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Symbiotic incompatibility between soybean and Bradyrhizobium arises from one amino acid determinant in soybean Rj2 protein


Autoři: Masayuki Sugawara aff001;  Yosuke Umehara aff002;  Akito Kaga aff003;  Masaki Hayashi aff002;  Masao Ishimoto aff003;  Shusei Sato aff001;  Hisayuki Mitsui aff001;  Kiwamu Minamisawa aff001
Působiště autorů: Graduate School of Life Sciences, Tohoku University, Sendai, Miyagi, Japan aff001;  Institute of Agrobiological Sciences, National Agriculture and Food Research Organization, Tsukuba, Ibaraki, Japan aff002;  National Institute of Crop Science, National Agriculture and Food Research Organization, Tsukuba, Ibaraki, Japan aff003
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0222469

Souhrn

Cultivated soybean (Glycine max) carrying the Rj2 allele restricts nodulation with specific Bradyrhizobium strains via host immunity, mediated by rhizobial type III secretory protein NopP and the host resistance protein Rj2. Here we found that the single isoleucine residue I490 in Rj2 is required for induction of symbiotic incompatibility. Furthermore, we investigated the geographical distribution of the Rj2-genotype soybean in a large set of germplasm by single nucleotide polymorphism (SNP) genotyping using a SNP marker for I490. By allelic comparison of 79 accessions in the Japanese soybean mini-core collection, we suggest substitution of a single amino acid residue (R490 to I490) in Rj2 induces symbiotic incompatibility with Bradyrhizobium diazoefficiens USDA 122. The importance of I490 was verified by complementation of rj2-soybean by the dominant allele encoding the Rj2 protein containing I490 residue. The Rj2 allele was also found in Glycine soja, the wild progenitor of G. max, and their single amino acid polymorphisms were associated with the Rj2-nodulation phenotype. By SNP genotyping against 1583 soybean accessions, we detected the Rj2-genotype in 5.4% of G. max and 7.7% of G. soja accessions. Distribution of the Rj2-genotype soybean plants was relatively concentrated in the temperate Asian region. These results provide important information about the mechanism of host genotype-specific symbiotic incompatibility mediated by host immunity and suggest that the Rj2 gene has been maintained by environmental conditions during the process of soybean domestication.


Zdroje

1. Carter TE, Nelson R, Sneller CH, Cui Z. Soybeans: Improvement, Production and Uses 3rd edn. Madison, Wisconsin, USA; 2004.

2. Sedivy EJ, Wu F, Hanzawa Y. Soybean domestication: the origin, genetic architecture and molecular bases. New Phytol. 2017; 214: 539–553. doi: 10.1111/nph.14418 28134435

3. Kim MY, Lee S, Van K, Kim T-H, Jeong S-C, Choi I-Y, et al. Whole-genome sequencing and intensive analysis of the undomesticated soybean (Glycine soja Sieb. and Zucc.) genome. Proc Natl Acad Sci U S A. 2010;107: 22032–22037. doi: 10.1073/pnas.1009526107 21131573

4. Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T, Nelson W, et al. Genome sequence of the palaeopolyploid soybean. Nature. 2010;463: 178–183. doi: 10.1038/nature08670 20075913

5. Qi X, Li M-W, Xie M, Liu X, Ni M, Shao G, et al. Identification of a novel salt tolerance gene in wild soybean by whole-genome sequencing. Nat Commun. 2014;5: 4340. doi: 10.1038/ncomms5340 25004933

6. Lam HM, Xu X, Liu X, Chen W, Yang G, Wong FL, et al. Resequencing of 31 wild and cultivated soybean genomes identifies patterns of genetic diversity and selection. Nat Genet. 2010;42: 1053–1059. doi: 10.1038/ng.715 21076406

7. Kaga A, Shimizu T, Watanabe S, Tsubokura Y, Katayose Y, Harada K, et al. Evaluation of soybean germplasm conserved in NIAS genebank and development of mini core collections. Breed Sci. 2012;61: 566–592. doi: 10.1270/jsbbs.61.566 23136496

8. Song Q, Hyten DL, Jia G, Quigley C V., Fickus EW, Nelson RL, et al. Development and evaluation of SoySNP50K, a high-density genotyping array for soybean. PLoS One. 2013;8(1): e54985. doi: 10.1371/journal.pone.0054985 23372807

9. Oliveira MF, Nelson RL, Geraldi IO, Cruz CD, de Toledo JFF. Establishing a soybean germplasm core collection. Field Crops Res. 2010;119: 277–289. doi: 10.1016/j.fcr.2010.07.021

10. Wang L, Guan Y, Guan R, Li Y, Ma Y, Dong Z, et al. Establishment of Chinese soybean Glycine max core collections with agronomic traits and SSR markers. Euphytica. 2006;151: 215–223. doi: 10.1007/s10681-006-9142-3

11. Delamuta JRM, Ribeiro RA, Ormeño-Orrillo E, Melo IS, Martínez-Romero E, Hungria M. Polyphasic evidence supporting the reclassification of Bradyrhizobium japonicum group Ia strains as Bradyrhizobium diazoefficiens sp. nov. Int J Syst Evol Microbiol. 2013;63: 3342–3351. doi: 10.1099/ijs.0.049130-0 23504968

12. Kuykendall LD, Saxena B, Devine TE, Udell SE. Genetic diversity in Bradyrhizobium japonicum Jordan 1982 and a proposal for Bradyrhizobium elkanii sp.nov. Can J Microbiol. 1992;38: 501–505. doi: 10.1139/m92-082

13. Scholla MH, Elkan GH. Rhizobium fredii sp. nov., a Fast-Growing Species That Effectively Nodulates Soybeans. Int J Syst Bacteriol. 1984;34: 484–486. doi: 10.1099/00207713-34-4-484

14. Itakura M, Saeki K, Omori H, Yokoyama T, Kaneko T, Tabata S, et al. Genomic comparison of Bradyrhizobium japonicum strains with different symbiotic nitrogen-fixing capabilities and other Bradyrhizobiaceae members. ISME J. 2009;3: 326–339. doi: 10.1038/ismej.2008.88 18971963

15. Senaratne R, Amornpimol C, Hardarson G. Effect of combined nitrogen on nitrogen fixation of soybean (Glycine max L. Merill.) as affected by cultivar and rhizobial strain. Plant Soil. 1987;103: 45–50. doi: 10.1007/BF02370666

16. Buendía-Clavería AM, Rodriguez-Navarro DN, Santamaría-Linaza C, Ruiz-Saínz JE, Temprano-Vera F. Evaluation of the Symbiotic Properties of Rhizobium fredii in European Soils. Syst Appl Microbiol. 1994;17: 155–160. doi: 10.1016/S0723-2020(11)80001-9

17. Saeki Y, Minami M, Yamamoto A, Akao S. Estimation of the bacterial community diversity of soybean-nodulating bradyrhizobia isolated from Rj-genotype soybeans. Soil Sci Plant Nutr. 2008;54: 718–724. doi: 10.1111/j.1747-0765.2008.00300.x

18. Suzuki K, Oguro H, Yamakawa T, Yamamoto A, Akao S, Saeki Y. Diversity and distribution of indigenous soybean-nodulating rhizobia in the Okinawa islands, Japan. Soil Sci Plant Nutr. 2008;54: 237–246. doi: 10.1111/j.1747-0765.2007.00236.x

19. Yang SH, Chen WH, Wang ET, Chen WF, Yan J, Han XZ, et al. Rhizobial biogeography and inoculation application to soybean in four regions across China. J Appl Microbiol. 2018;125: 853–866. doi: 10.1111/jam.13897 29719942

20. Ferguson BJ, Mens C, Hastwell AH, Zhang M, Su H, Jones CH, et al. Legume nodulation: The host controls the party. Plant Cell Environ. 2019;42: 41–51. doi: 10.1111/pce.13348 29808564

21. Hayashi M, Saeki Y, Haga M, Harada K, Kouchi H, Umehara Y. Rj (rj) genes involved in nitrogen-fixing root nodule formation in soybean. Breed Sci. 2012;61: 544–553. doi: 10.1270/jsbbs.61.544 23136493

22. Yamakawa T, Hussain AKMA, Ishizuka J. Soybean preference for Bradyrhizobium japonicum for nodulation. Soil Sci Plant Nutr. 2003;49: 835–841. doi: 10.1080/00380768.2003.10410345

23. Caldwell BE. Inheritance of a Strain-Specific Ineffective Nodulation in Soybeans. Crop Sci. 1966;6: 427–428. doi: 10.2135/cropsci1966.0011183X000600050010x

24. Sugawara M, Takahashi S, Umehara Y, Iwano H, Tsurumaru H, Odake H, et al. Variation in bradyrhizobial NopP effector determines symbiotic incompatibility with Rj2-soybeans via effector-triggered immunity. Nat Commun. 2018;9: 3139. doi: 10.1038/s41467-018-05663-x 30087346

25. Devine TE. A Comparison of Rhizobial Strain Compatibilities of Glycine max and its Progenitor Species Glycine soja. Crop Sci. 1987;27: 635–639. doi: 10.2135/cropsci1987.0011183X002700040005x

26. Devine TE, Breithaupt BH. Frequencies of Nodulation Response Alleles, Rj2 and Rj4, in Soybean Plant Introduction and Breeding Lines. USDA Tech Bull. United States Department of Agriculture, Economic Research Service; 1981;No.1628. Available from: https://econpapers.repec.org/paper/agsuerstb/157734.htm

27. Ishizuka J, Suemasu Y, Mizogami K. Preference of Rj-soybean cultivars for Bradyrhizobium japonicum for nodulation. Soil Sci Plant Nutr. 1991;37: 15–21. doi: 10.1080/00380768.1991.10415005

28. Yang S, Tang F, Gao M, Krishnan HB, Zhu H. R gene-controlled host specificity in the legume–rhizobia symbiosis. Proc Natl Acad Sci U S A. 2010;107: 18735–18740. doi: 10.1073/pnas.1011957107 20937853

29. Gassmann W, Bhattacharjee S. Effector-triggered immunity signaling: from gene-for-gene pathways to protein-protein interaction networks. Mol Plant Microbe Interact. 2012;25: 862–868. doi: 10.1094/MPMI-01-12-0024-IA 22414439

30. Kourelis J, van der Hoorn RAL. Defended to the Nines: 25 Years of Resistance Gene Cloning Identifies Nine Mechanisms for R Protein Function. Plant Cell. 2018;30: 285–299. doi: 10.1105/tpc.17.00579 29382771

31. Tsukui T, Eda S, Kaneko T, Sato S, Okazaki S, Kakizaki-Chiba K, et al. The Type III Secretion System of Bradyrhizobium japonicum USDA122 Mediates Symbiotic Incompatibility with Rj2 Soybean Plants. Appl Environ Microbiol. 2013;79: 1048–1051. doi: 10.1128/AEM.03297-12 23204412

32. Cesari S. Multiple strategies for pathogen perception by plant immune receptors. New Phytol. 2018;219: 17–24. doi: 10.1111/nph.14877 29131341

33. Meyers BC, Kozik A, Griego A, Kuang H, Michelmore RW. Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis. Plant Cell. 2003;15: 809–834. doi: 10.1105/tpc.009308 12671079

34. Michelmore RW, Meyers BC. Clusters of resistance genes in plants evolve by divergent selection and a birth-and-death process. Genome Res. 1998;8: 1113–1130. doi: 10.1101/gr.8.11.1113 9847076

35. Zhou T, Wang Y, Chen J-Q, Araki H, Jing Z, Jiang K, et al. Genome-wide identification of NBS genes in japonica rice reveals significant expansion of divergent non-TIR NBS-LRR genes. Mol Genet Genomics. 2004;271: 402–415. doi: 10.1007/s00438-004-0990-z 15014983

36. Hyten DL, Song Q, Zhu Y, Choi I-Y, Nelson RL, Costa JM, et al. Impacts of genetic bottlenecks on soybean genome diversity. Proc Natl Acad Sci U S A. 2006;103: 16666–16671. doi: 10.1073/pnas.0604379103 17068128

37. Kim MY, Van K, Kang YJ, Kim KH, Lee S-H. Tracing soybean domestication history: From nucleotide to genome. Breed Sci. 2012;61: 445–452. doi: 10.1270/jsbbs.61.445 23136484

38. Zheng F, Wu H, Zhang R, Li S, He W, Wong FL, et al. Molecular phylogeny and dynamic evolution of disease resistance genes in the legume family. BMC Genomics. 2016;17: 402. doi: 10.1186/s12864-016-2736-9 27229309

39. Zhong Y, Zhang X, Cheng ZM. Lineage-specific duplications of NBS-LRR genes occurring before the divergence of six Fragaria species. BMC Genomics. BMC Genomics; 2018;19: 128. doi: 10.1186/s12864-018-4521-4 29422035

40. Saeki Y, Aimi N, Tsukamoto S, Yamakawa T, Nagatomo Y, Akao S. Diversity and geographical distribution of indigenous soybean-nodulating bradyrhizobia in Japan. Soil Sci Plant Nutr. 2006;52: 418–426. doi: 10.1111/j.1747-0765.2006.00050.x

41. Devine TE, Kuykendall LD. Host genetic control of symbiosis in soybean (Glycine max l.). Plant Soil. 1996;186: 173–187. doi: 10.1007/BF00035072

42. Vest G, Caldwell BE. Rj4—A Gene Conditioning Ineffective Nodulation in Soybean. Crop Sci. 1972;12: 692–693. doi: 10.2135/cropsci1972.0011183X001200050042x

43. Saeki Y, Shiro S. Comparison of Soybean-Nodulating Bradyrhizobia Community Structures Along North Latitude Between Japan and USA. In: Ohyama T, editor. Advances in Biology and Ecology of Nitrogen Fixation. InTech; 2014. pp. 195–223. doi: 10.5772/57165

44. Vinuesa P, Rojas-Jiménez K, Contreras-Moreira B, Mahna SK, Prasad BN, Moe H, et al. Multilocus sequence analysis for assessment of the biogeography and evolutionary genetics of four Bradyrhizobium species that nodulate soybeans on the asiatic continent. Appl Environ Microbiol. 2008;74: 6987–6996. doi: 10.1128/AEM.00875-08 18791003

45. Wu LJ, Wang HQ, Wang ET, Chen WX, Tian CF. Genetic diversity of nodulating and non-nodulating rhizobia associated with wild soybean (Glycine soja Sieb. & Zucc.) in different ecoregions of China. FEMS Microbiol Ecol. 2011;76: 439–450. doi: 10.1111/j.1574-6941.2011.01064.x 21303397

46. Htwe AZ, Yamakawa T, Sarr PS, Sakata T. Diversity and distribution of soybean-nodulating bradyrhizobia isolated from major soybean-growing regions in Myanmar. Afr J Microbiol Res. 2015;9: 2183–2196. doi: 10.5897/ajmr2015.7702

47. Soe KM, Yamakawa T, Hashimoto S, Sarr PS. Phylogenetic diversity of indigenous soya bean bradyrhizobia from different agro-climatic regions in Myanmar. ScienceAsia. 2013;39: 574–583. doi: 10.2306/scienceasia1513-1874.2013.39.574

48. Cole MA, Elkan GH. Transmissible resistance to penicillin G, neomycin, and chloramphenicol in Rhizobium japonicum. Antimicrob Agents Chemother. 1973;4: 248–253. doi: 10.1128/aac.4.3.248 4491197

49. Miller JH. A short course in bacterial genetics: A laboratory manual and handbook for Escherichia coli and related bacteria. NY: Cold Spring Harbor Laboratory Press; 1992.

50. An G, Ebert PR, Mitra A, Ha SB. Binary vectors. In: Gelvin S.B., Schilperoort R.A., Verma D.P.S., editors. Plant Molecular Biology Manual. Dordrecht: Springer Netherlands; 1989. pp. 29–47. doi: 10.1007/978-94-009-0951-9_3

51. Akao S, Kouchi H. Light microscopic observation of root hair curling of soybean induced by Rhizobium infection. Japanese J Soil Sci Plant Nutr. 1989;60: 53–55.

52. Maekawa T, Kusakabe M, Shimoda Y, Sato S, Tabata S, Murooka Y, et al. Polyubiquitin promoter-based binary vectors for overexpression and gene silencing in Lotus japonicus. Mol Plant Microbe Interact. 2008;21: 375–382. doi: 10.1094/MPMI-21-4-0375 18321183

53. Kereszt A, Li D, Indrasumunar A, Nguyen CD, Nontachaiyapoom S, Kinkema M, et al. Agrobacterium rhizogenes-mediated transformation of soybean to study root biology. Nat Protoc. 2007;2: 948–952. doi: 10.1038/nprot.2007.141 17446894

54. Broughton WJ, Dilworth MJ. Control of leghaemoglobin synthesis in snake beans. Biochem J. 1971;125: 1075–1080. doi: 10.1042/bj1251075 5144223


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