A dominant function of CCaMK in intracellular accommodation of bacterial and fungal endosymbionts

Abstract

In legumes, Ca2+/calmodulin-dependent protein kinase (CCaMK) is a component of the common symbiosis genes that are required for both root nodule (RN) and arbuscular mycorrhiza (AM) symbioses and is thought to be a decoder of Ca2+ spiking, one of the earliest cellular responses to microbial signals. A gain-of-function mutation of CCaMK has been shown to induce spontaneous nodulation without rhizobia, but the significance of CCaMK activation in bacterial and/or fungal infection processes is not fully understood. Here we show that a gain-of-function CCaMKT265D suppresses loss-of-function mutations of common symbiosis genes required for the generation of Ca2+ spiking, not only for nodule organogenesis but also for successful infection of rhizobia and AM fungi, demonstrating that the common symbiosis genes upstream of Ca2+ spiking are required solely to activate CCaMK. In RN symbiosis, however, CCaMKT265D induced nodule organogenesis, but not rhizobial infection, on Nod factor receptor (NFRs) mutants. We propose a model of symbiotic signaling in host legume plants, in which CCaMK plays a key role in the coordinated induction of infection thread formation and nodule organogenesis.

Nuclear-Localized and Deregulated Calcium- and Calmodulin-Dependent Protein Kinase Activates Rhizobial and Mycorrhizal Responses in Lotus japonicus

“…In addition, another type of GOF-CCaMK has been identified in Medicago truncatula by truncation of the regulatory domains, resulting in similar phenotypes (Gleason et al, 2006). This indicates that the common Sym pathway is sufficient for activation of cortical cell division and consequent nodule formation in RNS (Hayashi et al, 2010;Madsen et al, 2010). However, the functions of GOF-CCaMK in AMS are largely unknown.…”

“…In previous studies, CCaMK TD , which has the amino acid substitution Thr265Asp (T265D) in wildtype CCaMK (CCaMK TT ), was shown to trigger SPN formation in L. japonicus (Banba et al, 2008;Hayashi et al, 2010), but regulation of symbiosis gene expression downstream of CCaMK TD was not examined. In addition, the functions of truncated CCaMK lacking the regulatory domains were not tested in L. japonicus.…”

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

“…2A and B and 3A and B). The CCaMK protein has a dominant function in nodule organogenesis and in successful infection for both RN and AM symbioses in legumes (13). Therefore, the OsCCaMK heterozygous genotype may have less of an impact on rhizobial and arbuscular mycorrhizal infections, but it may have some effects on other plant-associated bacteria.…”

“…S1 in the supplemental material) implies its importance in rice. CCaMK is thought to be a decoder of Ca spiking signals, a distinctive physiological response to endosymbioses (13,24), because of its structural similarity to CaMKII, which is activated by Ca oscillation in a frequencydependent manner in animals (4).…”

Cell autonomous and non-cell autonomous control of rhizobial and mycorrhizal infection inMedicago truncatula

“…This would be consistent with the fact that, in Lotus japonicus, spontaneous nodules obtained with autoactive forms of CCaMK cannot be infected via root hairs in the double NF receptor mutant nfr1/nfr5. 16,17 This, together with the fact that NFs are not thought to penetrate into inner root tissues, suggests that the control of infection by signaling from cortical NFP is unlikely to involve NFs.…”