectly through symbiosis with mycorrhiza fungi, which employ their extensive hyphal network to drastically increase the soil volume that can be explored by plants for P i . Besides mycorrhizal symbiosis, there is also a variety of other interactions with epiphytic, endophytic, and rhizospheric microbes that can indirectly or directly influence plant P i uptake. It was recently discovered that the PSR pathway is involved in the regulation of genes that promote formation and maintenance of AM symbiosis. Furthermore, the PSR system influences plant immunity and can also be a target of microbial manipulation. It is known for decades that the nutritional status of plants influences the outcome of plant-microbe interactions. The first molecular explanations for these observations are now emerging.
Arbuscular mycorrhiza (AM) is a widespread symbiosis between roots of the majority of land plants and Glomeromycotina fungi. AM is important for ecosystem health and functioning as the fungi critically support plant performance by providing essential mineral nutrients, particularly the poorly accessible phosphate, in exchange for organic carbon. AM fungi colonize the inside of roots and this is promoted at low but inhibited at high plant phosphate status, while the mechanistic basis for this phosphate-dependence remained obscure. Here we demonstrate that a major transcriptional regulator of phosphate starvation responses in rice PHOSPHATE STARVATION RESPONSE 2 (PHR2) regulates AM. Root colonization of phr2 mutants is drastically reduced, and PHR2 is required for root colonization, mycorrhizal phosphate uptake, and yield increase in field soil. PHR2 promotes AM by targeting genes required for pre-contact signaling, root colonization, and AM function. Thus, this important symbiosis is directly wired to the PHR2-controlled plant phosphate starvation response.
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