Gene expression indicates a zone of heterocyst differentiation within the thallus of the cyanolichen Pseudocyphellaria crocata.

Publisher: Wiley on behalf of New Phytologist Trust Country of Publication: England NLM ID: 9882884 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1469-8137 (Electronic) Linking ISSN: 0028646X NLM ISO Abbreviation: New Phytol Subsets: MEDLINE

Publication: Oxford : Wiley on behalf of New Phytologist Trust
Original Publication: London, New York [etc.] Academic Press.

Gene Expression Regulation, Bacterial* ; Genes, Bacterial*; Lichens/*cytology ; Lichens/*genetics ; Nostoc/*cytology; Bacterial Proteins/genetics ; Bacterial Proteins/metabolism ; Blotting, Northern ; Electron Transport Complex IV/genetics ; Electron Transport Complex IV/metabolism ; Fluorescence ; Gene Expression Profiling ; Lichens/metabolism ; Lichens/microbiology ; Microscopy, Confocal ; Nitrogen Fixation ; Nostoc/genetics ; Nostoc/metabolism ; Photosystem II Protein Complex/genetics ; Photosystem II Protein Complex/metabolism ; Phycobilins/metabolism ; RNA, Messenger/genetics ; RNA, Messenger/metabolism ; Reverse Transcriptase Polymerase Chain Reaction ; Symbiosis

Development of the symbiotic association in the bipartite lichen Pseudocyphellaria crocata was investigated by characterizing two regions of the thallus. Thallus organization was examined using microscopy. A HIP1-based differential display technique was modified for use on Nostoc strains, including lichenized strains. Northern hybridization and quantitative real-time polymerase chain reaction were used to confirm differential display results, and determine expression levels of key cyanobacterial genes. Photosystem II yield across the thallus was measured using pulse-amplitude modulated fluorescence. Microscopy revealed structural differences in the thallus margins compared with the centre and identified putative heterocysts in both regions. Differential display identified altered transcript levels in both Nostoc punctiforme and a lichenized Nostoc strain. Transcript abundance of cox2, atpA, and ribA was increased in the thallus margin compared with the centre. Expression of cox2 is heterocyst specific and expression of other heterocyst-specific genes (hetR and nifK) was elevated in the margin, whereas, expression of psbB and PSII yield were not. Structural organization of the thallus margin differed from the centre. Both regions contained putative heterocysts but gene expression data indicated increased heterocyst differentiation in the margins where photosystem II yield was decreased. This is consistent with a zone of heterocyst differentiation within the thallus margin.
(© 2012 The Authors. New Phytologist © 2012 New Phytologist Trust.)

Comment in: New Phytol. 2012 Nov;196(3):657-660. doi: 10.1111/j.1469-8137.2012.04361.x. (PMID: 23043588)

Bergman B, Hallbom L. 1981. Nostoc of Peltigera canina when lichenized and isolated. Canadian Journal of Botany 60: 2092-2098.
Bergman B, Rai A. 1989. The Nostoc-Nephroma symbiosis: localization, distribution pattern and levels of key proteins involved in nitrogen and carbon metabolism of the cyanobiont. Physiologia Plantarum 77: 216-224.
Bhaya D, Vaulot D, Amin P, Takahashi AW, Grossman AR. 2000. Isolation of regulated genes of the cyanobacterium Synechocystis sp. strain PCC 6803 by differential display. Journal of Bacteriology 182: 5692-5699.
Buikema WJ, Haselkorn R. 1991. Characterization of a gene controlling heterocyst differentiation in the cyanobacterium Anabaena-7120. Genes & Development 5: 321-330.
Campbell EL, Summers ML, Christman H, Martin ME, Meeks JC. 2007. Global gene expression patterns of Nostoc punctiforme in steady-state dinitrogen-grown heterocyst-containing cultures and at single time points during the differentiation of akinetes and hormogonia. Journal of Bacteriology 189: 5247-5256.
Elhai J, Wolk CP. 1990. Developmental regulation and spatial pattern of expression of the structural genes for nitrogenase in the cyanobacterium Anabaena. The EMBO Journal 9: 3379-3388.
Enderlin CS, Meeks JC. 1983. Pure culture and reconstitution of the Anthoceros-Nostoc symbiotic association. Planta 158: 157-165.
Flores E, Herrero A. 2010. Compartmentalized function through cell differentiation in filamentous cyanobacteria. Nature Reviews Microbiology 8: 39-50.
Frias JE, Flores E, Herrero A. 1994. Requirement of the regulatory protein NtcA for the expression of nitrogen assimilation and heterocyst development genes in the cyanobacterium Anabaena sp. PCC 7120. Molecular Microbiology 14: 823-832.
Galloway DJ. 1988. Studies in Pseudocyphellaria (lichens). I. The New Zealand species. Bulletin of the British Museum of Natural History (Botany) 17: 1-267.
Ginn HP, Pearson LA, Neilan BA. 2010. NtcA from Microcystis aeruginosa PCC 7806 is autoregulatory and binds to the microcystin promoter. Applied and Environmental Microbiology 76: 4362-4368.
Gupta A, Morby AP, Turner JS, Whitton BA, Robinson NJ. 1993. Deletion within the metallothionein locus of cadmium-tolerant Synechococcus PCC 6301 involving a highly iterated palindrome (HIP1). Molecular Microbiology 7: 189-195.
Henriksson E. 1961. Studies in the physiology of the lichen collema. IV. The occurrence of polysaccharides and some vitamins outside the cells of the phycobiont, Nostoc sp. Physiologia Plantarum 14: 813-817.
Hill DJ. 1989. The control of the cell cycle in microbial symbionts. New Phytologist 112: 175-184.
Honegger R. 1993. Developmental biology of lichens. New Phytologist 125: 659-677.
Johansson C, Bergman B. 1992. Early events during the establishment of the Gunnera/Nostoc symbiosis. Planta 188: 403-413.
Jones KM, Haselkorn R. 2002. Newly identified cytochrome c oxidase operon in the nitrogen-fixing cyanobacterium Anabaena sp. strain PCC 7120 specifically induced in heterocysts. Journal of Bacteriology 184: 2491-2499.
Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R et al. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947-2948.
Meeks JC. 1998. Symbiosis between nitrogen-fixing cyanobacteria and plants - the establishment of symbiosis causes dramatic morphological and physiological changes in the cyanobacterium. BioScience 48: 266-276.
Meeks JC, Elhai J. 2002. Regulation of cellular differentiation in filamentous cyanobacteria in free-living and plant-associated symbiotic growth states. Microbiology and Molecular Biology Reviews 66: 94-121.
Meeks JC, Elhai J, Thiel T, Potts M, Larimer F, Lamerdin J, Predki P, Atlas R. 2001. An overview of the genome of Nostoc punctiforme, a multicellular, symbiotic cyanobacterium. Photosynthesis Research 70: 85-106.
Paulsrud P, Lindblad P. 1998. Sequence variation of the tRNALeu intron as a marker for genetic diversity and specificity of symbiotic cyanobacteria in some lichens. Applied and Environmental Microbiology 64: 310-315.
Paz-Yepes J, Flores E, Herrero A. 2009. Expression and mutational analysis of the glnB genomic region in the heterocyst-forming cyanobacterium Anabaena sp. strain PCC 7120. Journal of Bacteriology 191: 2353-2361.
Rai AN, Soderback E, Bergman B. 2000. Cyanobacterium-plant symbioses. New Phytologist 147: 449-481.
Robinson NJ, Robinson PJ, Gupta A, Bleasby AJ, Whitton BA, Morby AP. 1995. Singular over-representation of an octameric palindrome, HIP1, in DNA from many cyanobacteria. Nucleic Acids Research 23: 729-735.
Soule T, Garcia-Pichel F, Stout V. 2009. Gene expression patterns associated with the biosynthesis of the sunscreen scytonemin in Nostoc punctiforme ATCC 29133 in response to UVA radiation. Journal of Bacteriology 191: 4639-4646.
Stewart WDP, Rowell P, Rai AN. 1983. Cyanobacteria-eukaryotic plant symbioses. Annales de Microbiologie (Institut Pasteur) 134(B): 205-228.
Summerfield TC, Eaton-Rye JJ. 2006. Pseudocyphellaria crocata, P. neglecta and P. perpetua from the Northern and Southern Hemispheres are a phylogenetic species and share cyanobionts. New Phytologist 170: 597-607.
Summerfield TC, Galloway DJ, Eaton-Rye JJ. 2002. Species of cyanolichens from Pseudocyphellaria with indistinguishable ITS sequences have different photobionts. New Phytologist 155: 121-129.
Summerfield TC, Shand JA, Bentley FK, Eaton-Rye JJ. 2005. PsbQ (sll1638) in Synechocystis sp. PCC 6803 is required for photosystem II activity in specific mutants and in nutrient-limiting conditions. Biochemistry 44: 805-815.
Summers ML, Wallis JG, Campbell EL, Meeks JC. 1995. Genetic evidence of a major role for glucose-6-phosphate dehydrogenase in nitrogen fixation and dark growth of the cyanobacterium Nostoc sp. strain ATCC 29133. Journal of Bacteriology 177: 6184-6194.
Valladares A, Herrero A, Pils D, Schmetterer G, Flores E. 2003. Cytochrome c oxidase genes required for nitrogenase activity and diazotrophic growth in Anabaena sp. PCC 7120. Molecular Microbiology 47: 1239-1249.
Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F. 2002. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biology 3: Research0034. 1-11.
Wastyn M, Achatz A, Molitor V, Peschek GA. 1988. Respiratory activities and aa3-type cytochrome-oxidase in plasma and thylakoid membranes from vegetative cells and heterocysts of the cyanobacterium Anabaena ATCC 29413. Biochimica et Biophysica Acta 935: 217-224.
Wei TF, Ramasubramanian TS, Golden JW. 1994. Anabaena sp. strain PCC 7120 ntcA gene required for growth on nitrate and heterocyst development. Journal of Bacteriology 176: 4473-4482.
Whitton BA, Potts M. 2002. Introduction to the cyanobacteria. In: Whitton BA, Potts M, eds. The ecology of cyanobacteria. Dordrecht, the Netherlands: Kluwer Academic Publishers, 1-11.
Wolk CP, Ernst A, Elhai J. 1994. Heterocyst metabolism and development. In: Bryant DA, ed. The molecular biology of cyanobacteria. Dordecht, the Netherlands: Kluwer Academic Press, 769-823.
Wong FCY, Meeks JC. 2001. The hetF gene product is essential to heterocyst differentiation and affects hetR function in the cyanobacterium Nostoc punctiforme. Journal of Bacteriology 183: 2654-2661.
Woodger FJ, Badger MR, Price GD. 2003. Inorganic carbon limitation induces transcripts encoding components of the CO2-concentrating mechanism in Synechococcus sp. PCC 7942 through a redox-independent pathway. Plant Physiology 133: 2069-2080.
Yang G, Bhuvaneswari TV, Joseph CM, King MD, Phillips DA. 2002. Roles for riboflavin in the Sinorhizobium-alfalfa association. Molecular Plant-Microbe Interactions 15: 456-462.

0 (Bacterial Proteins)
0 (Photosystem II Protein Complex)
0 (Phycobilins)
0 (RNA, Messenger)
135434-42-3 (HetR protein, Bacteria)
EC 1.9.3.1 (Electron Transport Complex IV)

Date Created: 20120831 Date Completed: 20130308 Latest Revision: 20210416

20250114

10.1111/j.1469-8137.2012.04272.x

22931432