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

Department of Plant and Soil Sciences, University of Kentucky, Lexington, Kentucky 40546, USA.
Plant physiology (Impact Factor: 6.84). 01/2008; 145(4):1619-28. DOI: 10.1104/pp.107.109876
Source: PubMed

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(2+)/calmodulin-dependent protein kinase (CCaMK) essential for the transduction of the Ca(2+) 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.

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    • "There is no explanation given for this observation in NC2713, but it is assumed that the observed aborted hyphae did not confer functionality of the symbiosis. Chen et al. (2008) noted that the colonisation phenotype displayed by the OsIPD3 mutants was comparable to that of the previously identified OsDMI3 mutant genotype (Chen et al. 2007). "
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    ABSTRACT: A significant challenge facing the study of arbuscular mycorrhiza is the establishment of suitable non-mycorrhizal treatments that can be compared with mycorrhizal treatments. A number of options are available, including soil disinfection or sterilisation, comparison of constitutively mycorrhizal and non-mycorrhizal plant species, comparison of plants grown in soils with different inoculum potential and the comparison of mycorrhiza-defective mutant genotypes with their mycorrhizal wild-type progenitors. Each option has its inherent advantages and limitations. Here, the potential to use mycorrhiza-defective mutant and wild-type genotype plant pairs as tools to study the functioning of mycorrhiza is reviewed. The emphasis of this review is placed on non-legume plant species, as mycorrhiza-defective plant genotypes in legumes have recently been extensively reviewed. It is concluded that non-legume mycorrhiza-defective mutant and wild-type pairs are useful tools in the study of mycorrhiza. However, the mutant genotypes should be well characterised and, ideally, meet a number of key criteria. The generation of more mycorrhiza-defective mutant genotypes in agronomically important plant species would be of benefit, as would be more research using these genotype pairs, especially under field conditions.
    Mycorrhiza 04/2015; DOI:10.1007/s00572-015-0639-2 · 3.46 Impact Factor
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    • "CCaMK are highly conserved in plants, including M. truncatula, L. japonicus, and Sesbania rostrata (Capoen et al. 2009; Godfroy et al. 2006; Lévy et al. 2004; Poovaiah et al. 1999; Tirichine et al. 2006). Rice CCaMK is required for AMS and can also functionally complement legume CCaMK knock-out mutations, indicating an equivalent role of CCaMK homologs in nonlegumes (Chen et al. 2007; Godfroy et al. 2006). "
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    ABSTRACT: The calcium/calmodulin-dependent protein kinase CCaMK forms a complex with its phosphorylation target CIP73 (for CCaMK- interacting protein of 73 kDa). In this work, a homolog of the animal HSC/HSP70 interacting protein HIP was identified as an interacting partner of CIP73 in Lotus japonicus. Lj HIP contains all functional domains characteristic of animal HIP proteins. The C-terminal STI1-like domain of Lj HIP was found to be necessary and sufficient for interaction with CIP73. The interaction between CIP73 and HIP occurred in both the nuclei and cytoplasm in Nicotiana benthamiana leaf cells. The interactions between CIP73 and HIP and between CIP73 and CCaMK could take place simultaneously in the same nuclei. HIP transcripts were detected in all plant tissues tested. As nodule primordia developed into young nodules, the expression of HIP was down-regulated and the HIP transcript level became very low in mature nodules. More nodules were formed in transgenic hairy roots of L. japonicus expressing HIP RNA interference (RNAi) at 16 days post inoculation as compared to the control hairy roots expressing the empty vector. It appears that HIP may play a role as a negative regulator for nodulation.
    Molecular Plant-Microbe Interactions 03/2015; 28(5). DOI:10.1094/MPMI-11-14-0354-R · 3.94 Impact Factor
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    • "Sequence analysis revealed that CgCCaMK has all the features of other plant CCaMKs. We found that CgCCaMK is able to fully complement the M. truncatula dmi3 mutant for mycorrhization and that downregulation of CgCCaMK strongly affects AM interaction, confirming the results of previous studies on legumes and rice ([28]. Recently, the mycorrhization phenotype of dmi3 mutants was fully complemented with CCaMK genes from hornworts and liverworts, two lineages that diverged from legumes more than 400 MY ago, suggesting that a strong selective pressure probably related to the widespread occurrence of AM associations among land plants maintained the key ancestral features of CCaMK [29]. "
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    ABSTRACT: Only species belonging to the Fabid clade, limited to four classes and ten families of Angiosperms, are able to form nitrogen-fixing root nodule symbioses (RNS) with soil bacteria. This concerns plants of the legume family (Fabaceae) and Parasponia (Cannabaceae) associated with the Gram-negative proteobacteria collectively called rhizobia and actinorhizal plants associated with the Gram-positive actinomycetes of the genus Frankia. Calcium and calmodulin-dependent protein kinase (CCaMK) is a key component of the common signaling pathway leading to both rhizobial and arbuscular mycorrhizal symbioses (AM) and plays a central role in cross-signaling between root nodule organogenesis and infection processes. Here, we show that CCaMK is also needed for successful actinorhiza formation and interaction with AM fungi in the actinorhizal tree Casuarina glauca and is also able to restore both nodulation and AM symbioses in a Medicago truncatula ccamk mutant. Besides, we expressed auto-active CgCCaMK lacking the auto-inhibitory/CaM domain in two actinorhizal species: C. glauca (Casuarinaceae), which develops an intracellular infection pathway, and Discaria trinervis (Rhamnaceae) which is characterized by an ancestral intercellular infection mechanism. In both species, we found induction of nodulation independent of Frankia similar to response to the activation of CCaMK in the rhizobia-legume symbiosis and conclude that the regulation of actinorhiza organogenesis is conserved regardless of the infection mode. It has been suggested that rhizobial and actinorhizal symbioses originated from a common ancestor with several independent evolutionary origins. Our findings are consistent with the recruitment of a similar genetic pathway governing rhizobial and Frankia nodule organogenesis.
    PLoS ONE 05/2013; 8(5):e64515. DOI:10.1371/journal.pone.0064515 · 3.23 Impact Factor
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