biologia plantarum

International journal on Plant Life established by Bohumil Němec in 1959

Biologia plantarum 53:451-460, 2009 | DOI: 10.1007/s10535-009-0085-0

A mutation affecting symbiosis in the pea line Risnod27 changes the ion selectivity filter of the DMI1 homolog

K. Novák1,*, J. Felsberg1, E. Biedermannová2, J. Vondrys2
1 Institute of Microbiology, Academy of Sciences of the Czech Republic, Prague, Czech Republic
2 Department of Crop Production, University of South Bohemia, České Budějovice, Czech Republic

After identifying regions of cDNA conserved between the symbiotic gene DMI1 of the model species Medicago truncatula and the homologous genomic region of Arabidopsis thaliana, universal primers were designed from 8 of 12 exons to allow the routine amplification of plant homologs. As an example, the complete homologous sequence from the pea (Pisum sativum L.) was amplified and sequenced, although the poorly conserved 5'-end and 5'-flanking region of the gene had to be amplified using a modified TAIL-PCR strategy. The identity of this amplified homolog with the SYM8 gene was independently confirmed by the presence of a single nucleotide change in the coding sequence of the mutant line Risnod27 (sym8) that cosegregated with the asymbiotic phenotype. Five insertions in pea introns responsible for increasing the total length of SYM8 by 1443 bp, compared to the M. truncatula homolog DMI1, belong to known transposon and retrotransposon families of pea and legumes in general. In view of the predicted function of SYM8 as an ion channel, the Risnod27 mutation (His309Tyr) appears to be localized in the selectivity filter domain. This finding confirms the essential role of histidine 309 in the symbiotic function of SYM8 and provides a guide to its ionic specificity. In view of the Risnod27 symbiotic phenotype, we hypothesize that SYM8 does not have identical functions in the transduction of rhizobial and mycorrhizal signals. The variability of the N-proximal region of the known legume homologs of DMI1 suggests an interaction with a variable ligand.

Keywords: Nod factor; Pisum sativum; recognition; Rhizobium; TAIL-PCR; universal primers
Subjects: Arabidopsis thaliana; Medicago truncatula; mutagenesis, mutants; pea; Pisum sativum; symbiosis; transgenic plants

Received: April 22, 2008; Accepted: November 15, 2008; Published: September 1, 2009  Show citation

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Novák, K., Felsberg, J., Biedermannová, E., & Vondrys, J. (2009). A mutation affecting symbiosis in the pea line Risnod27 changes the ion selectivity filter of the DMI1 homolog. Biologia plantarum53(3), 451-460. doi: 10.1007/s10535-009-0085-0
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References

  1. Albrecht, C., Geurts, R., Lapeyrie, F., Bisseling, T.: Endomycorrhizae and rhizobial Nod factors both require SYM8 to induce the expression of the early nodulin genes PsENOD5 and PsENOD12A. - Plant J. 15: 605-614, 1998. Go to original source...
  2. Ané, J.M., Kiss, G.B., Riely, B.K., Penmetsa, R.V., Oldroyd, G.E.D., Ayax, C., Lévy, J., Debellé, F., Baek, J.M., Kaló, P., Rosenberg, C., Roe, B.A., Long, S.R., Dénarié, J., Cook, D.R.: Medicago truncatula DMI1 required for bacterial and fungal symbioses in legumes. - Science 303: 1364-1367, 2004. Go to original source...
  3. Ané, J.M., Lévy, J., Thoquet, P., Kulikova, O., De Billy, F., Penmetsa, V., Kim, D.J., Debelle, F., Rosenberg, C., Cook, D.R., Bisseling, T., Huguet, T., Dénarié, J.: Genetic and cytogenetic mapping of DMI1, DMI2, and DMI3 genes of Medicago truncatula involved in Nod factor transduction, nodulation, and mycorrhization. - Mol. Plant-Microbe Interact. 15: 1108-1118, 2002. Go to original source...
  4. Ausubel, F.M., Brent, R., Kingston, R.E., Moore, D.D., Seidman, J.G., Smith, J.A., Struhl, K. (ed.): Current Protocols in Molecular Biology. - Wiley, New York 1989.
  5. Biedermannová, E., Novák, K., Vondrys, J.: Pea mutant Risnod27 as reference line for field assessment of impact of symbiotic nitrogen fixation. - J. Plant Nutr. 25: 2051-2066, 2002. Go to original source...
  6. Brendel, V., Kleffe, J., Carle-Urioste, J.C., Walbot, V.: Prediction of splice sites in plant pre-mRNA from sequence properties. - J. mol. Biol. 276: 85-104, 1998. Go to original source...
  7. Bureau, T.E., Wessler, S.R.: Stowaway: a new family of inverted repeat elements associated with the genes of both monocotyledonous and dicotyledonous plants. - Plant Cell 6: 907-916, 1994. Go to original source...
  8. Carroll, B.J., McNeil, D.L., Gresshoff, P.M.: Mutagenesis of soybean (Glycine max (L.) Merr.) and the isolation of nonnodulating mutants. - Plant Sci. 47: 109-114, 1986. Go to original source...
  9. Catoira, R., Galera, C., De Billy, F., Penmetsa, R.V., Journet, E.-P., Maillet, F., Rosenberg, C., Cook, D., Gough, C., Dénarié, J.: Four genes of Medicago truncatula controlling components of a Nod factor transduction pathway. - Plant Cell 12: 1647-1665, 2000. Go to original source...
  10. Charpentier, M., Bredemeier, R., Schleiff, E., Parniske, M.: CASTOR and POLLUX in symbiotic signal transduction. - In: Abstracts 13th International Congress on Molecular Plant-Microbe Interactions. P. 144. IS-MPMI, Sorrento 2007.
  11. Cornette, J.L., Cease, K.B., Margalit, H., Spouge, J.L., Berzofsky, J.A., DeLisi, C.: Hydrophobicity scales and computational techniques for detecting amphipathic structures in proteins. - J. mol. Biol. 195: 659-685, 1987. Go to original source...
  12. Demchenko, K., Winzer, T., Stougaard, J., Parniske, M., Pawlowski, K.: Distinct roles of Lotus japonicus SYMRK and SYM15 in root colonization and arbuscule formation. - New Phytol. 163: 381-392, 2004. Go to original source...
  13. Downie, J.A., Walker, S.A.: Plant responses to nodulation factors. - Curr. Opin. Plant Biol. 2: 483-489, 1999. Go to original source...
  14. Edwards, A., Heckmann, A.B., Yousafzai, F., Duc, G., Downie, J.A.: Structural implications of mutations in the pea SYM8 symbiosis gene, the DMI1 ortholog, encoding a predicted ion channel. - Mol. Plant-Microbe Interact. 20: 1183-1191, 2007. Go to original source...
  15. Ellis, T.H.N.: Approaches to the genetic mapping of pea. - Modern Methods Plant Anal. 16: 117-160, 1994. Go to original source...
  16. Ellis, T.H.N., Poyser, S.J., Knox, M.R., Vershinin, A.V., Ambrose, M.J.: Polymorphism of insertion sites of Ty1-copia class retrotransposons and its use for linkage and diversity analysis in pea. - Mol. gen. Genet. 260: 9-19, 1998. Go to original source...
  17. Emanuelsson, O., Nielsen, H., Von Heijne, G.: ChloroP, a neural network-based method for predicting chloroplast transit peptides and their cleavage sites. - Protein Sci. 8: 978-984, 1999. Go to original source...
  18. Endre, G., Kereszt, A., Kevei, Z., Mihacea, S., Kaló, P., Kiss, G.: A receptor kinase gene regulating symbiotic nodule development. - Nature 417: 962-966, 2002. Go to original source...
  19. Engvild, K.C.: Nodulation and nitrogen fixation mutants of pea, Pisum sativum. - Theor. appl. Genet. 74:711-713, 1987. Go to original source...
  20. Hall, T.A.: BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. - Nucl. Acids Symp. Ser. 41: 95-98, 1999.
  21. Handberg, K., Stougaard, J.: Lotus japonicus, an autogamous, diploid legume species for classical and molecular genetics. - Plant J. 2: 487-496, 1992. Go to original source...
  22. Häser, A., Robinson, D.L., Duc, G., Vance, C.P.: A mutation in Vicia faba results in ineffective nodules with impaired bacteroid differentiation and reduced synthesis of late nodulins. - J. exp. Bot. 43: 1397-1407, 1992. Go to original source...
  23. Imaizumi-Anraku, H., Takeda, N., Charpentier, M., Perry, J., Miwa, H., Umehara, Y., Kouchi, H., Murakami, Y., Mulder, L., Vickers, K., Pike, J., Downie, J.A., Wang, T., Sato, S., Asamizu, E., Tabata, S., Yoshikawa, M., Murooka, Y., Wu, G.J., Kawaguchi, M., Kawasaki, S., Parniske, M., Hayashi, M.: Plastid proteins crucial for symbiotic fungal and bacterial entry into plant roots. - Nature 433: 527-531, 2005. Go to original source...
  24. Jacobsen, E.: Modification of symbiotic interaction of pea (Pisum sativum L.) and Rhizobium leguminosarum by induced mutations. - Plant Soil 82: 427-438, 1984. Go to original source...
  25. Josey, D.P., Beynon, J.L., Johnston, A.W.B., Beringer, J.: Strain identification in Rhizobium using intrinsic antibiotic resistance. - J. appl. Microbiol. 46: 343-350, 1979. Go to original source...
  26. Kneen, B.E., Weeden, N.F., LaRue, T.A.: Non-nodulating mutants of Pisum sativum (L.) cv. Sparkle. - J. Heredity 85: 129-133, 1994. Go to original source...
  27. Kolycheva, A.N., Jakobi, L.M., Borisov, A.Y., Filatov, A.A., Tikhonovich, I.A., Muromtsev, G.S.: Pea gene sym8 affects symbiosis both with Rhizobium and endomycorrhizal fungi. - Pisum Genet. 25: 22, 1993.
  28. Koropatkin, N.M., Pakrasi, H.B., Smith, T.J.: Atomic structure of a nitrate-binding protein crucial for photosynthetic productivity. - Proc. nat. Acad. Sci. USA 103: 9820-9825, 2006. Go to original source...
  29. Kovářová, P., Navrátilová, A., Macas, J., Doležel, J.: Chromosome analysis and sorting in Vicia sativa using flow cytometry. - Biol. Plant. 51: 43-48, 2007. Go to original source...
  30. Lévy, J., Bres, C., Geurts, R., Chalhoub, B., Kulikova, O., Duc, G., Journet, E.P., Ane, J.M., Lauber, E., Bisseling, T., Dénarie, J., Rosenberg, C., Debelle, F.: A putative Ca2+ and calmodulin-dependent protein kinase required for bacterial and fungal symbioses. - Science 303: 1361-1364, 2004. Go to original source...
  31. Li, M., Schnell, D.J.: Reconstitution of protein targeting to the inner envelope membrane of chloroplasts. - J. Cell Biol. 175: 249-259, 2006. Go to original source...
  32. Limpens, E., Franken, C., Smit, P., Willemse, J., Bisseling, T., Geurts, R.: LysM domain receptor kinases regulating rhizobial Nod factor-induced infection. - Science 302: 630-633, 2003. Go to original source...
  33. Liu, Y.G., Mitsukawa, N., Oosumi, T., Whittier, R.F.: Efficient isolation and mapping of Arabidopsis thaliana T-DNA insert junctions by thermal asymmetric interlaced PCR. - Plant J. 8: 457-463, 1995. Go to original source...
  34. Macas, J., Koblizkova, A., Neumann, P.: Characterization of Stowaway MITEs in pea (Pisum sativum L.) and identification of their potential master elements. - Genome 48: 831-839, 2005. Go to original source...
  35. Markwei, C.M., LaRue, T.A.: Phenotypic characterization of sym8 and sym9, two genes conditioning non-nodulation in Pisum sativum Sparkle. - Can. J. Microbiol. 38: 548-554, 1992. Go to original source...
  36. Morais-Cabral, J.H., Zhou, Y.F., MacKinnon, R.: Energetic optimization of ion conduction rate by the K+ selectivity filter. - Nature 414: 37-42, 2001. Go to original source...
  37. Murray, V.: Improved double-stranded DNA sequencing using the linear polymerase chain reaction. - Nucl. Acids Res. 17: 8889, 1989. Go to original source...
  38. Novák, K.: Allelic relationships of pea nodulation mutants. - J. Hered. 94: 191-193, 2003. Go to original source...
  39. Novák, K., Felsberg, J., Pičmanová, M., Korittová, C., Biedermannová, E., Vondrys, J.: Symbiotic mutation located in the ionic filter of Pisum sativum DMI1 homolog (SYM8). - In: Abstracts 13th International Congress on Molecular Plant-Microbe Interactions. Pp. 244. IS-MPMI, Sorrento 2007.
  40. Provorov, N.A., Borisov, A.Y., Tikhonovich, I.A.: Developmental genetics and evolution of symbiotic structures in nitrogen-fixing nodules and arbuscular mycorrhiza. - J. theor. Biol. 214: 215-232, 2002. Go to original source...
  41. Radutoiu, S., Madsen, L.H., Madsen, E.B., Felle, H.H., Umehara, Y., Gronlund, M., Sato, S., Nakamura, Y., Tabata, S., Sandal, N., Stougaard, J.: Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases. - Nature 425: 585-592, 2003. Go to original source...
  42. Radutoiu, S., Madsen, L.H., Madsen, E.B., Jurkiewicz, A., Fukai, E., Quistgaard, E.M.H., Albrektsen, A.S., James, E.K., Thirup, S., Stougaard, J.: LysM domains mediate lipochitin-oligosaccharide recognition and Nfr genes extend the symbiotic host range. - EMBO J. 26: 3923-3935, 2007. Go to original source...
  43. Riely, B.K., Lougnon, G., Ané, J.M., Cook, D.R.: The symbiotic ion channel homolog DMI1 is localized in the nuclear membrane of Medicago truncatula roots. - Plant J. 49: 208-216, 2007. Go to original source...
  44. Sagan, M., Huguet, T., Duc, G.: Phenotypic characterization and classification of nodulation mutants of pea (Pisum sativum L.). - Plant Sci. 100: 59-70, 1994. Go to original source...
  45. Sagan, M., Morandi, D., Tarenghi, E., Duc, G.: Selection of nodulation and mycorrhizal mutants in the model plant Medicago truncatula (Gaertn) after gamma-ray mutagenesis. - Plant Sci. 111: 63-71, 1995. Go to original source...
  46. Sambrook, J., Fritsch, E.F., Maniatis, T. (ed.): Molecular Cloning: A Laboratory Manual. - Cold Spring Harbor Laboratory Press, Cold Spring Harbor 1989.
  47. Sanger, F., Nickeln, S., Coulson, A.R.: DNA sequencing with chain-terminator inhibitors. - Proc. nat. Acad. Sci. USA 74: 5463-5467, 1977. Go to original source...
  48. Schauser, L., Roussis, A., Stiller, J., Stougaard, J.A.: Plant regulator controlling development of symbiotic root nodules. - Nature 402: 191-195, 1999. Go to original source...
  49. Schneider, A., Walker, S.A., Sagan, M., Duc, G., Ellis, T.H.N., Downie, J.A.: Mapping of the nodulation loci sym9 and sym10 of pea (Pisum sativum L.). - Theor. appl. Genet. 104: 1312-1316, 2002. Go to original source...
  50. Škrdleta, V., Gaudinová, A., Němcová, M., Lisá, L.: Behavior of nodulated Pisum sativum L. under short-term nitrate stress conditions. - Biol. Plant. 26: 364-373, 1984. Go to original source...
  51. Škrdleta, V., Novák, K., Lisá, L.: Response of nodulating and nonnodulating Pisum sativum L. to nitrate. - Biol. Plant. 37: 113-120, 1995. Go to original source...
  52. Smit, P., Raedts, J., Portyanko, V., Debelle, F., Gough, C., Bisseling, T., Geurts, R.: NSP1 of the GRAS protein family is essential for rhizobial Nod factor-induced transcription. - Science 308: 1789-1791, 2005. Go to original source...
  53. Spaink, H.P.: Root nodulation and infection factors produced by rhizobial bacteria. - Annu. Rev. Microbiol. 54: 257-288, 2000. Go to original source...
  54. Stracke, S., Kistner, C., Yoshida, S., Mulder, L., Sato, S., Kaneko, T., Tabata, S., Sandal, N., Stougaard, J., Szczyglowski, K., Parniske, M.: A plant receptor-like kinase required for both bacterial and fungal symbiosis. - Nature 417: 959-962, 2002. Go to original source...
  55. Terauchi, R., Kahl, G.: Rapid isolation of promoter sequences by TAIL-PCR: the 5'-flanking regions of Pal and Pgi genes from yams (Dioscorea). - Mol. gen. Genet. 263: 554-560, 2000. Go to original source...
  56. Tsyganov, V.E, Voroshilova, V.A., Priefer, U.B., Borisov, A.Y., Tikhonovich, I.A.: Genetic dissection of the infection process and nodule tissue development in the Rhizobiumpea (Pisum sativum L.) symbiosis. - Ann. Bot. 89: 357-366, 2002. Go to original source...
  57. Voroshilova, V.A., Boesten, B., Tsyganov, V.E., Borisov, A.Y., Tikhonovich, I.A., Priefer, U.B.: Effect of mutations in Pisum sativum L. genes blocking different stages of nodule development on the expression of late symbiotic genes in Rhizobium leguminosarum bv. viciae. - Mol. Plant-Microbe Interact. 14: 471-476, 2001. Go to original source...
  58. Walker, S.A., Viprey, V., Downie, J.A.: Dissection of nodulation signaling using pea mutants defective for calcium spiking induced by Nod factors and chitin oligomers. - Proc. nat. Acad. Sci. USA 97: 13413-13418, 2000. Go to original source...
  59. Witte, C.P., Le, Q.H., Bureau, T., Kumar, A.: Terminal-repeat retrotransposons in miniature (TRIM) are involved in restructuring plant genomes. - Proc. nat. Acad. Sci. USA. 98: 13778-13783, 2001. Go to original source...
  60. Zhu, H.Y., Riely, B.K., Burns, N.J., Ané, J.M.: Tracing nonlegume orthologs of legume genes required for nodulation and arbuscular mycorrhizal symbioses. - Genetics 172: 2491-2499, 2006. Go to original source...