Startseite Expression of psbA1 gene in Synechocystis sp. PCC 6803 is influenced by CO2
Artikel Open Access

Expression of psbA1 gene in Synechocystis sp. PCC 6803 is influenced by CO2

  • Ciprian Chiş , Dalton Carmel , luliana Chiş , Aurel Ardelean , Nicolae Dragos und Cosmin Sicora EMAIL logo
Veröffentlicht/Copyright: 10. Mai 2017
Artikel downloaden (PDF)
Open Life Sciences
Aus der Zeitschrift Open Life Sciences Band 12 Heft 1

Abstract

In almost all cyanobacteria a small gene family encodes the photosystem II reaction center D1 proteins that play vital roles in the cell. Recently, several types of this protein were functionally characterised and the conditions for their transcript regulation were identified. One of the D1-encoding genes previously believed to be silent is induced by microaerobic conditions. This gene was first described in Synechocystis sp. PCC 6803 as psbA1 encoding the D1 isoform. When Synechocystis cells are shifted from high to ambient level CO2 we recorded an increase in gene expression, similar, but to a lesser extent, to microaerobic conditions. When synthetic air is used to remove the ambient CO2, the induction of the gene is absent. We documented for the first time that expression of a psbA gene is regulated by the inorganic carbon status of the cell. Our conclusion is that both CO2 and microaerobic conditions are independently influencing the expression of psbA1 gene in Synechocystis sp. PCC 6803. Hence, it is crucial to understand the mechanisms of regulation and function of D1 proteins as it could be used for future bio-technological applications as a virtual tool-box for modulating the function of PSII.

Keywords: Synechocystis; photosystem II; psbA1; D1; photosynthesis; carbon dioxide; microaerobic; qRT-RT-PCR; chlorophyll; fluorescence

1 Introduction

The “Great Oxidation Event” arguably due to the oxygenic photosynthesis by cyanobacteria not only sculpted the early biosphere but also allowed the evolution of higher and complex life forms [1]. During this evolutionary process cyanobacteria have developed specific mechanisms in response to changing environmental conditions to ensure their survival [2]. Expression of different isoforms of proteins beneficial to cell survival under different environmental conditions is one such adaptive strategy. The psbA gene family, encoding multiple forms of D1 proteins of the photosystem II complex in cyanobacteria [3] is such an example.

Many cyanobacterial genomes contain a small family of genes encoding D1 proteins. These different D1 isoforms are employed by cyanobacteria in various response strategies to changing environmental conditions. So far, two major strategies were described, one increasing the amount of transcript for the constitutively expressed D1 isoform and the other exchanging between two different isoforms in response to environmental stress [4–7]. In Synechocystissp. PCC 6803, the psbA gene family includes three genes, psbA1(slr1181), psbA2(slr1311) and psbA3(sll1867) (http://www.kazusa.or.jp/cyano/, http://genome.jgi-psf.org/mic_home.html). The psbA2 and psbA3 coding regions exhibit 99% identity in their nucleotide sequence and encode identical proteins. However, the psbA2 transcript is predominant accounting for 90% of the total D1 protein produced [4]. Hardly ever was the expression of psbA1 noticed and the condition, which caused the induction of the gene, remained enigmatic until [5] distinguished the expressions psbA1 from other isoforms of psbA gene under cells grown under low O2 environment. Concurrently, [6] showed the dramatic expression of psbA1 gene in Synechocystis under microaerobic condition. Presumably, different familes of psbA genes and their multiplicity appears to be not arbitrary, but merely based on environmental factors [7]. Furthermore this widens the possibility of additional environmental parameters involved in the regulation of these families of genes.

Cyanobacteria absorb inorganic carbon in the form of carbon dioxide (CO2) and bicarbonate and the availability of these inorganic carbon sources limits the photosynthetic rate in cyanobacteria [8]. Cyanobacteria have developed various adaptive methods to accommodate a wide range of atmospheric CO2 levels. This intricate process of acclimation follows changes at various cellular levels, including expression regulation of genes involved in the carbon concentrating mechanism (CCM) [9].

In this study, the differential expression of the psbA1 gene under various levels of CO2 was analysed in order to correlate the involvement of various proteins participating in cellular adaptation.

2 Materials and methods

2.1 Culture and growth conditions

Synechocystis sp. PCC 6803 was obtained from the Pasteur Culture Collection, France. Cells were grown in cylindrical glass tubes containing 200 ml of BG-11 medium. The cultures were continuously illuminated at 50 μmol photons m-2s-1 and the temperature was maintained at 30 oC [10]. To ensure thorough nutrient and O2 availability, the cultures were bubbled with air unless stated otherwise. When cells were grown under low CO2 condition, Na2CO3 was omitted from BG-11 medium.

High CO2 to low CO2 shift assay was carried out by bubbling the culture initially with 5% CO2 (High CO2 condition) until the optical density at 730 nm corresponds to 0.8 and the bubbling gas was changed to ambient level CO2 (low CO2 conditions) for the next 120 min. Samples were collected at 0 min, 30 min, 60 min and 120 min. In another experiment the cultures were bubbled with synthetic air, of similar composition to atmospheric air, but completely lacking CO2. Sampling was done at 0 min, 15 min, 60 min, 120 min, 1500 min and after 3000 min. Microaerobic conditions were achieved in the cultures by bubbling with pure N2 gas. Cells were harvested at 0 min, 30 min, 60 min and 120 min. Treatments were run on two separate cultures grown under the same conditions and the experiments were repeated three times to avoid culture-dependent expression variations.

2.2 RNA isolation and cDNA synthesis

The cells were harvested from 10 mL culture (OD730= 0.8) by centrifugation at 8000 rpm, 4 °C, 5 min at previously mentioned sampling point. The cell pellets were immediately suspended in Trizol reagent (Ambion, Life Technologies, California) to prepare total RNA. The concentration of total RNA was measured with a NanoDrop 2000 spectrophotometer (Thermo Scientific, Waltham, MA). RNA samples were treated with 1 U DNase (Turbo DNA free kit, Ambion, Austin, TX) to remove any trace of genomic DNA. Synthesis of cDNA was performed using iScript™ cDNA Synthesis Kit (BioRad, California) using 1.0 μg of purified RNA as template and random hexamer primers.

2.3 Real Time Quantitative Reverse Transcriptase Polymerase Chain Reaction (RT-qRT-PCR)

RT-qRT-PCR was performed in triplicate with a BioRad iQ5 System (BioRad, Berkeley, CA) using Sso Advanced™ SYBR Green Supermix (Bio-Rad, Berkeley, California) in domed cap PCR tubes. Both forward and reverse primers were added at a concentration of 250 nM each in the reaction mix. The PCR protocol is as follows: one cycle of 95 °C for 3 min, followed by 45 cycles of 95 °C for 15 s, 55 °C for 30 s, and 72 °C for 30 s. Negative controls (reactions without cDNA template and minus RT) were included to detect the presence of any DNA contamination. All the reactions were performed in triplicate for each cDNA sample. Specific primers were designed for the detection of psbA1 transcript: forward 5’-3’-AGC-TTA-AAC-CCA-AAA-TCT-TAC-TTC-GT and reverse 5’-3’-CCA-TCA-GAG-AAG-GAG-CCT-TGA-CCA. The expression data were normalized using the level of expression of rnpB as a reference gene using specific primers: forward 5’-3’-CTC-CCG-AAA-GAC-CAG-ACT-TG and reverse 5’-3’- CCG-GGT-TCT-GTT-CTC-TGT-GT, as previously described [6].

2.4 Flash induced chlorophyll fluorescence

Flash-induced chlorophyll fluorescence and subsequent decay was measured using fluorometer (FL-3500, Photon System Instruments, Czech Republic) [11]. Saturating actinic flashes (20 μs) and measuring flashes (8 μs) was provided by instrument’s LED system. The cyanobacterial cells were incubated in dark for 5 min prior to the measurement and then the fluorescence decay was recorded over time range on logarithmic scale both in the presence and in the absence of DCMU((3-(3,4-dichlorophenyl)-1,1-dimethylurea)) [12].

3 Results

In our experiments, the culture exposed to microaerobic conditions displays a strong induction of the psbA1 gene, in direct agreement with previous studies (Fig. 1a) [5–6]. When the Synechocystis cells were shifted from high CO2 to ambient CO2 conditions, the psbA1 gene showed increased expression up to 30-fold within 15 min and remained up-regulated until 120 min under atmospheric CO2 level (Fig. 1b). Nevertheless, a negligible decrease in the expression of psbA1 gene was observed commencing 60 min after treatment while the expression remained well above the control level (Fig. 1b). Interestingly, when the cells are recovered from low CO2 shift, the expression of psbA1 continues to increase compared to the cells subjected to microaerobic conditions where the level of psbA1 decreases and returns to the original level (Fig. 1a,b). During microaerobic treatments, when nitrogen is introduced into the medium in order to remove oxygen, CO2 is lost as well and could be the reason for psbA gene induction. If this is the case we should see an induction independent of the oxygen concentration. To test this hypothesis, cells grown on 5% CO2 conditions were exposed to synthetic air composed solely of oxygen and nitrogen expecting an induction of the gene expression. On the contrary, when the Synechocystis cells were subjected to CO2 free synthetic air, the induction of psbA1 is imperceptible (Fig. 2). The chlorophyll fluorescence decay kinetics in the cells shifted from high CO2 to ambient CO2 after 30 min, showed no significant changes in PSII function of both donor and acceptor side of the photosystem with an electron transfer similar to the cells subjected to microaerobic conditions (Fig. 3).

Figure 1 RT-qRT-PCR Analysis: Expression level of psbA1 gene quantified from cells subjected to microaerobic conditions (a) and under high CO2 to low CO2 shift (b). Measurements were carried out from the cells harvested from control (0 min) and treatments (15 min, 30 min, 60 min and 120 min). Recovery measurements were taken after the cells were shifted back to control conditions at 120 min and 180 min from the start of the experiment.
Figure 1

RT-qRT-PCR Analysis: Expression level of psbA1 gene quantified from cells subjected to microaerobic conditions (a) and under high CO2 to low CO2 shift (b). Measurements were carried out from the cells harvested from control (0 min) and treatments (15 min, 30 min, 60 min and 120 min). Recovery measurements were taken after the cells were shifted back to control conditions at 120 min and 180 min from the start of the experiment.

Figure 2 RT-qRT-PCR Analysis: Expression level of psbA1 gene quantified from cells grown on 5% CO2 and subjected to synthetic air. Measurements were carried out from the cells harvested from control (0 min) and treatments (15 min, 60 min, 120 min, 1500 min and 3000 min).
Figure 2

RT-qRT-PCR Analysis: Expression level of psbA1 gene quantified from cells grown on 5% CO2 and subjected to synthetic air. Measurements were carried out from the cells harvested from control (0 min) and treatments (15 min, 60 min, 120 min, 1500 min and 3000 min).

Figure 3 Influence of microaerobiosis and low CO2 on PSII function: Chlorophyll fluorescence decay kinetics measured from cells grown under microaerobic without DCMU (a) and with DCMU (c) and high CO2 to low CO2 shift without DCMU (b) and with DCMU (d). Measurements were taken for control and treated cells (2h after shift to microaerobic condition and 48h after shift to low CO2).
Figure 3

Influence of microaerobiosis and low CO2 on PSII function: Chlorophyll fluorescence decay kinetics measured from cells grown under microaerobic without DCMU (a) and with DCMU (c) and high CO2 to low CO2 shift without DCMU (b) and with DCMU (d). Measurements were taken for control and treated cells (2h after shift to microaerobic condition and 48h after shift to low CO2).

In cyanobacteria, psbA gene expression is regulated at the various levels of transcription initiation, elongation, and termination, mRNA stability as well as translation [13]. As an attempt to investigate any CO2 responsive regulator controlling the expression of the psbA1 gene, we analyzed the upstream sequence of the psbA1 gene. NdhR, a LysR type regulator, has been shown to control the expression of most of the Ci responsive gene in Synechocystis by binding to a unique signature sequence denoted by a pattern T-N11-A [14,15] presented in Figure 4 as the consensus sequence. Investigation of psbA1 gene sequence also revealed similar palindromic sequence pattern at 146 nucleotide upstream the start codon (Fig. 4) indicating the conceivable regulation by NdhR under low CO2 condition.

Figure 4 Sequence alignment: The probable NdhR-binding site T (N) 11A in the upstream sequence of psbA1 gene. The LysR-type T (N) 11 A motif (consensus) [14–15] was compared to SynechocystispsbA1, sbtA and ndhF3.
Figure 4

Sequence alignment: The probable NdhR-binding site T (N) 11A in the upstream sequence of psbA1 gene. The LysR-type T (N) 11 A motif (consensus) [14–15] was compared to SynechocystispsbA1, sbtA and ndhF3.

4 Discussion

Cyanobacteria redefine their metabolic processes at various level based on the changing environment, which helped their survival during the course of evolution. Establishment of flexible photosynthetic processes remained essential in cyanobacteria as the early photosynthetic machinery became useless due to the formation of the modern oxidative atmosphere [16]. The ancient anoxic environment exhibited a carbon dioxide concentration several orders of magnitude higher than the present atmospheric level. The subsequent modification of atmospheric gas concentrations prompted the development of response mechanisms able to cope with the modern oxidative environment [17].

The D1’ protein encoded by the psbA1 gene in Synechocystis remains unexpressed during growth conditions [10] but is induced when the cells were shifted to microaerobic conditions [5,6]. In both aforementioned studies the microaerobic environment was achieved by bubbling either argon or 99,9% N2 and 0.1% CO2 gas into the culture. Our results with high CO2 (5%) to low CO2 (atmospheric level) shift experiments show a clear induction of the psbA1 gene from Synechocystis sp. PCC 6803 in conditions where the oxygen concentration is constant. A smaller induction under the same conditions was previously recorded in a microarray study [18] but never verified by other methods of investigation until now. Further, we explored the possibility that oxygen does not play any role at all in the induction of psbA gene given the fact that the previously employed methods for obtaining microaerobic conditions [6] were depleting not only oxygen but also other atmospheric gases including CO2 and the induction of psbA1 gene might result from the cumulative effect of O2 and CO2 depletion. Our experiments with synthetic air, containing only oxygen and nitrogen, where the CO2 is completely missing, showed no change in the expression level of psbA1. Hence, the lack of CO2 alone is not sufficient to induce the expression of the gene (Fig. 2). These results allow us to conclude that both O2 and CO2 act as trigger in inducing psbA1 gene expression. The induction by CO2 is triggered by the shift from a higher concentration to atmospheric CO2 levels by unknown mechanisms, which needs to be unravelled. This shows for the first time that one member of the cyanobacterial psbA gene family is under control of CO2 concentration, a fact supported also by the presence in the promoter region of the gene of regulatory elements responsible for carbon regulation (Fig. 4). No such regulatory elements were found in the promoter regions of similar genes from Anabaena sp. PCC 7120 or Thermosynechococcuselongatus BP-1 being an indication that in Synechocystis sp. PCC 6803 we have a specific form of expression regulation (data not shown). In both cases of induction, CO2 or microaerobically triggered, no significant functional changes were recorded on either the donor or the acceptor side of photosystem II. Hence, we conclude that the induction of psbA1 gene in Synechocystis does not generate a modification of the general reaction center function or its photochemistry. This remains similar to normal growth conditions where regularly expressed D1 occupies the PSII reaction centres.

Acknowledgements

The project was partially funded by Romanian National Authority for Scientific Research, CNCS-UEFISCDI, project number: PN-II-IDPCE-2011-3-0765 and the Executive Unit for Financing Higher Education, Research, Development and Innovation (UEFISCDI), Romania, project code PN-II-RU-PD-2011-3-0255.

D.C. was financed by a post-doctoral research fellowship jointly financed by Biological Research Center Jibou and Western University "Vasile Goldis", Arad.

  1. Conflict of interest: Authors state no conflict of interest

References

[1] Buick R., When did oxygenic photosynthesis evolve?, Phil. Trans. R. Soc. B., 2008,363, 2731-274310.1098/rstb.2008.0041Suche in Google Scholar PubMed PubMed Central

[2] Shi T., and Falkowski P.G., Genome evolution in cyanobacteria: The stable core and the variable shell, PNAS., 2008, 105(7), 2510-251510.1073/pnas.0711165105Suche in Google Scholar PubMed PubMed Central

[3] Sugiura M., and Boussac A., Some Photosystem II properties depending on the D1 protein variants in Thermosynechococcuselongates, Biochim Biophys Acta., 2014, 1837(9), 1427-34.10.1016/j.bbabio.2013.12.011Suche in Google Scholar PubMed

[4] Salih G.F., and Jansson C., Activation of the silent psbA1 gene in the cyanobacterium Synechocystis sp strain 6803 produces a nove1 and functional D1 protein, The Plant Cell, 1997, 9, 869-87810.1105/tpc.9.6.869Suche in Google Scholar PubMed PubMed Central

[5] Summerfield T.C., Toepel J., and Sherman L.A., Low-Oxygen Induction of Normally Cryptic psbA Genes in Cyanobacteria, Biochemistry, 2008, 47 (49), 12939-1294110.1021/bi8018916Suche in Google Scholar PubMed

[6] Sicora C.I., Ho F.M., Salminen T., Styring S., Aro E.M., Transcription of a “silent” cyanobacterial psbA gene is induced by microaerobic conditions, Biochim. Biophys. Acta, 2009, 1787,105-11210.1016/j.bbabio.2008.12.002Suche in Google Scholar PubMed

[7] Zhang X., Sherman L.A., Alternate copies of D1 are used by cyanobacteria under different environmental conditions, Photosynth. Res., 2012, 114,133-13510.1007/s11120-012-9783-0Suche in Google Scholar PubMed

[8] Holland S.C., Kappell A.D., Burnap R.L., Redox changes accompanying inorganic carbon limitation in Synechocystis sp. PCC 6803, Biochim. Biophys. Acta, 2015, 1847(3), 355-63.10.1016/j.bbabio.2014.12.001Suche in Google Scholar PubMed

[9] Burnap R.L., Hagemann M., and Kaplan A., Regulation of CO2 Concentrating Mechanism in Cyanobacteria, Life, 2015, 5, 348-37110.3390/life5010348Suche in Google Scholar PubMed PubMed Central

[10] Ripka R., Deruelles J., Waterbury J.B., Herdman, Stanier R.Y., Generic assignments, strain histories and properties of pure cultures of cyanobacteria, J. Gen. Microbiol., 1979, 111, 1-6110.1099/00221287-111-1-1Suche in Google Scholar

[11] Trtilek M., Kramer D.M., Koblizek M., Dual-modulation LED kinetic fluorometer, J. Lumin., 1997, 72-74, 597-599.10.1016/S0022-2313(97)00066-5Suche in Google Scholar

[12] Vass I., Kirilovsky D., Etienne A.L., UV-B radiation-induced donor- and acceptor-side modifications of photosystem II in the cyanobacterium Synechocystis sp. PCC 6803, Biochemistry, 1999, 38(39), 12786-9410.1021/bi991094wSuche in Google Scholar PubMed

[13] Mulo P., Sicora C.I., Aro E.M., Cyanobacterial psbA gene family: optimization of oxygenic photosynthesis, Cell. Mol. Life Sci., 2009, 66, 3697-371010.1007/s00018-009-0103-6Suche in Google Scholar PubMed PubMed Central

[14] Figge R.M., Chauvat C.C., Chauvat F., Cerff R., Characterization and analysis of an NAD(P)H dehydrogenase transcriptional regulator critical for the survival of cyanobacteria facing inorganic carbon starvation and osmotic stress, Mol. Microbiol., 2001, 39, 455-46810.1046/j.1365-2958.2001.02239.xSuche in Google Scholar PubMed

[15] Carmel D., Dahlström K.M., Holmström M., Allahverdiyeva Y., Battchikova N., Aro E.M., Salminen T.A., Mulo P., Structural model, physiology and regulation of Slr0006 in Synechocystis PCC 6803, Arch. Microbiol. 2013, 195, 727-736.Suche in Google Scholar

[16] Kupriyanova E.V., Samylina O.S., CO2-concentrating mechanism and its traits in haloalkaliphilic cyanobacteria, Microbiol., 2015, 84 (2), 112-124.10.1134/S0026261715010075Suche in Google Scholar

[17] Catling D.C., Glein C.R., Zahnle K.J., Mckay C.P., Why O2 Is Required by Complex Life on Habitable Planets and the Concept of Planetary “Oxygenation Time”, Astrobiology, 2005, 5(3), 415-43810.1089/ast.2005.5.415Suche in Google Scholar PubMed

[18] Wang H.L., Postier B.L., Burnap R.L., Alterations in global patterns of gene expression in Synechocystis sp. PCC 6803 in response to inorganic carbon limitation and the inactivation of ndhR, a LysR family regulator, J. Biol. Chem., 2004, 279, 5739-575110.1074/jbc.M311336200Suche in Google Scholar PubMed

Received: 2016-8-5
Accepted: 2017-3-8
Published Online: 2017-5-10

© 2017 Ciprian Chiş et al.

This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 3.0 License.

Artikel in diesem Heft

  1. Research Articles
  2. Field Performance and Genetic Fidelity of Micropropagated Plants of Coffea canephora (Pierre ex A. Froehner)
  3. Research Articles
  4. Foliage maturity of Quercus ilex affects the larval development of a Croatian coastal population of Lymantria dispar (Lepidoptera: Erebidae)
  5. Research Articles
  6. Structural and functional impact of SNPs in P-selectin gene: A comprehensive in silico analysis
  7. Research Articles
  8. High embryogenic ability and regeneration from floral axis of Amorphophallus konjac (Araceae)
  9. Research Articles
  10. Terpene content of wine from the aromatic grape variety ‘Irsai Oliver’ (Vitis vinifera L.) depends on maceration time
  11. Research Articles
  12. Light and smell stimulus protocol reduced negative frontal EEG asymmetry and improved mood
  13. Research Articles
  14. Swailing affects seed germination of plants of European bio-and agricenosis in a different way
  15. Research Articles
  16. Survey analysis of soil physicochemical factors that influence the distribution of Cordyceps in the Xiahe Region of Gansu Province
  17. Research Articles
  18. Production of biogas: relationship between methanogenic and sulfate-reducing microorganisms
  19. Research Articles
  20. Pentraxin 3 and atherosclerosis among type 2 diabetic patients
  21. Research Articles
  22. Evaluation of ribosomal P0 peptide as a vaccine candidate against Argulus siamensis in Labeo rohita
  23. Research Articles
  24. Variation of autosomes and X chromosome STR in breast cancer and gynecological cancer tissues
  25. Research Articles
  26. Response of antioxidant enzymes to cadmium-induced cytotoxicity in rat cerebellar granule neurons
  27. Research Articles
  28. Cardiac hypertrophy and IGF-1 response to testosterone propionate treatment in trained male rats
  29. Research Articles
  30. BRAF-activated non-protein coding RNA (BANCR) advances the development of esophageal squamous cell carcinoma via cell cycle
  31. Research Articles
  32. The influence of soil salinity on volatile organic compounds emission and photosynthetic parameters of Solanum lycopersicum L. varieties
  33. Research Articles
  34. Simple Protocol for immunoglobulin G Purification from Camel “Camelus dromedarius” Serum
  35. Research Articles
  36. Expression of psbA1 gene in Synechocystis sp. PCC 6803 is influenced by CO2
  37. Research Articles
  38. Frequency of Thrombophilic Gene Mutations in Patients with Deep Vein Thrombosis and in Women with Recurrent Pregnancy Loss
  39. Research Articles
  40. Evaluation of anticancer properties of a new α-methylene-δ-lactone DL-249 on two cancer cell lines
  41. Research Articles
  42. Impact of heated waters on water quality and macroinvertebrate community in the Narew River (Poland)
  43. Research Articles
  44. Effects of Some Additives on In Vitro True Digestibility of Wheat and Soybean Straw Pellets
  45. Research Articles
  46. RNAi-mediated gene silencing in Rhynchophorus ferrugineus (Oliver) (Coleoptera: Curculionidae)
  47. Research Articles
  48. New pathway of icariin-induced MSC osteogenesis: transcriptional activation of TAZ/Runx2 by PI3K/Akt
  49. Research Articles
  50. Tudor-SN protein expression in colorectal cancer and its association with clinical characteristics
  51. Research Articles
  52. Proteomic and bioinformatics analysis of human saliva for the dental-risk assessment
  53. Research Articles
  54. Reverse transcriptase sequences from mulberry LTR retrotransposons: characterization analysis
  55. Research Articles
  56. Strain Stimulations with Different Intensities on Fibroblast Viability and Protein Expression
  57. Research Articles
  58. miR-539 mediates osteoblast mineralization by regulating Distal-less genes 2 in MC3T3-E1 cell line
  59. Research Articles
  60. Diversity of Intestinal Microbiota in Coilia ectenes from Lake Taihu, China
  61. Research Articles
  62. The production of arabitol by a novel plant yeast isolate Candida parapsilosis 27RL-4
  63. Research Articles
  64. Effectiveness of Azospirillum brasilense Sp245 on young plants of Vitis vinifera L.
  65. Research Articles
  66. Changes of photochemical efficiency and epidermal polyphenols content of Prosopis glandulosa and Prosopis juliflora leaves exposed to cadmium and copper
  67. Research Articles
  68. Ultraweak photon emission in strawberry fruit during ripening and aging is related to energy level
  69. Research Articles
  70. Molecular cloning, characterization and evolutionary analysis of leptin gene in Chinese giant salamander, Andrias davidianus
  71. Research Articles
  72. Longevity and stress resistance are affected by activation of TOR/Myc in progenitor cells of Drosophila gut
  73. Research Articles
  74. Curcumin attenuates oxidative stress in liver in Type 1 diabetic rats
  75. Research Articles
  76. Risk factors of long-term postoperative renal function after partial nephrectomy in a solitary kidney
  77. Research Articles
  78. Developmental anomalies of the right hepatic lobe: systematic comparative analysis of radiological features
  79. Review articles
  80. Genetic Defects Underlie the Non-syndromic Autosomal Recessive Intellectual Disability (NS-ARID)
  81. Review articles
  82. Research Progress on Tissue Culture and Genetic Transformation of Kenaf (Hibiscus cannabinus)
  83. Topical Issue On Precision Medicine
  84. MiR-107 inhibits proliferation of lung cancer cells through regulating TP53 regulated inhibitor of apoptosis 1 (TRIAP1)
  85. Topical Issue On Precision Medicine
  86. The functional role of exosome microRNAs in lung cancer
  87. Topical Issue On Precision Medicine
  88. The diagnostic value of serum microRNA-183 and TK1 as biomarkers for colorectal cancer diagnosis
  89. Topical Issue On Precision Medicine
  90. Screening feature modules and pathways in glioma using EgoNet
  91. Topical Issue On Precision Medicine
  92. Isoliquiritigenin inhibits colorectal cancer cells HCT-116 growth by suppressing the PI3K/AKT pathway
  93. Topical Issue On Precision Medicine
  94. Association between Caveolin-1 expression and pathophysiological progression of femoral nerves in diabetic foot amputation patients
  95. Topical Issue On Precision Medicine
  96. Biomarkers in patients with myocardial fibrosis
  97. Topical Issue On Precision Medicine
  98. Dysregulated pathways for off-pump coronary artery bypass grafting
  99. Topical Issue On Precision Medicine
  100. Individualized identification of disturbed pathways in sickle cell disease
  101. Topical Issue On Precision Medicine
  102. The prognostic value of serum PCT, hs-CRP, and IL-6 in patients with sepsis
  103. Topical Issue On Precision Medicine
  104. Sevoflurane-medicated the pathway of chemokine receptors bind chemokines in patients undergoing CABG
  105. Topical Issue On Precision Medicine
  106. The functional role of microRNAs in laryngeal carcinoma
  107. Topical Issue On Precision Medicine
  108. Revealing pathway cross-talk related to diabetes mellitus by Monte Carlo Cross-Validation analysis
  109. Topical Issue On Precision Medicine
  110. Correlation between CDKAL1 rs10946398C>A single nucleotide polymorphism and type 2 diabetes mellitus susceptibility: A meta-analysis
  111. Special Issue on Agricultural and Biological Sciences
  112. Effects of environmental variables on seedling distribution of rare and endangered Dacrydium pierrei
  113. Special Issue on Agricultural and Biological Sciences
  114. Study on synthesis and properties of nanoparticles loaded with amaryllidaceous alkaloids
  115. Special Issue on Agricultural and Biological Sciences
  116. Bacterial Infection Potato Tuber Soft Rot Disease Detection Based on Electronic Nose
  117. Special Issue on Agricultural and Biological Sciences
  118. Effects of subsoiling on maize yield and water-use efficiency in a semiarid area
https://doi.org/10.1515/biol-2017-0018
Schlagwörter für diesen Artikel
Synechocystis; photosystem II; psbA1; D1; photosynthesis; carbon dioxide; microaerobic; qRT-RT-PCR; chlorophyll; fluorescence
Creative Commons
BY-NC-ND 3.0

Artikel in diesem Heft

  1. Research Articles
  2. Field Performance and Genetic Fidelity of Micropropagated Plants of Coffea canephora (Pierre ex A. Froehner)
  3. Research Articles
  4. Foliage maturity of Quercus ilex affects the larval development of a Croatian coastal population of Lymantria dispar (Lepidoptera: Erebidae)
  5. Research Articles
  6. Structural and functional impact of SNPs in P-selectin gene: A comprehensive in silico analysis
  7. Research Articles
  8. High embryogenic ability and regeneration from floral axis of Amorphophallus konjac (Araceae)
  9. Research Articles
  10. Terpene content of wine from the aromatic grape variety ‘Irsai Oliver’ (Vitis vinifera L.) depends on maceration time
  11. Research Articles
  12. Light and smell stimulus protocol reduced negative frontal EEG asymmetry and improved mood
  13. Research Articles
  14. Swailing affects seed germination of plants of European bio-and agricenosis in a different way
  15. Research Articles
  16. Survey analysis of soil physicochemical factors that influence the distribution of Cordyceps in the Xiahe Region of Gansu Province
  17. Research Articles
  18. Production of biogas: relationship between methanogenic and sulfate-reducing microorganisms
  19. Research Articles
  20. Pentraxin 3 and atherosclerosis among type 2 diabetic patients
  21. Research Articles
  22. Evaluation of ribosomal P0 peptide as a vaccine candidate against Argulus siamensis in Labeo rohita
  23. Research Articles
  24. Variation of autosomes and X chromosome STR in breast cancer and gynecological cancer tissues
  25. Research Articles
  26. Response of antioxidant enzymes to cadmium-induced cytotoxicity in rat cerebellar granule neurons
  27. Research Articles
  28. Cardiac hypertrophy and IGF-1 response to testosterone propionate treatment in trained male rats
  29. Research Articles
  30. BRAF-activated non-protein coding RNA (BANCR) advances the development of esophageal squamous cell carcinoma via cell cycle
  31. Research Articles
  32. The influence of soil salinity on volatile organic compounds emission and photosynthetic parameters of Solanum lycopersicum L. varieties
  33. Research Articles
  34. Simple Protocol for immunoglobulin G Purification from Camel “Camelus dromedarius” Serum
  35. Research Articles
  36. Expression of psbA1 gene in Synechocystis sp. PCC 6803 is influenced by CO2
  37. Research Articles
  38. Frequency of Thrombophilic Gene Mutations in Patients with Deep Vein Thrombosis and in Women with Recurrent Pregnancy Loss
  39. Research Articles
  40. Evaluation of anticancer properties of a new α-methylene-δ-lactone DL-249 on two cancer cell lines
  41. Research Articles
  42. Impact of heated waters on water quality and macroinvertebrate community in the Narew River (Poland)
  43. Research Articles
  44. Effects of Some Additives on In Vitro True Digestibility of Wheat and Soybean Straw Pellets
  45. Research Articles
  46. RNAi-mediated gene silencing in Rhynchophorus ferrugineus (Oliver) (Coleoptera: Curculionidae)
  47. Research Articles
  48. New pathway of icariin-induced MSC osteogenesis: transcriptional activation of TAZ/Runx2 by PI3K/Akt
  49. Research Articles
  50. Tudor-SN protein expression in colorectal cancer and its association with clinical characteristics
  51. Research Articles
  52. Proteomic and bioinformatics analysis of human saliva for the dental-risk assessment
  53. Research Articles
  54. Reverse transcriptase sequences from mulberry LTR retrotransposons: characterization analysis
  55. Research Articles
  56. Strain Stimulations with Different Intensities on Fibroblast Viability and Protein Expression
  57. Research Articles
  58. miR-539 mediates osteoblast mineralization by regulating Distal-less genes 2 in MC3T3-E1 cell line
  59. Research Articles
  60. Diversity of Intestinal Microbiota in Coilia ectenes from Lake Taihu, China
  61. Research Articles
  62. The production of arabitol by a novel plant yeast isolate Candida parapsilosis 27RL-4
  63. Research Articles
  64. Effectiveness of Azospirillum brasilense Sp245 on young plants of Vitis vinifera L.
  65. Research Articles
  66. Changes of photochemical efficiency and epidermal polyphenols content of Prosopis glandulosa and Prosopis juliflora leaves exposed to cadmium and copper
  67. Research Articles
  68. Ultraweak photon emission in strawberry fruit during ripening and aging is related to energy level
  69. Research Articles
  70. Molecular cloning, characterization and evolutionary analysis of leptin gene in Chinese giant salamander, Andrias davidianus
  71. Research Articles
  72. Longevity and stress resistance are affected by activation of TOR/Myc in progenitor cells of Drosophila gut
  73. Research Articles
  74. Curcumin attenuates oxidative stress in liver in Type 1 diabetic rats
  75. Research Articles
  76. Risk factors of long-term postoperative renal function after partial nephrectomy in a solitary kidney
  77. Research Articles
  78. Developmental anomalies of the right hepatic lobe: systematic comparative analysis of radiological features
  79. Review articles
  80. Genetic Defects Underlie the Non-syndromic Autosomal Recessive Intellectual Disability (NS-ARID)
  81. Review articles
  82. Research Progress on Tissue Culture and Genetic Transformation of Kenaf (Hibiscus cannabinus)
  83. Topical Issue On Precision Medicine
  84. MiR-107 inhibits proliferation of lung cancer cells through regulating TP53 regulated inhibitor of apoptosis 1 (TRIAP1)
  85. Topical Issue On Precision Medicine
  86. The functional role of exosome microRNAs in lung cancer
  87. Topical Issue On Precision Medicine
  88. The diagnostic value of serum microRNA-183 and TK1 as biomarkers for colorectal cancer diagnosis
  89. Topical Issue On Precision Medicine
  90. Screening feature modules and pathways in glioma using EgoNet
  91. Topical Issue On Precision Medicine
  92. Isoliquiritigenin inhibits colorectal cancer cells HCT-116 growth by suppressing the PI3K/AKT pathway
  93. Topical Issue On Precision Medicine
  94. Association between Caveolin-1 expression and pathophysiological progression of femoral nerves in diabetic foot amputation patients
  95. Topical Issue On Precision Medicine
  96. Biomarkers in patients with myocardial fibrosis
  97. Topical Issue On Precision Medicine
  98. Dysregulated pathways for off-pump coronary artery bypass grafting
  99. Topical Issue On Precision Medicine
  100. Individualized identification of disturbed pathways in sickle cell disease
  101. Topical Issue On Precision Medicine
  102. The prognostic value of serum PCT, hs-CRP, and IL-6 in patients with sepsis
  103. Topical Issue On Precision Medicine
  104. Sevoflurane-medicated the pathway of chemokine receptors bind chemokines in patients undergoing CABG
  105. Topical Issue On Precision Medicine
  106. The functional role of microRNAs in laryngeal carcinoma
  107. Topical Issue On Precision Medicine
  108. Revealing pathway cross-talk related to diabetes mellitus by Monte Carlo Cross-Validation analysis
  109. Topical Issue On Precision Medicine
  110. Correlation between CDKAL1 rs10946398C>A single nucleotide polymorphism and type 2 diabetes mellitus susceptibility: A meta-analysis
  111. Special Issue on Agricultural and Biological Sciences
  112. Effects of environmental variables on seedling distribution of rare and endangered Dacrydium pierrei
  113. Special Issue on Agricultural and Biological Sciences
  114. Study on synthesis and properties of nanoparticles loaded with amaryllidaceous alkaloids
  115. Special Issue on Agricultural and Biological Sciences
  116. Bacterial Infection Potato Tuber Soft Rot Disease Detection Based on Electronic Nose
  117. Special Issue on Agricultural and Biological Sciences
  118. Effects of subsoiling on maize yield and water-use efficiency in a semiarid area
Jetzt anmelden und 20% sparen
Institutioneller Zugang
Wie funktioniert Authentifizierung?
Haben Sie eine Idee, wie wir unsere Website verbessern können?
Bitte schreiben Sie uns.
© 2025 De Gruyter Brill
Heruntergeladen am 17.9.2025 von https://www.degruyterbrill.com/document/doi/10.1515/biol-2017-0018/html
Button zum nach oben scrollen