Arbuscular Mycorrhiza–Specific Signaling in Rice Transcends the Common Symbiosis Signaling Pathway

Abstract

Knowledge about signaling in arbuscular mycorrhizal (AM) symbioses is currently restricted to the common symbiosis (SYM) signaling pathway discovered in legumes. This pathway includes calcium as a second messenger and regulates both AM and rhizobial symbioses. Both monocotyledons and dicotyledons form symbiotic associations with AM fungi, and although they differ markedly in the organization of their root systems, the morphology of colonization is similar. To identify and dissect AM-specific signaling in rice (Oryza sativa), we developed molecular phenotyping tools based on gene expression patterns that monitor various steps of AM colonization. These tools were used to distinguish common SYMdependent and -independent signaling by examining rice mutants of selected putative legume signaling orthologs predicted to be perturbed both upstream (CASTOR and POLLUX) and downstream (CCAMK and CYCLOPS) of the central, calciumspiking signal. All four mutants displayed impaired AM interactions and altered AM-specific gene expression patterns, therefore demonstrating functional conservation of SYM signaling between distant plant species. In addition, differential gene expression patterns in the mutants provided evidence for AM-specific but SYM-independent signaling in rice and furthermore for unexpected deviations from the SYM pathway downstream of calcium spiking.

Dating in the dark: how roots respond to fungal signals to establish arbuscular mycorrhizal symbiosis

“…Like the rhizobium-legume symbiosis, Ca2+ oscillations were detected in dmi3 but not in dmi1 and dmi2 Medicago mutants in response to AMFs that support the hierarchical distribution of the SYM pathway with the nuclear kinase DMI3 located downstream as the decoder of the calcium spiking [24 and 30]. On the one hand, it seems evolutionary convenient that the same subset of genes, which are common in plant taxa [ 31] and have been shown to function in mycorrhizal signaling in non-legumes [ 32], could control two diverse biological systems. On the other hand, this common response again raises the problem of specificity: how do legumes distinguish between AMFs and rhizobia and organize the appropriate accommodation of the microbe inside the root tissues?…”

Identification of arbuscular mycorrhiza-inducible Nitrate Transporter 1/Peptide Transporter Family (NPF) genes in rice

“…In the AMF Rhizophagus intraradices (formerly called Glomus intraradices), that is found in rice roots in paddy fields and is used in most AM-rice studies (e.g. Paszkowski et al 2002;Güimil et al 2005;Glassop et al 2007;Gutjahr et al 2008), the ammonium transporters AMT1, AMT2 and AMT3 are expressed in the intraradical mycelium (Lopez-Pedrosa et al 2006;Perez-Tienda et al 2011;Calabrese et al 2016), suggesting a participation in retrieval of NH 4 + leaking from the fungus during fungal metabolism at the symbiotic interface. Alternatively, ammonium released by the AM at this interface may be taken up by the plant.…”

The Genotype of the Calcium/Calmodulin-Dependent Protein Kinase Gene ( CCaMK ) Determines Bacterial Community Diversity in Rice Roots under Paddy and Upland Field Conditions

“…The results make more sense if OsCCaMK is less important under paddy conditions, since CCaMK is essential for arbuscular mycorrhization, which is more likely to occur under upland conditions (3,10).…”

“…The equivalent functionality of these orthologous genes between legumes and nonlegumes has been confirmed (3, 10): among CSP genes of rice, OsCASTOR, OsPOLLUX, and OsCCaMK are involved in mycorrhization in rice roots (3,10). Nonlegumes are ideal materials for examining the effects of CSP genes on plant-associated bacterial communities because they obviate the disturbance of roots by rhizobial infection.…”