Fungal Symbiosis in Rice Requires an Ortholog of a Legume Common Symbiosis Gene Encoding a Ca²⁺/Calmodulin-Dependent Protein Kinase

Abstract

In natural ecosystems, many plants are able to establish mutually beneficial symbioses with microorganisms. Of critical importance to sustainable agriculture are the symbioses formed between more than 80% of terrestrial plants and arbuscular mycorrhizal (AM) fungi and between legumes and nitrogen-fixing rhizobial bacteria. Interestingly, the two symbioses share overlapping signaling pathways in legumes, suggesting that the evolutionarily recent root nodule symbiosis may have acquired functions from the ancient AM symbiosis. The Medicago truncatula DMI3 (DOESN'T MAKE INFECTIONS3) gene (MtDMI3) and its orthologs in legumes are required for both bacterial and fungal symbioses. MtDMI3 encodes a Ca 21 / calmodulin-dependent protein kinase (CCaMK) essential for the transduction of the Ca 21 signal induced by the perception of Nod factors. Putative orthologs of MtDMI3 are also present in non-legumes, but their function in AM symbiosis has not been demonstrated in any non-legume species. Here, we combine reverse genetic approaches and a cross-species complementation test to characterize the function of the rice (Oryza sativa) ortholog of MtDMI3, namely, OsDMI3, in AM symbiosis. We demonstrate that OsDMI3 is not only required for AM symbiosis in rice but also is able to complement a M. truncatula dmi3 mutant, indicating an equivalent role of MtDMI3 orthologs in non-legumes.

Antiquity and Function ofCASTORandPOLLUX, the Twin Ion Channel-Encoding Genes Key to the Evolution of Root Symbioses in Plants

“…As part of our effort to address the function of nonlegume orthologs of legume genes required for root symbioses, we seek to determine whether the common symbiosis genes in legumes also are required for mycorrhizal symbioses in nonlegumes using rice (Oryza sativa) as a study model. We as well as others have demonstrated that Os-DMI3, the rice ortholog of Mt-DMI3/ Lj-CCaMK/Ps-SYM9, is required for AM symbiosis in rice and able to complement a M. truncatula dmi3 mutant (Godfroy et al, 2006;Chen et al, 2007). Two recent studies revealed that the Mt-DMI2/Ms-NORK/ Lj-SYMRK/Ps-SYM19 orthologs from the two actinorhizal plants, Casuarina glauca and Datisca glomerata, are Figure 1.…”

Flowers and mycorrhizal roots – closer than we think?

“…Subsequent work showed that the AM-related function of CCaMK and its expression in flowers are conserved in rice (Oryza sativa) [29,30]. The function of CCaMK in symbiosis is thought to be the decoding of a calcium signal (calcium spiking) in root cells that have perceived AM fungal or rhizobial signals (reviewed in [6]).…”

A Rice Gene for Microbial Symbiosis, Oryza sativa CCaMK , Reduces CH 4 Flux in a Paddy Field with Low Nitrogen Input

“…Legume CCaMK is a key player in the coordinated induction of infection thread formation and nodule organogenesis (7), providing fixed nitrogen in exchange for plant photosynthates as energy (5,8). Orthologs of CSP genes, including CCaMK, are also well conserved in nonleguminous plants (9,10). The Oryza sativa CCaMK (OsCCaMK) genes were strongly expressed in the roots of field-grown rice at the vegetative and reproductive stages (11); such expression is required for mycorrhization (9,12).…”