دورية أكاديمية
Phosphatidylcholine-deficient suppressor mutant of Sinorhizobium meliloti, altered in fatty acid synthesis, partially recovers nodulation ability in symbiosis with alfalfa (Medicago sativa).
| العنوان: | Phosphatidylcholine-deficient suppressor mutant of Sinorhizobium meliloti, altered in fatty acid synthesis, partially recovers nodulation ability in symbiosis with alfalfa (Medicago sativa). |
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| المؤلفون: | García-Ledesma JD; Centro de Ciencias Genómicas, Universidad Nacional Autónoma de México, Avenida Universidad s/n, Cuernavaca, Morelos, CP 62210, Mexico., Cárdenas-Torres L; Instituto de Biotecnología, Universidad Nacional Autónoma de México, Avenida Universidad 2001, Cuernavaca, Morelos, CP 62210, Mexico., Martínez-Aguilar L; Centro de Ciencias Genómicas, Universidad Nacional Autónoma de México, Avenida Universidad s/n, Cuernavaca, Morelos, CP 62210, Mexico., Chávez-Martínez AI; Instituto de Biotecnología, Universidad Nacional Autónoma de México, Avenida Universidad 2001, Cuernavaca, Morelos, CP 62210, Mexico., Lozano L; Centro de Ciencias Genómicas, Universidad Nacional Autónoma de México, Avenida Universidad s/n, Cuernavaca, Morelos, CP 62210, Mexico., López-Lara IM; Centro de Ciencias Genómicas, Universidad Nacional Autónoma de México, Avenida Universidad s/n, Cuernavaca, Morelos, CP 62210, Mexico., Geiger O; Centro de Ciencias Genómicas, Universidad Nacional Autónoma de México, Avenida Universidad s/n, Cuernavaca, Morelos, CP 62210, Mexico. |
| المصدر: | The Plant journal : for cell and molecular biology [Plant J] 2024 May; Vol. 118 (4), pp. 1136-1154. Date of Electronic Publication: 2024 Feb 11. |
| نوع المنشور: | Journal Article |
| اللغة: | English |
| بيانات الدورية: | Publisher: Blackwell Scientific Publishers and BIOS Scientific Publishers in association with the Society for Experimental Biology Country of Publication: England NLM ID: 9207397 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1365-313X (Electronic) Linking ISSN: 09607412 NLM ISO Abbreviation: Plant J Subsets: MEDLINE |
| أسماء مطبوعة: | Original Publication: Oxford : Blackwell Scientific Publishers and BIOS Scientific Publishers in association with the Society for Experimental Biology, c1991- |
| مواضيع طبية MeSH: | Sinorhizobium meliloti*/physiology , Sinorhizobium meliloti*/genetics , Medicago sativa*/microbiology , Medicago sativa*/genetics , Plant Root Nodulation*/genetics , Symbiosis* , Fatty Acids*/metabolism , Fatty Acids*/biosynthesis , Phosphatidylcholines*/metabolism , Phosphatidylcholines*/biosynthesis, Bacterial Proteins/genetics ; Bacterial Proteins/metabolism ; Root Nodules, Plant/microbiology ; Root Nodules, Plant/genetics ; Root Nodules, Plant/metabolism ; Mutation ; Polysaccharides, Bacterial/metabolism ; Polysaccharides, Bacterial/biosynthesis ; Nitrogen Fixation |
| مستخلص: | Rhizobial phosphatidylcholine (PC) is thought to be a critical phospholipid for the symbiotic relationship between rhizobia and legume host plants. A PC-deficient mutant of Sinorhizobium meliloti overproduces succinoglycan, is unable to swim, and lacks the ability to form nodules on alfalfa (Medicago sativa) host roots. Suppressor mutants had been obtained which did not overproduce succinoglycan and regained the ability to swim. Previously, we showed that point mutations leading to altered ExoS proteins can reverse the succinoglycan and swimming phenotypes of a PC-deficient mutant. Here, we report that other point mutations leading to altered ExoS, ChvI, FabA, or RpoH1 proteins also revert the succinoglycan and swimming phenotypes of PC-deficient mutants. Notably, the suppressor mutants also restore the ability to form nodule organs on alfalfa roots. However, nodules generated by these suppressor mutants express only low levels of an early nodulin, do not induce leghemoglobin transcript accumulation, thus remain white, and are unable to fix nitrogen. Among these suppressor mutants, we detected a reduced function mutant of the 3-hydoxydecanoyl-acyl carrier protein dehydratase FabA that produces reduced amounts of unsaturated and increased amounts of shorter chain fatty acids. This alteration of fatty acid composition probably affects lipid packing thereby partially compensating for the previous loss of PC and contributing to the restoration of membrane homeostasis. (© 2024 Society for Experimental Biology and John Wiley & Sons Ltd.) |
| References: | Bao, X., Koorengevel, M.C., Koerkamp, M.J.A., Homavar, A., Weijn, A., Crielaard, S. et al. (2021) Shortening of membrane lipid acyl chains compensates for phosphatidylcholine deficiency in choline‐auxotroph yeast. The EMBO Journal, 40, e107966. Available from: https://doi.org/10.15252/embj.2021107966. Bligh, E.G. & Dyer, W.J. (1959) A rapid method of total lipid extraction and purification. The Canadian Journal of Biochemistry and Physiology, 37, 911–917. Available from: https://doi.org/10.1139/o59‐099. Bourret, R.B. (2010) Receiver domain structure and function in response regulator proteins. Current Opinion in Microbiology, 13(2), 142–149. Available from: https://doi.org/10.1016/j.mib.2010.01.015. Brewin, N.J. (2004) Plant cell wall remodelling in the rhizobium‐legume symbiosis. Critical Reviews in Plant Sciences, 23, 293–316. Available from: https://doi.org/10.1080/07352680490480734. Cheng, H.P. & Walker, G.C. (1998) Succinoglycan production by Rhizobium meliloti is regulated through the ExoS‐ChvI two‐component regulatory system. Journal of Bacteriology, 180, 20–26. Available from: https://doi.org/10.1128/JB.180.1.20‐26.1998. de Lucena, D.K.C., Pühler, A. & Weidner, S. (2010) The role of sigma factor RpoH1 in the pH stress response of Sinorhizobium meliloti. BMC Miocrobiology, 18(10), 265. Available from: https://doi.org/10.1186/1471‐2180‐10‐265. de Rudder, K.E.E., López‐Lara, I.M. & Geiger, O. (2000) Inactivation of the gene for phospholipid N‐methyltransferase in Sinorhizobium meliloti: phosphatidylcholine is required for normal growth. Molecular Microbiology, 37, 763–772. Available from: https://doi.org/10.1046/j.1365‐2958.2000.02032.x. de Rudder, K.E.E., Sohlenkamp, C. & Geiger, O. (1999) Plant‐exuded choline is used for rhizobial membrane lipid biosynthesis by phosphatidylcholine synthase. Journal of Biological Chemistry, 274, 20011–20016. Available from: https://doi.org/10.1074/jbc.274.28.20011. de Rudder, K.E.E., Thomas‐Oates, J.E. & Geiger, O. (1997) Rhizobium meliloti mutants deficient in phospholipid N‐methyltransferase still contain phosphatidylcholine. Journal of Bacteriology, 179, 6921–6928. Available from: https://doi.org/10.1128/jb.179.22.6921‐6928.1997. Ernst, R., Ejsing, C.S. & Antonny, B. (2016) Homeoviscous adaptation and the regulation of membrane lipids. Journal of Molecular Biology, 428, 4776–4791. Available from: https://doi.org/10.1016/j.jmb.2016.08.013. Esseling, J.J., Lhuissier, F.G.P. & Emons, A.M. (2003) Nod factor‐induced root hair curling: continuous polar growth towards the point of nod factor application. Plant Physiology, 132(4), 1982–1998. Available from: https://doi.org/10.1104/pp.103.021634. Gao, J.‐L., Weissenmayer, B., Taylor, A., Thomas‐Oates, J., López‐Lara, I.M. & Geiger, O. (2004) Identification of a gene required for the formation of lyso‐ornithine lipid, an intermediate in the biosynthesis of ornithine‐containing lipids. Molecular Microbiology, 53, 1757–1770. Geiger, O., López‐Lara, I.M. & Sohlenkamp, C. (2013) Phosphatidylcholine biosynthesis and function in bacteria. Biochimica et Biophysica Acta, 1831(3), 503–513. Available from: https://doi.org/10.1016/j.bbalip.2012.08.009. Geiger, O., Sohlenkamp, C., Vera‐Cruz, D., Medeot, D.B., Martínez‐Aguilar, L., Sahonero‐Canavesi, D.X. et al. (2021) ExoS/ChvI two‐component signal‐transduction system activated in the absence of bacterial phosphatidylcholine. Frontiers in Plant Science, 12, 678976. Available from: https://doi.org/10.3389/fpls.2021.678976. Gibson, K.E., Kobayashi, H. & Walker, G.C. (2008) Molecular determinants of a symbiotic chronic infection. Annual Review of Genetics, 42, 413–441. Available from: https://doi.org/10.1146/annurev.genet.42.110807.091427. Greenwich, J.L., Heckel, B.C., Alakavuklar, M.A. & Fuqua, C. (2023) The ChvG‐ChvI regulatory network: a conserved global regulatory circuit among the alphaproteobacterial with pervasive impacts on host interactions and diverse cellular processes. Annual Review of Microbiology, 77, 131–148. Available from: https://doi.org/10.1146/annurev‐micro‐120822‐102714. Hanahan, D. (1983) Studies on transformation of Escherichia coli with plasmids. Journal of Molecular Biology, 166, 557–580. Available from: https://doi.org/10.1016/s0022‐2836(83)80284‐8. Isidra‐Arellano, M.C., Pozas‐Rodríguez, E.A., Reyero‐Saavedra, M.R., Arroyo‐Canales, J., Ferrer‐Orgaz, S., Sánchez‐Correa, M.S. et al. (2020) Inhibition of legume nodulation by pi deficiency is dependent on the autoregulation of nodulation (AON) pathway. Plant Journal, 103, 1125–1133. Available from: https://doi.org/10.1111/tpj.14789. Jiang, S., Jardinaud, M.‐F., Gao, J., Pecrix, Y., Wen, J., Mysore, K. et al. (2021) NIN‐like protein transcription factors regulate leghemoglobin genes in legume nodules. Plant Science, 374, 625–628. Jones, K.M., Kobayashi, H., Davies, B.W., Taga, M.E. & Walker, G.C. (2007) How rhizobial symbionts invade plants: the Sinorhizobium–Medicago model. Nature Reviews Microbiology, 5, 619–633. Khosa, S., Hoeppner, A., Gohlke, H., Schmitt, L. & Smits, S.H.J. (2016) Structure of the response regulator NsrR from Streptococcus agalactiae, which is involved in lantibiotic resistance. PLoS One, 11(3), e0149903. Available from: https://doi.org/10.1371/journal.pone.0149903. Kouchi, H., Imaizumi‐Anraku, H., Hayashi, M., Hakoyama, T., Nakagawa, T., Umehara, Y. et al. (2010) How many peas in a pod? Legume genes responsible for mutualistic symbioses underground. Plant and Cell Physiology, 51, 1381–1397. Langmead, B. & Salzberg, S.L. (2012) Fast gapped‐read alignment with bowtie 2. Nature Methods, 9, 357–359. Available from: https://doi.org/10.1038/nmeth.1923. Leigh, J.A., Signer, E.R. & Walker, G.C. (1985) Exopolysaccharide‐deficient mutants of Rhizobium meliloti that form ineffective nodules. Proceedings of the National Academy of Sciences of the United States of America, 82, 6231–6235. Available from: https://doi.org/10.1073/pnas.82.18.6231. Li, H. (2011) A statistical framework for SNP calling, mutation discovery, association mapping and population genetical parameter estimation from sequencing data. Bioinformatics, 27, 2987–2993. Available from: https://doi.org/10.1093/bioinformatics/btr509. López‐Lara, I.M., Gao, J.L., Soto, M.J., Solares‐Pérez, A., Weissenmayer, B., Sohlenkamp, C. et al. (2005) Phosphorus‐free membrane lipids of Sinorhizobium meliloti are not required for the symbiosis with alfalfa but contribute to increased cell yields under phosphorus‐limiting conditions of growth. Molecular Plant‐Microbe Interactions, 18, 973–982. Available from: https://doi.org/10.1094/MPMI‐18‐0973. Lu, H.Y., Luo, L., Yang, M.H. & Cheng, H.P. (2012) Sinorhizobium meliloti ExoR is the target of periplasmic proteolysis. Journal of Bacteriology, 194, 4029–4040. Available from: https://doi.org/10.1128/JB.00313‐12. Medeot, D.B., Sohlenkamp, C., Dardanelli, M.S., Geiger, O., Garcia de Lema, M. & López‐Lara, I.M. (2010) Phosphatidylcholine levels of peanut‐nodulating Bradyrhizobium sp. SEMIA 6144 affect cell size and motility. FEMS Microbiology Letters, 303, 123–131. Available from: https://doi.org/10.1111/j.1574‐6968.2009.01873.x. Minder, A.C., de Rudder, K.E.E., Narberhaus, F., Fischer, H.‐S., Hennecke, H. & Geiger, O. (2001) Phosphatidylcholine levels in Bradyrhizobium japonicum membranes are critical for an efficient symbiosis with the soybean host plant. Molecular Microbiology, 39(5), 1186–1198. Moynié, L., Leckie, S.M., McMahon, S.A., Duthie, F.G., Koehnke, A., Taylor, J.W. et al. (2013) Structural insights into the mechanism and inhibition of the β‐hydroxydecanoyl‐acyl carrier protein dehydratase from Pseudomonas aeruginosa. Journal of Molecular Biology, 425, 365–377. Available from: https://doi.org/10.1016/j.jmb.2012.11.017. Olivares, J., Casadesus, J. & Bedmar, E.J. (1980) Method for testing degree of infectivity of Rhizobium meliloti strains. Applied and Environmental Microbiology, 39(5), 967–970. Available from: https://doi.org/10.1128/aem.39.5.967‐970.1980. Paulucci, N.S., Dardanelli, M.S. & García de Lema, M. (2014) Biochemical and molecular evidence of a Δ9 fatty acid desaturase from Ensifer meliloti 1021. Microbiological Research, 165(5–6), 463–468. Available from: https://doi.org/10.1016/j.micres.2013.08.003. Pichaud, M., Journet, E.P., Dedieu, A., de Billy, F., Truchet, G. & Barker, D. (1992) Rhizobium meliloti elicits transient expression of the early nodulin gene ENOD12 in the differentiating root epidermis of transgenic alfalfa. Plant Cell, 4(10), 1199–1211. Available from: https://doi.org/10.1105/tpc.4.10.1199. Rigaud, J. & Puppo, A. (1975) Indole‐2 acetic acid catabolism by soybean bacteroids. Journal of General Microbiology, 88, 223–228. Available from: https://doi.org/10.1099/00221287‐88‐2‐223. Sambrook, J. & Russell, D.R. (2001) Molecular cloning: a laboratory manual. Cold Spring Harbor, NY: Cold Spring Harbor Press. Schmittgen, T.D. & Livak, K.J. (2008) Analyzing real‐time PCR data by the comparative C(T) method. Nature Protocols, 3(6), 1101–1108. Scott, H.N., Laible, P.D. & Hanson, D.K. (2003) Sequences of versatile broad‐host‐range vectors of the RK2 family. Plasmid, 50(1), 74–79. Available from: https://doi.org/10.1016/s0147‐619x(03)00030‐1. Simon, R., Priefer, U. & Pühler, A. (1983) A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in gram‐negative bacteria. Bio/Technology, 1, 784–791. Sohlenkamp, C., de Rudder, K.E.E. & Geiger, O. (2004) Phosphatidylethanolamine is not essential for growth of Sinorhizobium meliloti on complex culture media. Journal of Bacteriology, 186, 1667–1677. Available from: https://doi.org/10.1128/jb.186.6.1667‐1677.2004. Sohlenkamp, C., de Rudder, K.E.E., Röhrs, V., López‐Lara, I.M. & Geiger, O. (2000) Cloning and characterization of the gene for phosphatidylcholine synthase. Journal of Biological Chemistry, 275, 18919–18925. Available from: https://doi.org/10.1074/jbc.M000844200. Stuurman, N., Bras, C.P., Schlaman, H.R.M., Wijfjes, A.H.M., Bloemberg, G. & Spaink, H.P. (2000) Use of green fluorescent protein color variants expressed on stable broad‐host‐range vectors to visualize rhizobia interacting with plants. Molecular Plant‐Microbe Interactions, 13(11), 1163–1169. Available from: https://doi.org/10.1094/MPMI.2000.13.11.1163. Tsyganova, A.V., Brewin, N.J. & Tsyganov, V.E. (2021) Structure and development of the legume‐rhizobial symbiotic interface in infection threads. Cell, 10, 1050. Available from: https://doi.org/10.3390/cells10051050. Wang, X., Fu, Y., Ban, L., Wang, Z., Feng, G., Li, J. et al. (2015) Selection of reliable reference genes for quantitative real‐time RT‐PCR in alfalfa. Genes & Genetic Systems, 90, 175–180. Wells, D.H., Chen, E.J., Fisher, R.F. & Long, S.R. (2007) ExoR is genetically coupled to the ExoS‐ChvI two‐component system and located in the periplasma of Sinorhizobium meliloti. Molecular Microbiology, 64, 647–664. Available from: https://doi.org/10.1111/j.1365‐2958.2007.05680.x. Yao, S.Y., Luo, L., Har, K.J., Becker, A., Rüberg, S., Yu, G.Q. et al. (2004) Sinorhizobium meliloti ExoR and ExoS proteins regulate both succinoglycan and flagellum production. Journal of Bacteriology, 186, 6042–6049. Available from: https://doi.org/10.1128/JB.186.18.6042‐6049. |
| معلومات مُعتمدة: | P20 RR16475 United States RR NCRR NIH HHS; P20 RR16475 United States RR NCRR NIH HHS |
| فهرسة مساهمة: | Keywords: 3‐hydroxydecanoyl‐acyl carrier protein‐dehydratase; FabA; Nod factor; RpoH1; phosphatidylcholine; phosphatidylethanolamine; sigma factor; succinoglycan; swimming ability |
| تواريخ الأحداث: | Date Created: 20240211 Date Completed: 20240514 Latest Revision: 20240514 |
| رمز التحديث: | 20240515 |
| DOI: | 10.1111/tpj.16661 |
| PMID: | 38341846 |
| قاعدة البيانات: | MEDLINE |
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