Abstract
Cyanobacteria are distributed globally in the sea, fresh water, and land. Akinetes (dormant cells) of cyanobacteria are highly resistant to dry conditions, contributing to the survival of terrestrial cyanobacteria. However, the substances that regulate akinete dormancy and germination have not been elucidated. The present study investigated the effects of the phytohormone cytokinin (CK), on the germination stage of a terrestrial filamentous cyanobacterium, Nostoc sp. HK-01. In the cell suspensions of Nostoc sp. HK-01, isopentenyladenine (iP), isopentenyladenosine (iPR), cis-zeatin (cZ), cis-zeatinriboside (cZR), trans-zeatin (tZ), and a trace amount of trans-zeatinriboside (tZR) were identified, according to their retention times and multiple reaction monitoring (MRM) transitions, using high performance liquid chromatography and electrospray ionization tandem mass spectrometry (HPLC-ESI-MS/MS). Product ion scans also identified iP, iPR, cZ, and cZR. The present study established an isolation method for the dormant Nostoc akinetes, and then treated them with CKs. iP and tZ promoted the germination of akinetes, while cZ did not. S-4893, which is a CK antagonist, inhibited germination and the promotive activity of the applied iP. The results strongly suggest that cyanobacteria have a very similar perception system to plants, and that they regulate the dormancy and germination of their own cells and/or other cells via CKs. The production of CKs by several species of cyanobacteria was previously reported. However, this is the first investigation showing the role of phytohormones in the dormant cell physiology of cyanobacteria.
Similar content being viewed by others
Abbreviations
- BA:
-
Benzyl adenine
- CE:
-
Collision energy
- CK:
-
Cytokinin
- cZ:
-
cis-Zeatin
- cZR:
-
cis-Zeatinriboside
- DHZ:
-
Dihydrozeatin
- DMSO:
-
Dimethyl sulfoxide
- EPS:
-
Extracellular polysaccharides
- HPLC-ESI-MS/MS:
-
High performance liquid chromatography and electrospray ionization tandem mass spectrometry
- iP:
-
Isopentenyladenine
- iPR:
-
Isopentenyladenosine
- tZ:
-
trans-Zeatin
- tZR:
-
trans-Zeatinriboside
References
Adams GD, Duggan SP (1999) Heterocyst and akinete differentiation in cyanobacteria. New Phytol 144:3–33. https://doi.org/10.1046/j.1469-8137.1999.00505.x
Allen CJ, Lacey RF, Bickford B, Alixandri B, Beshears CP, Gilmartin C, Binder BM (2019) Cyanobacteria respond to low levels of ethylene. Front Plant Sci 10(950). https://doi.org/10.3389/fpls.2019.00950
Anantharaman V, Aravind L (2001) The CHASE domain: a predicted ligand-binding module in plant cytokinin receptors and other eukaryotic and bacterial receptors. Trends Biochem Sci 26:579–582. https://doi.org/10.1016/S0968-0004(01)01968-5
Arata Y, Nagasawa-Iida A, Uneme H, Nakajima H, Kakimoto T, Sato R (2010) The phenylquinazoline compound S-4893 is a non-competitive cytokinin antagonist that targets Arabidopsis cytokinin receptor CRE1 and promotes root growth in Arabidopsis and rice. Plant Cell Physiol 51:2047–2059. https://doi.org/10.1093/pcp/pcq163
Archibald JM (2015) Endosymbiosis and eukaryotic cell evolution. Curr Biol 25:R911–R921. https://doi.org/10.1016/j.cub.2015.07.055
Barták P, Bednář P, Stránský Z, Boček P, Vespalec R (2000) Determination of dissociation constants of cytokinins by capillary zone electrophoresis. J Chromatogr A 878:249–259. https://doi.org/10.1016/S0021-9673(00)00245-4
Cameron RE (1962) Species of Nostoc vaucher occurring in the sonoran desert in Arizona. Trans Am Microsc Soc 81:379–384. https://doi.org/10.2307/3223790
Carpenter EJ, Romans K (1991) Major role of the cyanobacterium Trichodesmium in nutrient cycling in the North Atlantic Ocean. Science 254:1356–1358. https://doi.org/10.1126/science.254.5036.1356
De Philippis R, Vincenzini M (1998) Exocellular polysaccharides from cyanobacteria and their possible applications. FEMS Microbiol Rev 22:151–175. https://doi.org/10.1111/j.1574-6976.1998.tb00365.x
Fisher RW, Wolk CP (1976) Substance stimulating the differentiation of spores of the blue-green alga Cylindrospermum licheniforme. Nature 259:394–395. https://doi.org/10.1038/259394a0
Frébortová J, Greplová M, Seidl MF, Heyl A, Frébort I (2015) Biochemical characterization of putative adenylate dimethylallyltransferase and cytokinin dehydrogenase from Nostoc sp. PCC 7120. PLoS One 10:e0138468. https://doi.org/10.1371/journal.pone.0138468
Frébortová J, Plíhal O, Florová V, Kokáš F, Kubiasová K, Greplová M, Šimura J, Novák O, Frébort I (2017) Light influences cytokinin biosynthesis and sensing in Nostoc (cyanobacteria). J Phycol 53:703–714. https://doi.org/10.1111/jpy.12538
Golubic S, Sergeev VN, Knoll AH (1995) Mesoproterozoic Archaeoellipsoides: akinetes of heterocystous cyanobacteria. Lethaia 28:285–298. https://doi.org/10.1111/j.1502-3931.1995.tb01817.x
Hilhorst HWM, Karssen CM (1992) Seed dormancy and germination: the role of abscisic acid and gibberellins and the importance of hormone mutants. Plant Growth Regul 11:225–238. https://doi.org/10.1007/BF00024561
Hirosawa T, Wolk CP (1979a) Factors controlling the formation of Akinetes adjacent to Heterocysts in the cyanobacterium Cylindrospermum licheniforme Kütz. Microbiology 114:423–432. https://doi.org/10.1099/00221287-114-2-423
Hirosawa T, Wolk CP (1979b) Isolation and characterization of a substance which stimulates the formation of Akinetes in the cyanobacterium Cylindrospermum licheniforme Kütz. Microbiology 114:433–441. https://doi.org/10.1099/00221287-114-2-433
Hussain A, Krischke M, Roitsch T, Hasnain S (2010) Rapid determination of cytokinins and auxin in cyanobacteria. Curr Microbiol 61:361–369. https://doi.org/10.1007/s00284-010-9620-7
Hwang I, Sheen J, Müller B (2012) Cytokinin signaling networks. Annu Rev Plant Biol 63:353–380. https://doi.org/10.1146/annurev-arplant-042811-105503
Inoue T, Higuchi M, Hashimoto Y, Seki M, Kobayashi M, Kato T, Tabata S, Shinozaki K, Kakimoto T (2001) Identification of CRE1 as a cytokinin receptor from Arabidopsis. Nature 409:1060–1063. https://doi.org/10.1038/35059117
Kaplan-Levy RN, Hadas O, Summers ML, Rücker J, Sukenik A (2010) Akinetes: dormant cells of cyanobacteria. In: Lubzens E, Cerdá J, Clark MS (eds) Topic in current genetics 21; dormancy and resistance in harsh environments. Springer, Heidelberg/Dordrecht/London/SNew York, pp 5–27. https://doi.org/10.1007/978-3-642-12422-8_2
Kapoor K, Sharma VK (1981) Effect of growth-promoting chemicals on growth, nitrogen fixation and heterocyst frequency of a blue-green alga. Z Allg Mikrobiol 21:305–311. https://doi.org/10.1002/jobm.19810210406
Katoh H, Shiga Y, Nakahira Y, Ohmori M (2003) Isolation and characterization of a drought-tolerant cyanobacterium, Nostoc sp. HK-01. Microbes Environ 18:82–88. https://doi.org/10.1264/jsme2.18.82
Kermode AR (2005) Role of abscisic acid in seed dormancy. J Plant Growth Regul 24:319–344. https://doi.org/10.1007/s00344-005-0110-2
Kieninger AK, Forchhammer K, Maldener I (2019) A nanopore array in the septal peptidoglycan hosts gated septal junctions for cell-cell communication in multicellular cyanobacteria. Int J Med Microbiol 309:151303. https://doi.org/10.1016/j.ijmm.2019.03.007
Kimura S, Tomita-Yokotani K, Igarashi Y, Sato S, Katoh H, Abe T, Sonoike K, Ohmori M (2015) The heat tolerance of dry colonies of a terrestrial cyanobacterium, Nostoc sp. HK-01. Biol Sci Space 29:12–18. https://doi.org/10.2187/bss.29.12
Kimura S, Ong M, Ichikawa S, Tomita-Yokotani K (2017a) Compatible solutes in the akinetes of the terrestrial cyanobacterium Nostoc sp. HK-01 contribute to its heat tolerance. Am J Plant Sci 8:2695–2711. https://doi.org/10.4236/ajps.2017.811181
Kimura S, Tomita-Yokotani K, Katoh H, Sato S, Ohmori M (2017b) Complete life cycle and heat tolerance of dry colonies of a terrestrial cyanobacterium, Nostoc sp. HK-01. Biol Sci Space 31:1–8. https://doi.org/10.2187/bss.31.1
Knoll AH, Summons RE, Waldbauer JR, Zumberge JE (2007) The geological succession of primary producers in the oceans. In: Falkowski PG, Knoll AH (eds) Evolution of primary producers in the sea. Academic, Cambridge, pp 133–163. https://doi.org/10.1016/B978-012370518-1/50009-6
Kuiper D, Kuiper PJ, Lambers H, Schuit J, Staal M (1989) Cytokinin concentration in relation to mineral nutrition and benzyladenine treatment in Plantago major ssp. pleiosperma. Physiol Plant 75:511–517. https://doi.org/10.1111/j.1399-3054.1989.tb05617.x
Lacey RF, Binder BM (2016) Ethylene regulates the physiology of the cyanobacterium Synechocystis sp. PCC 6803 via an ethylene receptor. Plant Physiol 171:2798–2809. https://doi.org/10.1104/pp.16.00602
Leonard NJ (1974) Chemistry of the cytokinins. In: Runeckles VC, Sondheimer E, Walton DC (eds) The chemistry and biochemistry of plant hormones: recent advances in phytochemistry, vol 7. Academic, New York/London, pp 21–56
Lu Y, Xu J (2015) Phytohormones in microalgae: a new opportunity for microalgal biotechnology? Trends Plant Sci 20:273–282. https://doi.org/10.1016/j.tplants.2015.01.006
Lu Y, Tarkowská D, Turečková V, Luo T, Xin Y, Li J, Wang Q, Jiao N, Strnad M, Xu J (2014) Antagonistic roles of abscisic acid and cytokinin during response to nitrogen depletion in oleaginous microalga Nannochloropsis oceanica expand the evolutionary breadth of phytohormone function. Plant J 80:52–68 https://doi.org/10.1111/tpj.12615
Maldener I, Summers ML, Sukenik A (2014) Cellular differentiation in filamentous cyanobacteria. In: Flores E, Herrero A (eds) The cell biology of cyanobacteria. Caister Academic Press, Norfolk, pp 263–291
Mansouri H, Talebizadeh B (2016) Effect of gibberellic acid on the cyanobacterium Nostoc linckia. J Appl Phycol 28:2187–2193. https://doi.org/10.1007/s10811-015-0756-5
Maor R (2010) Compositions and methods for increasing oil content in algae. Google Patents WO2010113149A1
Mariscal V (2014) Cell-cell joining proteins in heterocyst-forming cyanobacteria. In: Flores E, Herrero A (eds) The cell biology of cyanobacteria. Caister Academic Press, Norfolk, pp 293–304
Martin W, Kowallik KV (1999) Annotated English translation of Mereschkowsky’s 1905 paper ‘Über Natur und Ursprung der Chromatophoren im Pflanzenreiche’. Eur J Phycol 34:287–295. https://doi.org/10.1080/09670269910001736342
Miller CO, Skoog F, Von Saltza MH, Strong FM (1955) Kinetin, a cell division factor from deoxyribonucleic acid. J Am Chem Soc 77:1392–1392. https://doi.org/10.1021/ja01610a105
Potts M (2000) Nostoc. In: Whitton BA, Potts M (eds) The ecology of cyanobacteria. Kluwer academic publishers, Dordrecht, pp 465–504. https://doi.org/10.1007/0-306-46855-7_17
Rippka R, Deruelles J, Waterbury JB, Herdman M, Stanier RY (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. Microbiology 111:1–61. https://doi.org/10.1099/00221287-111-1-1
Sakakibara H (2006) Cytokinins: activity, biosynthesis, and translocation. Annu Rev Plant Biol 57:431–449. https://doi.org/10.1146/annurev.arplant.57.032905.105231
Schmitz RY, Skoog F, Playtis AJ, Leonard NJ (1972) Cytokinins: synthesis and biological activity of geometric and position isomers of zeatin. Plant Physiol 50:702–705. https://doi.org/10.1104/pp.50.6.702
Selivankina SY, Zubkova NK, Kupriyanova EV, Lyukevich TV, Kusnetsov VV, Los DA, Kulaeva ON (2006) Cyanobacteria respond to cytokinin. Russ J Plant Physiol 53:751. https://doi.org/10.1134/S1021443706060045
Spiess LD (1975) Comparative activity of isomers of zeatin and ribosyl-zeatin on Funaria hygrometrica. Plant Physiol 55:583–585. https://doi.org/10.1104/pp.55.3.583
Stirk WA, Ördög V, Van Staden J (1999) Identification of the cytokinin isopentenyladenine in a strain of Arthronema africanum (Cyanobacteria). J Phycol 35:89–92. https://doi.org/10.1046/j.1529-8817.1999.3510089.x
Stirk WA, Václavíková K, Novák O, Gajdošová S, Kotland O, Motyka V, Strnad M, van Staden J (2012) Involvement of cis-zeatin, dihydrozeatin, and aromatic cytokinins in germination and seedling establishment of maize, oats, and lucerne. J Plant Growth Regul 31:392–405. https://doi.org/10.1007/s00344-011-9249-1
Sukenik A, Rücker J, Maldener I (2019) Dormant cells (Akinetes) of filamentous cyanobacteria demonstrate a great variability in morphology, physiology, and ecological function. In: Mishra AK, Tiwari DN, Rai AN (eds) Cyanobacteria: from basic science to applications. Academic, Cambridge, pp 65–77
Suzuki T, Nakasato K, Shapiro S, Pomati F, Neilan BA (2004) Effects of synthetic local anaesthetics on the growth of the cyanobacterium Synechococcus leopoliensis. J Appl Phycol 16:145–152. https://doi.org/10.1023/B:JAPH.0000044776.04977.00
Takagi M, Yokota T, Murofushi N, Ota Y, Takahashi N (1985) Fluctuation of endogenous cytokinin contents in rice during its life cycle-quantification of cytokinins by selected ion monitoring using deuterium-labelled internal standards. Agric Biol Chem 49:3271–3277. https://doi.org/10.1271/bbb1961.49.3271
Tsavkelova EA, Klimova SY, Cherdyntseva TA, Netrusov AI (2006a) Microbial producers of plant growth stimulators and their practical use: a review. Appl Biochem Microbiol 42:117–126. https://doi.org/10.1134/S0003683806020013
Tsavkelova EA, Klimova SY, Cherdyntseva TA, Netrusov AI (2006b) Hormones and hormone-like substances of microorganisms: a review. Appl Biochem Microbiol 42:229–235. https://doi.org/10.1134/S000368380603001X
Yamaguchi S (2008) Gibberellin metabolism and its regulation. Annu Rev Plant Biol 59:225–251. https://doi.org/10.1146/annurev.arplant.59.032607.092804
Yamamoto Y (1972) The fatty acid composition of akinetes, heterocysts and vegetative cells in Anabaena cylindrica. Plant Cell Physiol 13:913–915. https://doi.org/10.1093/oxfordjournals.pcp.a074803
Yamamoto Y (1976) Effect of some physical and chemical factors on the germination of akinetes of Anabaena cylindrica. J Gen Appl Microbiol 22:311–323. https://doi.org/10.2323/jgam.22.311
Yokota T, Murofushi N, Takahashi N (1980) Extraction, purification, and identification. In: MacMillan J (ed) Hormonal regulation of development I. Springer, Berlin/Heidelberg, pp 113–201
Yoshimura H, Kotake T, Aohara T, Tsumuraya Y, Ikeuchi M, Ohmori M (2012) The role of extracellular polysaccharides produced by the terrestrial cyanobacterium Nostoc sp. strain HK-01 in NaCl tolerance. J Appl Phycol 24:237–243. https://doi.org/10.1007/s10811-011-9672-5
Žižková E, Kubeš M, Dobrev PI, Přibyl P, Šimura J, Zahajská L, Drábková LZ, Novák O, Motyka V (2017) Control of cytokinin and auxin homeostasis in cyanobacteria and algae. Ann Bot 119:151–166. https://doi.org/10.1093/aob/mcw194
Acknowledgments
This work was supported by Grant-in-Aid for JSPS Fellows (JP17J00274, JP19J00830 to SK), Grant-in-Aid for Scientific Research (B) (18H02142 to MN) and Sasakawa Scientific Research Grant from The Japan Science Society (28-539 to SK). The authors thank Dr. Takao Yokota (Teikyo University, Japan) for internal standards of cytokinin, and thank Dr. Masayuki Ohmori (The University of Tokyo, Japan) and Dr. Hiroshi Katoh (Mie University, Japan) for their useful advice about the genome of cyanobacteria. The authors would like to thank Editage (www.editage.com) for English language editing.
Funding
This work was funded by Grant-in-Aid for JSPS Fellows (JP17J00274, JP19J00830), Grant-in-Aid for Scientific Research (B) (18H02142) and Sasakawa Scientific Research Grant from The Japan Science Society (28-539).
Author information
Authors and Affiliations
Contributions
SK, MN, and KTY designed the experiments. SK, EY, KM, HY, MO, and KTY performed the experiments. SK edited the data, figures, table, and drafted the manuscript. MN, KM, and TA revised the manuscript. MN and TA supervised the project.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Research involving human and animal participants
This article does not contain any studies with human participants or animals performed by any of the authors.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Kimura, S., Nakajima, ., Yumoto, E. et al. Cytokinins affect the akinete-germination stage of a terrestrial filamentous cyanobacterium, Nostoc sp. HK-01. Plant Growth Regul 92, 273–282 (2020). https://doi.org/10.1007/s10725-020-00636-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10725-020-00636-x