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Identification of Bradyrhizobium Elkanii USDA61 Type III Effectors

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Identification of Bradyrhizobium Elkanii USDA61 Type III Effectors G C A T T A C G G C A T genes Article Identification of Bradyrhizobium elkanii USDA61 Type III Effectors Determining Symbiosis with Vigna mungo 1, 2 3 4 Hien P. Nguyen y , Safirah T. N. Ratu , Michiko Yasuda , Neung Teaumroong and Shin Okazaki 2,3,* 1 Institute of Global Innovation Research (IGIR), Tokyo University of Agriculture and Technology (TUAT), Fuchu, Tokyo 183-8538, Japan; [email protected] 2 United Graduate School of Agricultural Science, TUAT, Fuchu, Tokyo 183-8509, Japan; safi[email protected] 3 Graduate School of Agriculture, TUAT, Fuchu, Tokyo 183-8509, Japan; [email protected] 4 School of Biotechnology, Institute of Agricultural Technology, Suranaree University of Technology (SUT), Ratchasima 30000, Thailand; [email protected] * Correspondence: [email protected]; Tel./Fax: +81-42-367-5847 Present address: Beltsville Agricultural Research Center (BARC), Agricultural Research Service (ARS), y the U.S. Department of Agriculture (USDA), Beltsville, MD 20705, USA. Received: 11 March 2020; Accepted: 24 April 2020; Published: 27 April 2020 Abstract: Bradyrhizobium elkanii USDA61 possesses a functional type III secretion system (T3SS) that controls host-specific symbioses with legumes. Here, we demonstrated that B. elkanii T3SS is essential for the nodulation of several southern Asiatic Vigna mungo cultivars. Strikingly, inactivation of either Nod factor synthesis or T3SS in B. elkanii abolished nodulation of the V. mungo plants. Among the effectors, NopL was identified as a key determinant for T3SS-dependent symbiosis. Mutations of other effector genes, such as innB, nopP2, and bel2-5, also impacted symbiotic effectiveness, depending on host genotypes. The nopL deletion mutant formed no nodules on V. mungo, but infection thread formation was still maintained, thereby suggesting its pivotal role in nodule organogenesis. Phylogenetic analyses revealed that NopL was exclusively conserved among Bradyrhizobium and Sinorhizobium (Ensifer) species and showed a different phylogenetic lineage from T3SS. These findings suggest that V. mungo evolved a unique symbiotic signaling cascade that requires both NFs and T3Es (NopL). Keywords: symbiosis; T3SS; effectors; NopL; Vigna mungo; Bradyrhizobium elkanii 1. Introduction Bacteria have continuously evolved a multitude of strategies to promote infections in their hosts, including the direct injection of proteins via protein secretion systems. Numerous Gram-negative pathogenic bacteria employ a type III secretion system (T3SS) to translocate their virulence effector proteins (hereafter T3Es) directly into host cells to promote infection and pathogenesis [1]. Similarly, rhizobia, nitrogen-fixing bacteria inducing nodules on leguminous plants, have adopted such a system for symbiotic purposes [2–6]. Rhizobial T3SS-secreted proteins, called nodulation outer proteins (Nops), are injected into host cells as T3Es depending on an extracellular secretion apparatus [7]. Once translocated, some T3Es modulate host functions toward promoting infection and symbiosis with legumes [6], while several T3Es may be recognized as asymbiotic factors directly or indirectly via host resistance (R) proteins or specific receptors, consequently triggering immune responses that restrict nodulation [7]. Genes 2020, 11, 474; doi:10.3390/genes11050474 www.mdpi.com/journal/genes Genes 2020, 11, 474 2 of 14 Bradyrhizobium elkanii USDA61 (hereafter USDA61), first isolated from the soybean [8], possesses a functional T3SS controlling host-specific symbiosis with legumes [9]. Among the T3SS-secreted proteins, at least eight, including NopA, NopB, NopC, NopX, NopL, NopP, Bel2-5, and InnB, have been confirmed by extracellular protein and immunodetection analyses [9–11]. Three of them (NopA, B, and X) are required for T3SS components, protein secretions, and translocations [12]. In contrast, NopC, NopL, NopP, InnB, and Bel2-5 are characterized among rhizobial strains as functioning T3Es in plant cells [9,10,13]. Our previous studies demonstrate that InnB is a novel rhizobium-specific effector that functions negatively or positively in symbioses with Vigna radiata and Vigna mungo, respectively. However, the mutation of innB resulted in symbiotic phenotypes significantly different to those of the T3SS-deficient mutant [9]. The innB mutant induced fewer nodules and less plant biomass on V. mungo cv. PI173934 than USDA61 did, whereas the inactivation of T3SS more fully abolished nodulation [9]. However, symbiotic implications of B. elkanii T3SS among V. mungo cultivars and other Vigna species remain unclear. In this study, we further characterized the roles of bradyrhizobial T3SS as a determinant for symbiosis with V. mungo cultivars. Our results revealed that B. elkanii T3SS is essential for nodulating at least two South Asiatic V. mungo cultivars. Furthermore, T3SS-triggered symbiosis relied on a T3E cocktail, in which NopL served as the key player required for establishing early infections and nodule organogenesis. 2. Materials and Methods 2.1. Microbiological and Molecular Techniques The bacterial strains used in this study are shown in Table1 and Table S1. Rhizobia and Escherichia coli were grown as described previously [9]. Briefly, rhizobial and Escherichia coli strains were cultured using arabinose–gluconate (AG) [14] and Luria–Bertani (LB) media, respectively. Antibiotics were supplemented to the media or agar plates with appropriate concentrations when required for the 1 culture and selection of mutants. For rhizobial strains, polymyxin (Pol) at 50 µg mL− , kanamycin 1 1 (Km) and streptomycin (Sm) at 200 µg mL− , and spectinomycin (Sp) at 100 µg mL− . For E. coli strains, 1 Km, Sm, and Sp at 50 µg mL− . The primer sets used for rhizobial mutant constructions are detailed in Table S2. Single-crossover homologous recombination was conducted as described previously [15]. For double-crossover homologous recombination [16], the single deletion mutants of the effector genes were constructed by overlap extension PCR using two primer pairs amplifying the upstream and downstream fragments flanking the genes of interest, respectively. The PCR fragments were then cloned into the plasmid pK18mobsac derived from pK18mob [17] and linearized by EcoRI and HindIII restriction enzymes. The plasmid derivatives were transformed into rhizobia via triparental conjugations [18]. Similarly, double gene deletion mutants were constructed using the single deletion mutants as the backgrounds. The mutants were finally verified by antibiotic resistance, PCR, and inoculation assays. Genes 2020, 11, 474 3 of 14 Table 1. Bradyrhiozbium elkanii strains used for inoculation tests. Strains Characteristics a References USDA61 Wild-type strain, Polr USDA b USDA61 derivative harboring insertion in rhcJ encoding a BErhcJ membrane protein of the type III secretion apparatus, [11] defective in type III protein secretion, Polr, Kmr, Tcr USDA61 derivative harboring insertion in nodC gene, Polr, BEnodC [19] Kmr, Tcr USDA61 derivative harboring insertion in ttsI and nodC genes, BEttsInod [19] Polr, Kmr, Smr, Tcr USDA61 derivative with the nopL gene deleted via BEnopL This study double-crossover, Polr USDA61 derivative harboring insertion of the plasmid BEnopP1 pSUPSCAKm::nopP1 in the nopP1 gene via single-crossover, This study Polr, Kmr USDA61 derivative with the nopP2 gene deleted via BEnopP2 This study double-crossover, Polr USDA61 derivative with the bel2-5 gene deleted via BE5208 This study double-crossover, Polr USDA61 derivative with the innB gene deleted via BEinnB This study double-crossover, Polr USDA61 derivative with the nopL gene deleted via BEnopL This study double-crossover, Polr USDA61 derivative harboring insertion of the plasmid BEnopP1 pSUPSCAKm::nopP1 in the nopP1 gene via single-crossover, This study Polr, Kmr USDA61 derivative with the nopP2 gene deleted via BEnopP2 This study double-crossover, Polr USDA61 derivative with both innB and nopP2 deleted via BEinnBnopP2 This study double-crossover, Polr USDA61 derivative with both innB and bel2-5 deleted via BEinnB5208 This study double-crossover, Polr a Polr, polymyxin resistant; Kmr, kanamycin resistant; Smr, streptomycin resistant; Spr, spectinomycin resistant; Tcr, tetracycline resistant; Tpr, trimethoprim resistant; Apr, ampicillin resistant. b United States Department of Agriculture (USDA), Beltsville, MD. 2.2. Plant Assays The seeds of Vigna species used in this study are shown in Table S3. Seeds of Vigna species were surface sterilized and germinated as described previously [15]. To optimize seed germination, Vigna seeds were sanded prior to surface sterilization. One day after transplantation, seedlings were 1 inoculated with B. elkanii strains (1 mL of 107 cells mL− per seedling). The plants were grown in a plant growth cabinet (LPH-410SP; NK Systems, Co. Ltd., Osaka, Japan) at 25 ◦C and 70% humidity under a day/night regimen of 16/8 h. The plants used for microscopic analysis were grown using seed pouches (Daiki Rika Co. Ltd., Saitama, Japan) supplemented with nitrogen-free Broughton and Dilworth (B&D) solution [20], with two plants per pouch [21]. The symbiotic phenotypes, including nodule number, fresh nodule weight, and whole fresh plant weight, were examined 35 days post-inoculation (dpi). 2.3. GUS Assay and Microscopic Analysis The GUS-tagged B. elkanii strains were constructed by chromosomal integration of the plasmids pCAM120 [22] via conjugations. Single colonies of the constructed mutants were verified by antibiotic resistance, PCR, and GUS assays using X-Glc (Wako
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