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. 2008 Mar 25;105(12):4928-32.
doi: 10.1073/pnas.0710618105. Epub 2008 Mar 3.

SymRK defines a common genetic basis for plant root endosymbioses with arbuscular mycorrhiza fungi, rhizobia, and Frankiabacteria

Hassen Gherbi  1 , Katharina Markmann, Sergio Svistoonoff, Joan Estevan, Daphné Autran, Gabor Giczey, Florence Auguy, Benjamin Péret, Laurent Laplaze, Claudine Franche, Martin Parniske, Didier Bogusz
Affiliations

SymRK defines a common genetic basis for plant root endosymbioses with arbuscular mycorrhiza fungi, rhizobia, and Frankiabacteria

Hassen Gherbi et al. Proc Natl Acad Sci U S A. .

Abstract

Root endosymbioses vitally contribute to plant nutrition and fitness worldwide. Nitrogen-fixing root nodulation, confined to four plant orders, encompasses two distinct types of associations, the interaction of legumes (Fabales) with rhizobia bacteria and actinorhizal symbioses, where the bacterial symbionts are actinomycetes of the genus Frankia. Although several genetic components of the host-symbiont interaction have been identified in legumes, the genetic basis of actinorhiza formation is unknown. Here, we show that the receptor-like kinase gene SymRK, which is required for nodulation in legumes, is also necessary for actinorhiza formation in the tree Casuarina glauca. This indicates that both types of nodulation symbiosis share genetic components. Like several other legume genes involved in the interaction with rhizobia, SymRK is also required for the interaction with arbuscular mycorrhiza (AM) fungi. We show that SymRK is involved in AM formation in C. glauca as well and can restore both nodulation and AM symbioses in a Lotus japonicus symrk mutant. Taken together, our results demonstrate that SymRK functions as a vital component of the genetic basis for both plant-fungal and plant-bacterial endosymbioses and is conserved between legumes and actinorhiza-forming Fagales.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.
C. glauca SymRK gene. (A) Genomic structure of CgSymRK with indicated predicted protein domains. Exons are depicted as boxes, introns as a black line. SP, predicted signal peptide; EC, extracellular domain; LRR leucine-rich repeat motifs; TM, transmembrane domain; PK, protein kinase domain. Percentages of similarity and identity between CgSYMRK and LjSYMRK are indicated below each predicted protein domain. (B) Distance tree of predicted SYMRK protein sequences based on a CLUSTALW alignement. Numbers above the branches represent the percentages of 1,000 bootstrap replications.
Fig. 2.
Fig. 2.
Knockdown phenotype of CgSymRK after Frankia inoculation. (A) Nontransgenic nodule consisting of multiple lobes 10 weeks postinoculation (wpi). A nodular root develops at the apex of each nodule lobe. (B) Nodule on a hairy root transformed with a control vector at 10 wpi. Nodule morphology is similar to wild-type nodules. (C) Nodule-like structure formed on CgSymRK knockdown (RNAi) roots 10 wpi. Nodule lobes are small and do not branch to form a multilobed structure. (D and E) Sections of wild-type and transgenic control nodules. Each nodule lobe exhibits a central vascular bundle and cortical parenchyma infected with Frankia. (F) Section of a nodule-like structure observed on an RNAi plant showing few small infected cells and abnormal accumulation of polyphenols in the endodermis. (G) Closeup of area in D, showing both infected and uninfected cortical cells. Infected cells are hypertrophied and filled with Frankia. (H) Closeup of area in E. As in nontransgenic nodules, hypertrophied cortical cells are filled with Frankia. (I) Closeup of area in F. Infected cells are few and small compared with cells in nontransgenic and transgenic control nodules. IC, infected cell with Frankia; RN, root nodule; NA, nodule apex; VT, vascular tissue; P, polyphenol droplets; RH, root hair. [Scale bars: 1 mm (A–C); 100 μm (D–F); 25 μm (G–I).]
Fig. 3.
Fig. 3.
AM formation in L. japonicus symrk-10 mutants complemented with the CgSymRK coding sequence under control of the LjSymRK promoter, after 3 weeks of cocultivation with G. intraradices. Cleared roots with fungal structures are stained with acidic ink. (A and B) symrk-10 roots transformed with a control vector. (A) Noncolonized root with extraradical mycelium and aborted infection structure (arrow). (B) Fungal appressorium and entry point associated with aborted infection structure within host epidermal cell. (C and D) Wild-type and (E and F) symrk-10 roots transformed with CgSymRK linked to the LjSymRK promoter. Fungal hyphae grow through epidermis and exodermis and form arbuscules and vesicles in the inner root cortex. A, arbuscule; IH, intraradical hyphae; V, vesicle. [Scale bars: 100 μm (A, C, and E); 20 μm (B, D, and F).]
Fig. 4.
Fig. 4.
Nodulation in L. japonicus symrk-10 mutants complemented with the CgSymRK coding sequence under control of the LjSymRK promoter, 8 weeks after inoculation with M. loti MAFF expressing DsReD. Transgenic roots carried an sGFP reporter gene. (A, C, and F) Roots and nodules under white light. (B, D, and G) Transgenic roots and nodules showing GFP fluorescence. (E and H) Red fluorescence of bacterial DsRED. (A and B) symrk-10 root transformed with the control vector, showing no nodules. (C–E) Transgenic wild-type root carrying the CgSymRK coding sequence. Nodules contain DsReD-expressing bacteria (E). (F–H) symrk-10 mutant root transformed with the CgSymRK coding sequence, carrying wild-type-like nodules. (I–L) Semithin sections of nodules stained with toluidine blue. (I and J) Nodules on symrk-10 mutant and wild-type roots complemented with the CgSymRK coding sequence, respectively. (K and L) Nodules on symrk-10 mutant and wild-type roots complemented with the LjSymRK coding sequence, respectively. Infection threads (IT) are contained within bacteria-infected cells (IC). [Scale bars: 500 μm (A–H); 25 μm (I–L).]
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