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


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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    • "OsCASTOR Os03g0843600 Cation ion channel Oscastor-1 (1B-08643 *4 ) M y c − Ljcastor: Nod + Fix + Ljcastor:Myc + Banba et al. (2008) Gutjahr et al. (2008) Chen et al. (2009) OsPOLLUX Os01g0870100 Cation ion channel Ospollux-1 (1C-03411 *4 ) M y c − Ljpollux: Nod ± Fix − Ljpollux: Myc ± Banba et al. (2008) Ospollux-2 (NC6423 *5 ) Mtdmi1: Nod + Fix − Mtdmi1: Myc + Gutjahr et al. (2008) Ospollux-3 (ND5050 *5 ) Chen et al. (2009) OsCCaMK/OsDMI3 Os05g0489900 Ca 2+ /CaM-dependent protein kinase Osccamk-1 (NE1115 *5 ) M y c − Ljccamk: Nod + Fix + /Spn + Ljccamk: Myc + Godfroy et al. (2006) Osccamk-2 (NF8513 *5 ) OsDMI3-i (RNAi) Mtdmi3: Nod + Fix − Mtdmi3: Myc + Chen et al. (2007) Banba et al. (2008) Gutjahr et al. (2008) OsCYCLOPS/OsIPD3 Os06g0115600 interacting protein of CCaMK Oscyclops-1 (NG0782 *5 ) M y c − Ljcyclops: Nod + Fix + Ljcyclops:Myc + Yano et al. (2008) Oscyclops-2 (NC2415 *5 ) Gutjahr et al. (2008) Oscyclops-3 (NC2713 *5 ) Chen et al. (2008) ND5032 *5 NC0263 *5 NC2794 *5 OsNSP1 Os03g0408600 GRAS TF no hit *3 - Ljnsp1: Nod + Fix + - Yokota et al. (2010) OsNSP2 Os03g0263300 GRAS TF no hit *3 - Ljnsp2: Nod + Fix + n/a *9 Yokota et al. (2010) OsPT11 Os01g0657100 Phosphate transporter Ospt11-1 *4 Low mycorrhizaion (small arbuscules) - - Yang et al. (2012) Ospt11R1 (RNAi) OsPT13 Os04g0186800 Phosphate transporter Ospt13-1 *7 Low mycorrhizaion (small arbuscules) - - Yang et al. (2012) Ospt13R1 (RNAi) OsSTR1 Os09g0401100 half-size ABC transporter str1-1 (1C-04850 *4 ) Small and stunted arbuscules in cortex - - Gutjahr et al. (2012) str1-2 (CL522472 *6 ) OsSTR2 Os07g0191600 half-size ABC transporter str-2-1 (RdSpm2654D *7 ) Small and stunted arbuscules in cortex - - Gutjahr et al. (2012) "
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    ABSTRACT: Rice (Oryza sativa L.) is a monocot model crop for cereal molecular biology. Following the emergence of molecular genetics of arbuscular mycorrhizal (AM) symbiosis in model legumes in the 1990s, studies on rice genetic resources have considerably contributed to our understanding of the molecular mechanisms and evolution of root intracellular symbioses. In this review, we trace the history of these studies and suggest the potential utility of AM symbiosis for improvement in rice productivity.
    Full-text · Article · Oct 2015 · Rice
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    • "All components described here are part of the common symbiotic pathway, which are also required for a symbiotic interaction between plants and rhizobia (Oldroyd 2013). Plants with impaired CCaMK expression have been shown to be unable to form a functional symbiosis between rhizobia/AMF and several legumes and rice (Levy et al. 2004; Mitra et al. 2004; Chen et al. 2007). When inoculated with Rhizophagus irregularis, Funelliformis mosseae or Gigaspora spp. "
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    ABSTRACT: While the biochemical function of calcium and calmodulin-dependent protein kinase (CCaMK) is well studied, and plants impaired in the expression of CCaMK are known not to be infected by arbuscular mycorrhizal fungi (AMF) in glasshouse studies, the whole-plant and ecological consequences of CCaMK silencing are not well understood. Here we show that three independently transformed lines of Nicotiana attenuata plants silenced in CCaMK (irCCaMK) are neither infected by Rhizophagus irregularis in the glasshouse nor by native fungal inoculum in the field. The overall fungal community of field-grown roots did not differ significantly among empty vector (EV) and the transgenic lines, and the bacterial communities only showed minor differences, as revealed by the alpha diversity parameters of bacterial OTUs, which were higher in EV plants compared to two of the three transformed lines, while beta-diversity parameters did not differ. Furthermore, growth and fitness parameters were similar in the glasshouse and field. Herbivory-inducible and basal levels of salicylic acid, jasmonic acid and abscisic acid did not differ amongst the genotypes, suggesting that activation of the classical defense pathways are not affected by CCaMK silencing. Based on these results we conclude that silencing of CCaMK has few, if any, non-target effects. This article is protected by copyright. All rights reserved.
    Full-text · Article · Apr 2015 · Plant Cell and Environment
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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.
    Full-text · Article · Apr 2015 · Mycorrhiza
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