Analysis of a Het- mutation in Anabaena sp. strain PCC 7120 implicates a secondary metabolite in the regulation of heterocyst spacing
10.1128/jb.176.8.2282-2292.1994
Crossref journal-article
American Society for Microbiology
Journal of Bacteriology (235)
Abstract

Transposon-generated mutant N10 of Anabaena sp. strain PCC 7120 has a Het- phenotype (A. Ernst, T. Black, Y. Cai, J.-M. Panoff, D. N. Tiwari, and C. P. Wolk, J. Bacteriol. 174:6025-6032, 1992). Reconstruction of the transposon mutation reproduced a Het- phenotype, but reconstructions with other insertions at the position of the transposon produced strains that form multiple contiguous heterocysts. Sequence analysis around the site of insertion of the transposon showed that the insertion lies within the 5' end of an 861-bp open reading frame (ORF) (hetN). The product of translation of hetN (HetN) shows extensive similarity to NAD(P)H-dependent oxidoreductases that are involved in biosyntheses of fatty acids, poly-beta-hydroxybutyrate, nod factor, and polyketides. A second, 1,518-bp ORF (hetM) that ends 556 bp 5' from the start of hetN appears to encode a protein that has at least two functional domains: its amino terminus is similar to an acyl carrier protein, while its central portion is similar to domains of proteins that perform reductive reactions. A third, 711-bp ORF (hetI) encoded on the opposite strand ends 42 bp away from the 3' end of hetN. The protein encoded by hetI, HetI, is similar to Sfp from Bacillus subtilis and EntD from Escherichia coli, proteins that are required for the biosynthesis or export of cyclic peptides. Clones from a lambda-EMBL3 library that contain the wild-type DNA for hetN do not complement the hetN::Tn5-1063 mutation in N10. The presence of hetN, as the only ORF, on a replicating plasmid suppresses heterocyst formation in wild-type cells, whereas the additional presence of hetI alleviates this effect.

Bibliography

Black, T. A., & Wolk, C. P. (1994). Analysis of a Het- mutation in Anabaena sp. strain PCC 7120 implicates a secondary metabolite in the regulation of heterocyst spacing. Journal of Bacteriology, 176(8), 2282–2292.

Authors 2
  1. T A Black (first)
  2. C P Wolk (additional)
References 54 Referenced 148
  1. Adams , D. G. 1992 . Multicellularity in cyanobacteria . Symp. Soc. Gen. Microbiol. 47 : 341 - 384 . / Symp. Soc. Gen. Microbiol. / Multicellularity in cyanobacteria by Adams D. G. (1992)
  2. Altschul , S. F. , W. Gish , W. Miller , E. W. Myers , and D. J. Lipman . 1990 . Basic local alignment search tool . J. Mol. Biol. 215 : 403 - 410 . (10.1016/S0022-2836(05)80360-2) / J. Mol. Biol. / Basic local alignment search tool by Altschul S. F. (1990)
  3. Armstrong , S. K. , G. S. Pettis , L. J. Forrester , and M. A. McIntosh . 1989 . The Escherichia coli enterobactin biosynthesis gene, entD: nucleotide sequence and membrane localization of its protein product . Mol. Microbiol. 3 : 757 - 766 . (10.1111/j.1365-2958.1989.tb00224.x) / Mol. Microbiol. / The Escherichia coli enterobactin biosynthesis gene, entD: nucleotide sequence and membrane localization of its protein product by Armstrong S. K. (1989)
  4. Arrowsmith , T. J. , F. Malpartida , D. H. Sherman , A. Birch , D. A. Hopwood , and J. A. Robinson . 1992 . Characterization of actIhomologous DNA encoding polyketide synthase genes from the monensin producer Streptomyces cinnamonensis . Mol. Gen. Genet. 234 : 254 - 264 . (10.1007/BF00283846) / Mol. Gen. Genet. / Characterization of actIhomologous DNA encoding polyketide synthase genes from the monensin producer Streptomyces cinnamonensis by Arrowsmith T. J. (1992)
  5. Bancroft , I. , and C. P. Wolk L 1989 . Characterization of an insertion sequence (IS891) of novel structure from the cyanobacterium Anabaena sp. strain M-131 . J. Bacteriol. 171 : 5949 - 5954 . (10.1128/jb.171.11.5949-5954.1989) / J. Bacteriol. / Characterization of an insertion sequence (IS891) of novel structure from the cyanobacterium Anabaena sp. strain M-131 by Bancroft I. (1989)
  6. Beck , J. , S. Ripka , A. Siegner , E. Schiltz , and E. Schweizer . 1990 . The multifunctional 6-methylsalicylic acid synthase gene of Penicillium patulum; its gene structure relative to that of other polyketide synthases . Eur. J. Biochem. 192 : 487 - 498 . (10.1111/j.1432-1033.1990.tb19252.x) / Eur. J. Biochem. / The multifunctional 6-methylsalicylic acid synthase gene of Penicillium patulum; its gene structure relative to that of other polyketide synthases by Beck J. (1990)
  7. Beppu , T. 1992 . Secondary metabolites as chemical signals for differentiation . Gene 115 : 159 - 165 . (10.1016/0378-1119(92)90554-3) / Gene / Secondary metabolites as chemical signals for differentiation by Beppu T. (1992)
  8. Black , T. A. , Y. Cai , and C. P. Wolk L 1993 . Spatial expression and autoregulation of hetR, a gene involved in the control of heterocyst development in Anabaena. Mol. Microbiol. 9 : 77 - 84 . (10.1111/j.1365-2958.1993.tb01670.x) / Anabaena. Mol. Microbiol. / Spatial expression and autoregulation of hetR, a gene involved in the control of heterocyst development by Black T. A. (1993)
  9. Buikema , W. J. , and R. Haselkorn . 1991 . Isolation and complementation of nitrogen fixation mutants of the cyanobacterium Anabaena sp. strain PCC 7120 . J. Bacteriol. 173 : 1879 - 1885 . (10.1128/JB.173.6.1879-1885.1991) / J. Bacteriol. / Isolation and complementation of nitrogen fixation mutants of the cyanobacterium Anabaena sp. strain PCC 7120 by Buikema W. J. (1991)
  10. Buikema , W. J. , and R. Haselkorn . 1991 . Characterization of a gene controlling heterocyst differentiation in the cyanobacterium Anabaena 7120 . Genes Dev. 5 : 321 - 330 . (10.1101/gad.5.2.321) / Genes Dev. / Characterization of a gene controlling heterocyst differentiation in the cyanobacterium Anabaena 7120 by Buikema W. J. (1991)
  11. Cai , Y. , and C. P. Wolk . 1990 . Use of a conditionally lethal gene in Anabaena sp. strain PCC 7120 to select for double recombinants and to entrap insertion sequences . J. Bacteriol. 172 : 3138 - 3145 . (10.1128/JB.172.6.3138-3145.1990) / J. Bacteriol. / Use of a conditionally lethal gene in Anabaena sp. strain PCC 7120 to select for double recombinants and to entrap insertion sequences by Cai Y. (1990)
  12. Cai Y. and C. P. Wolk Unpublished data.
  13. Carafa , Y. d' A. , E. Brody , and C. Thermes . 1990 . Prediction of Rho-independent Escherichia coli transcriptional terminators: statistical analysis of their RNA stem-loop structures . J. Mol. Biol. 216 : 835 - 858 . (10.1016/S0022-2836(99)80005-9) / J. Mol. Biol. / Prediction of Rho-independent Escherichia coli transcriptional terminators: statistical analysis of their RNA stem-loop structures by Carafa Y. (1990)
  14. Chirala , S. S. , R. Kasturi , M. Pazirandeh , D. T. Szowlow , W. -Y. Huang , and S. J. Wakil . 1989 . A novel cDNA extension procedure: isolation of chicken fatty acid synthase cDNA clones . J. Biol. Chem. 264 : 3750 - 3757 . (10.1016/S0021-9258(19)84913-X) / J. Biol. Chem. / A novel cDNA extension procedure: isolation of chicken fatty acid synthase cDNA clones by Chirala S. S. (1989)
  15. Cortes , J. , S. H. Haydock , G. A. Roberts , D. J. Brevitt , and P. F. Leadlay . 1990 . An unusually large multifunctional polypeptide in the erythromycin-producing polyketide synthase of Saccharopolyspora erythraea . Nature (London) 348 : 176 - 178 . (10.1038/348176a0) / Nature (London) / An unusually large multifunctional polypeptide in the erythromycin-producing polyketide synthase of Saccharopolyspora erythraea by Cortes J. (1990)
  16. Debelle , F. , and S. B. Sharma . 1986 . Nucleotide sequence of Rhizobium meliloti RCR2011 genes involved in host specificity of nodulation . Nucleic Acids Res. 14 : 7453 - 7472 . (10.1093/nar/14.18.7453) / Nucleic Acids Res. / Nucleotide sequence of Rhizobium meliloti RCR2011 genes involved in host specificity of nodulation by Debelle F. (1986)
  17. Donadio , S. , and L. Katz . 1992 . Organization of the enzymatic domains in the multifunctional polyketide synthase involved in erythromycin formation in Saccharopolyspora erythraea . Gene 111 : 51 - 60 . (10.1016/0378-1119(92)90602-L) / Gene / Organization of the enzymatic domains in the multifunctional polyketide synthase involved in erythromycin formation in Saccharopolyspora erythraea by Donadio S. (1992)
  18. Donadio , S. , M. J. Staver , J. B. McAlpine , S. J. Swanson , and L. Katz . 1991 . Modular organization of genes required for complex polyketide biosynthesis . Science 252 : 675 - 679 . (10.1126/science.2024119) / Science / Modular organization of genes required for complex polyketide biosynthesis by Donadio S. (1991)
  19. D'Souza , C. , M. M. Nakano , N. Corbell , and P. Zuber . 1993 . Amino-acylation site mutations in amino acid-activating domains of surfactin synthetase: effects on surfactin production and competence development in Bacillus subtilis . J. Bacteriol. 175 : 3502 - 3510 . (10.1128/JB.175.11.3502-3510.1993) / J. Bacteriol. / Amino-acylation site mutations in amino acid-activating domains of surfactin synthetase: effects on surfactin production and competence development in Bacillus subtilis by D'Souza C. (1993)
  20. Elhai , J. , and C. P. Wolk . 1988 . Conjugal transfer of DNA to cyanobacteria . Methods Enzymol. 167 : 747 - 754 . (10.1016/0076-6879(88)67086-8) / Methods Enzymol. / Conjugal transfer of DNA to cyanobacteria by Elhai J. (1988)
  21. Elhai , J. , and C. P. Wolk . 1988 . A versatile class of positiveselection vectors based on the non-viability of palindrome-containing plasmids that allows cloning into long polylinkers . Gene 68 : 119 - 138 . (10.1016/0378-1119(88)90605-1) / Gene / A versatile class of positiveselection vectors based on the non-viability of palindrome-containing plasmids that allows cloning into long polylinkers by Elhai J. (1988)
  22. Ernst , A. , T. Black , Y. Cai , J. -M. Panoff , D. N. Tiwari , and C. P. Wolk . 1992 . Synthesis of nitrogenase in mutants of the cyanobacterium Anabaena sp. strain 7120 affected in heterocyst development or metabolism . J. Bacteriol. 174 : 6025 - 6032 . (10.1128/jb.174.19.6025-6032.1992) / J. Bacteriol. / Synthesis of nitrogenase in mutants of the cyanobacterium Anabaena sp. strain 7120 affected in heterocyst development or metabolism by Ernst A. (1992)
  23. Fernandez-Pifias F. F. Leganes and C. P. Wolk. Unpublished data.
  24. Fuma , S. , Y. Fujishima , N. Corbell , C. D'Souza , M. M. Nakano , P. Zuber , and K. Yamane . 1993 . Nucleotide sequence of 5' portion of srfA that contains the region required for competence establishment in Bacillus subtilis . Nucleic Acids Res. 21 : 93 - 97 . (10.1093/nar/21.1.93) / Nucleic Acids Res. / Nucleotide sequence of 5' portion of srfA that contains the region required for competence establishment in Bacillus subtilis by Fuma S. (1993)
  25. Furste , J. P. , W. Pansegrau , R. Frank , H. Blocker , P. Scholz , M. Bagdasarian , and E. Lanka . 1986 . Molecular cloning of the plasmid RP4 primase region in a multi-host-range tacP expression vector . Gene 48 : 119 - 131 . (10.1016/0378-1119(86)90358-6) / Gene / Molecular cloning of the plasmid RP4 primase region in a multi-host-range tacP expression vector by Furste J. P. (1986)
  26. Grossman , T. H. , M. Tuckman , S. Ellestad , and M. S. Osbourne . 1993 . Isolation and characterization of Bacillus subtilis genes involved in siderophore biosynthesis: relationship between B. subtilis sfp° and Escherichia coli entD genes . J. Bacteriol. 175 : 6203 - 6211 . (10.1128/JB.175.19.6203-6211.1993) / J. Bacteriol. / Isolation and characterization of Bacillus subtilis genes involved in siderophore biosynthesis: relationship between B. subtilis sfp° and Escherichia coli entD genes by Grossman T. H. (1993)
  27. Gutierrez , S. , B. Diez , E. Montenegro , and J. F. Martin . 1991 . Characterization of the Cephalosporium acremonium pcbAB gene encoding ot-aminoadipyl-cysteinyl-valine synthetase, a large multidomain peptide synthetase: linkage to the pcbC gene as a cluster of early cephalosporin biosynthetic genes and evidence of multiple functional domains . J. Bacteriol. 173 : 2354 - 2365 . (10.1128/JB.173.7.2354-2365.1991) / J. Bacteriol. / Characterization of the Cephalosporium acremonium pcbAB gene encoding ot-aminoadipyl-cysteinyl-valine synthetase, a large multidomain peptide synthetase: linkage to the pcbC gene as a cluster of early cephalosporin biosynthetic genes and evidence of multiple functional domains by Gutierrez S. (1991)
  28. Hallam , S. E. , F. Malpartida , and D. A. Hopwood . 1988 . Nucleotide sequence, transcription and deduced function of a gene involved in polyketide antibiotic synthesis in Streptomyces coelicolor . Gene 74 : 305 - 320 . (10.1016/0378-1119(88)90165-5) / Gene / Nucleotide sequence, transcription and deduced function of a gene involved in polyketide antibiotic synthesis in Streptomyces coelicolor by Hallam S. E. (1988)
  29. Hopwood , D. A. , and D. H. Sherman . 1990 . Molecular genetics of polyketides and its comparison to fatty acid biosynthesis. Annu . Rev. Genet. 24 : 37 - 66 . (10.1146/annurev.ge.24.120190.000345) / Rev. Genet. / Molecular genetics of polyketides and its comparison to fatty acid biosynthesis. Annu by Hopwood D. A. (1990)
  30. Hu , N. - T. , T. Thiel , T. H. Giddings , and C. P. Wolk . 1982 . Anabaena and Nostoc cyanophages from sewage settling ponds . Virology 114 : 236 - 246 . (10.1016/0042-6822(81)90269-5) / Virology / Anabaena and Nostoc cyanophages from sewage settling ponds by Hu N. (1982)
  31. Kratzschmar , J. , M. Krause , and M. A. Marahiel . 1989 . Gramicidin S biosynthesis operon containing the structural genes grsA and grsB has an open reading frame encoding a protein homologous to fatty acid thioesterases . J. Bacteriol. 171 : 5422 - 5429 . (10.1128/jb.171.10.5422-5429.1989) / J. Bacteriol. / Gramicidin S biosynthesis operon containing the structural genes grsA and grsB has an open reading frame encoding a protein homologous to fatty acid thioesterases by Kratzschmar J. (1989)
  32. Lampa , G. , and C. Jacks . 1991 . Analysis of two linked genes coding for the acyl carrier protein (ACP) from Arabidopsis thaliana (Columbia) . Plant Mol. Biol. 16 : 469 - 474 . (10.1007/BF00023997) / Plant Mol. Biol. / Analysis of two linked genes coding for the acyl carrier protein (ACP) from Arabidopsis thaliana (Columbia) by Lampa G. (1991)
  33. Liang , J. , L. Scappino , and R. Haselkorn . 1992 . The patA gene product, which contains a region similar to CheY of Eschenichia coli, controls heterocyst pattern formation in the cyanobacterium Anabaena 7120 . Proc. Natl. Acad. Sci. USA 89 : 5655 - 5659 . (10.1073/pnas.89.12.5655) / Proc. Natl. Acad. Sci. USA / The patA gene product, which contains a region similar to CheY of Eschenichia coli, controls heterocyst pattern formation in the cyanobacterium Anabaena 7120 by Liang J. (1992)
  34. Lipmann , F. 1980 . Bacterial production of antibiotic polypeptides by thiol-linked synthesis on protein templates . Adv. Microb. Physiol. 21 : 227 - 260 . (10.1016/S0065-2911(08)60357-4) / Adv. Microb. Physiol. / Bacterial production of antibiotic polypeptides by thiol-linked synthesis on protein templates by Lipmann F. (1980)
  35. Maniatis T. E. F. Fritsch and J. Sambroolk 1982. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Cold Spring Harbor N.Y.
  36. Morris , M. E. , and S. Jinks-Robinson . 1991 . Nucleotide sequence of the LYS2 gene of Saccharomyces cerevisiae: homology to Bacillus brevis tyrocidine synthetase 1 . Gene 98 : 141 - 145 . (10.1016/0378-1119(91)90117-T) / Gene / Nucleotide sequence of the LYS2 gene of Saccharomyces cerevisiae: homology to Bacillus brevis tyrocidine synthetase 1 by Morris M. E. (1991)
  37. Nakano , M. M. , N. Corbell , J. Benson , and P. Zuber . 1992 . Isolation and characterization of sfr: a gene that functions in the production of the lipopeptide biosurfactant, surfactin, in Bacillus subtilis . Mol. Gen. Genet. 232 : 313 - 321 . (10.1007/BF00280011) / Mol. Gen. Genet. / Isolation and characterization of sfr: a gene that functions in the production of the lipopeptide biosurfactant, surfactin, in Bacillus subtilis by Nakano M. M. (1992)
  38. Peltoketo , H. , V. Isomaa , 0. Maentausta , and R. V. Vihko . 1988 . Complete amino acid sequence of human placental 17p-hydroxysteroid dehydrogenase . FEBS Lett. 239 : 73 - 77 . (10.1016/0014-5793(88)80548-9) / FEBS Lett. / Complete amino acid sequence of human placental 17p-hydroxysteroid dehydrogenase by Peltoketo H. (1988)
  39. Peoples , 0. P. , and A. J. Sinskey . 1989 . Poly-3-hydroxybutyrate biosynthesis in Alcaligenes eutrophus H16 . J. Biol. Chem. 264 : 15293 - 15297 . (10.1016/S0021-9258(19)84824-X) / J. Biol. Chem. / Poly-3-hydroxybutyrate biosynthesis in Alcaligenes eutrophus H16 by Peoples 0. (1989)
  40. Rawlings , M. , and J. E. Cronan , Jr. 1992 . The gene encoding Escherichia coli acyl carrier protein lies within a cluster of fatty acid biosynthetic genes . J. Biol. Chem. 267 : 5751 - 5754 . (10.1016/S0021-9258(18)42616-6) / J. Biol. Chem. / The gene encoding Escherichia coli acyl carrier protein lies within a cluster of fatty acid biosynthetic genes by Rawlings M. (1992)
  41. Slabas , A. R. , D. Chase , I. Nishida , N. Murata , C. Sidebottom , R. Safford , P. S. Sheldon , R. G. 0. Kekwick , D. G. Hardie , and R. W. MacKintosh . 1992 . Molecular cloning of higher-plant 3-oxoacyl(acyl carrier protein) reductase. Sequence identities with the nodG-gene product of the nitrogen-fixing soil bacterium Rhizobium meliloti . Biochem. J. 283 : 321 - 326 . (10.1042/bj2830321) / Biochem. J. / Molecular cloning of higher-plant 3-oxoacyl(acyl carrier protein) reductase. Sequence identities with the nodG-gene product of the nitrogen-fixing soil bacterium Rhizobium meliloti by Slabas A. R. (1992)
  42. Thomas , J. , J. C. Meeks , C. P. Wolk , P. W. Shaffer , S. M. Austin , and W. -S. Chien . 1977 . Formation of glutamine from [13N]ammonia, [13N]dinitrogen, and ['4C]glutamate by heterocysts isolated from Anabaena cylindrica . J. Bacteriol. 129 : 1545 - 1555 . (10.1128/JB.129.3.1545-1555.1977) / J. Bacteriol. / Formation of glutamine from [13N]ammonia, [13N]dinitrogen, and ['4C]glutamate by heterocysts isolated from Anabaena cylindrica by Thomas J. (1977)
  43. Turgay , K. , M. Krause , and M. A. Marahiel . 1992 . Four homologous domains in the primary structure of GrsB are related to domains in a superfamily of adenylate-forming enzymes . Mol. Microbiol. 6 : 529 - 546 . (10.1111/j.1365-2958.1992.tb01498.x) / Mol. Microbiol. / Four homologous domains in the primary structure of GrsB are related to domains in a superfamily of adenylate-forming enzymes by Turgay K. (1992)
  44. Vieira , J. , and J. Messing . 1982 . The pUC plasmids, an M13mp 7- derived system for insertion mutagenesis and sequencing with synthetic universal primers . Gene 19 : 259 - 268 . (10.1016/0378-1119(82)90015-4) / Gene / The pUC plasmids, an M13mp 7- derived system for insertion mutagenesis and sequencing with synthetic universal primers by Vieira J. (1982)
  45. Vieira , J. , and J. Messing . 1987 . Production of single-stranded DNA . Methods Enzymol. 153 : 3 - 11 . (10.1016/0076-6879(87)53044-0) / Methods Enzymol. / Production of single-stranded DNA by Vieira J. (1987)
  46. Wilcox , M. , G. J. Mitchison , and R. J. Smith . 1973 . Pattern formation in the blue-green alga, Anabaena. I. Basic mechanisms . J. Cell Sci. 12 : 707 - 723 . (10.1242/jcs.12.3.707) / J. Cell Sci. / Pattern formation in the blue-green alga, Anabaena. I. Basic mechanisms by Wilcox M. (1973)
  47. Wilcox , M. , G. J. Mitchison , and R. J. Smith . 1973 . Pattern formation in the blue-green alga, Anabaena. II. Controlled proheterocyst regression . J. Cell Sci. 13 : 637 - 649 . (10.1242/jcs.13.3.637) / J. Cell Sci. / Pattern formation in the blue-green alga, Anabaena. II. Controlled proheterocyst regression by Wilcox M. (1973)
  48. Wolk , C. P. 1967 . Physiological basis of the pattern of vegetative growth of a blue-green alga . Proc. Natl. Acad. Sci. USA 57 : 1246 - 1251 . (10.1073/pnas.57.5.1246) / Proc. Natl. Acad. Sci. USA / Physiological basis of the pattern of vegetative growth of a blue-green alga by Wolk C. P. (1967)
  49. Wolk C. P. 1982. Heterocysts p. 359-386. In N. G. Carr and B. A. Whitton (ed.) The biology of cyanobacteria. Blackwell Scientific Publications London.
  50. Wolk , C. P. 1991 . Genetic analysis of cyanobacterial development . Curr. Opin. Gen. Dev. 1 : 336 - 341 . (10.1016/S0959-437X(05)80297-7) / Curr. Opin. Gen. Dev. / Genetic analysis of cyanobacterial development by Wolk C. P. (1991)
  51. Wolk , C. P. , and M. P. Quine . 1975 . Formation of one-dimensional patterns by stochastic processes and by filamentous blue-green algae . Dev. Biol. 46 : 370 - 382 . (10.1016/0012-1606(75)90113-X) / Dev. Biol. / Formation of one-dimensional patterns by stochastic processes and by filamentous blue-green algae by Wolk C. P. (1975)
  52. Wolk , C. P. , A. Vonshak , P. Kehoe , and J. Elhai . 1984 . Construction of shuttle vectors capable of conjugative transfer from Escherichia coli to nitrogen-fixing filamentous cyanobacteria . Proc. Natl. Acad. Sci. USA 81 : 1561 - 1565 . (10.1073/pnas.81.5.1561) / Proc. Natl. Acad. Sci. USA / Construction of shuttle vectors capable of conjugative transfer from Escherichia coli to nitrogen-fixing filamentous cyanobacteria by Wolk C. P. (1984)
  53. Wolk , C. P. , Y. Cai , and J. -M. Panoff . 1991 . Use of a transposon with Iuciferase as a reporter to identify environmentally responsive genes in a cyanobacterium . Proc. Natl. Acad. Sci. USA 88 : 5355 - 5359 . (10.1073/pnas.88.12.5355) / Proc. Natl. Acad. Sci. USA / Use of a transposon with Iuciferase as a reporter to identify environmentally responsive genes in a cyanobacterium by Wolk C. P. (1991)
  54. Wolk , C. P. , J. Elhai , T. Kuritz , and D. Holland . 1993 . Amplified expression of a transcriptional pattern formed during development of Anabaena. Mol. Microbiol. 7 : 441 - 445 . (10.1111/j.1365-2958.1993.tb01135.x) / Anabaena. Mol. Microbiol. / Amplified expression of a transcriptional pattern formed during development of by Wolk C. P. (1993)
Dates
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Created 8 years, 9 months ago (Nov. 7, 2016, 2:08 p.m.)
Deposited 4 years, 1 month ago (July 29, 2021, 1:21 p.m.)
Indexed 3 weeks, 6 days ago (Aug. 6, 2025, 9:39 a.m.)
Issued 31 years, 5 months ago (April 1, 1994)
Published 31 years, 5 months ago (April 1, 1994)
Published Print 31 years, 5 months ago (April 1, 1994)
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@article{Black_1994, title={Analysis of a Het- mutation in Anabaena sp. strain PCC 7120 implicates a secondary metabolite in the regulation of heterocyst spacing}, volume={176}, ISSN={1098-5530}, url={http://dx.doi.org/10.1128/jb.176.8.2282-2292.1994}, DOI={10.1128/jb.176.8.2282-2292.1994}, number={8}, journal={Journal of Bacteriology}, publisher={American Society for Microbiology}, author={Black, T A and Wolk, C P}, year={1994}, month=apr, pages={2282–2292} }