Skip to main content
SpringerLink
Log in

Stress-induced changes in the ultrastructure of the photosynthetic apparatus of green microalgae

  • Original Article
  • Published:
Protoplasma Aims and scope Submit manuscript

Abstract

In photosynthetic organisms including unicellular algae, acclimation to and damage by environmental stresses are readily apparent at the level of the photosynthetic apparatus. Phenotypic manifestations of the stress responses include rapid and dramatic reduction of photosynthetic activity and pigment content aimed at mitigating the risk of photooxidative damage. Although the physiological and molecular mechanisms of these events are well known, the ultrastructural picture of the stress responses is often elusive and frequently controversial. We analyzed an extensive set of transmission electron microscopy images of the microalgal cells obtained across species of Chlorophyta and in a wide range of growth conditions. The results of the analysis allowed us to pinpoint distinct ultrastructural changes typical of normal functioning and emergency reduction of the chloroplast membrane system under high light exposure and/or mineral nutrient starvation. We demonstrate the patterns of the stress-related ultrastructural changes including peculiar thylakoid rearrangements and autophagy-like processes and provide an outlook on their significance for implementation of the stress responses.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Abbreviations

AMPT:

Appressed membrane pair thickness

DGDG:

Digalactosyldiacylglycerol

EMS:

Epichloroplastic membrane structures

FAME:

Fatty acid methyl esters

FID:

Flame ionization detector

HLS:

Hub-like structures

MGDG:

Monogalactosyldiacylglycerol

NPQ:

Non-photochemical quenching

OB:

Oil bodies

PLB:

Prolamellar bodies

PSA:

Photosynthetic apparatus

RCB:

Rubisco-containing bodies

S C :

Chloroplast area

S P :

Protoplast area

STM:

Stroma with thylakoid membranes of the chloroplast

S STM :

Area of the STM

TEM:

Transmission electron microscopy

TLC:

Thin-layer chromatography

References

  • Avila-Ospina L, Moison M, Yoshimoto K, Masclaux-Daubresse C (2014) Autophagy, plant senescence, and nutrient recycling. J Exp Bot 65:3799–3811. https://doi.org/10.1093/jxb/eru039

    Article  PubMed  Google Scholar 

  • Baulina OI (2012) Ultrastructural plasticity of cyanobacteria. Springer-Verlag, Berlin

    Book  Google Scholar 

  • Baulina O, Gorelova O, Solovchenko A, Chivkunova O, Semenova L, Selyakh I, Scherbakov P, Burakova O, Lobakova E (2016) Diversity of the nitrogen starvation responses in subarctic Desmodesmus sp. (Chlorophyceae) strains isolated from symbioses with invertebrates. FEMS Microbiol Ecol 92:fiw031. https://doi.org/10.1093/femsec/fiw031

    Article  CAS  PubMed  Google Scholar 

  • Berner T, Sukenik A (1998) Photoacclimation in photosynthetic microorganisms: an ultrastructural response. Israel J Plant Sci 46:141–146. https://doi.org/10.1080/07929978.1998.10676721

    Article  Google Scholar 

  • Berner T, Dubinsky Z, Wyman K, Falkowski P (1989) Photoadaptation and the “package” effect in Dunaliella tertiolecta (Chlorophyceae). J Phycol 25:70–78

    Article  CAS  Google Scholar 

  • Bryan G, Zdylak AH, Ehret C (1967) Photoinduction of plastids and of chlorophyll in a Chlorella mutant. J Cell Sci 2:513–528

    CAS  PubMed  Google Scholar 

  • Burgess J (1985) Introduction to plant cell development. CUP Archive, Cambridge

    Google Scholar 

  • Chekanov K, Lobakova E, Selyakh I, Semenova L, Sidorov R, Solovchenko A (2014) Accumulation of astaxanthin by a new Haematococcus pluvialis strain BM1 from the White Sea coastal rocks (Russia). Mar Drugs 12:4504–4520

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chiba A, Ishida H, Nishizawa NK, Makino A, Mae T (2003) Exclusion of ribulose-1, 5-bisphosphate carboxylase/oxygenase from chloroplasts by specific bodies in naturally senescing leaves of wheat. Plant Cell Physiol 44:914–921

    Article  CAS  PubMed  Google Scholar 

  • Davey MP, Horst I, Duong G-H, Tomsett EV, Litvinenko AC, Howe CJ, Smith AG (2014) Triacylglyceride production and autophagous responses in Chlamydomonas reinhardtii depend on resource allocation and carbon source. Eukaryot Cell 13:392–400

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Davidi L, Shimoni E, Khozin-Goldberg I, Zamir A, Pick U (2014) Origin of β-carotene-rich plastoglobuli in Dunaliella bardawil. Plant Physiol 164:2139–2156. https://doi.org/10.1104/pp.113.235119

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Deme B, Cataye C, Block MA, Marechal E, Jouhet J (2014) Contribution of galactoglycerolipids to the 3-dimensional architecture of thylakoids. FASEB J 28:3373–3383. https://doi.org/10.1096/fj.13-247395

    Article  CAS  PubMed  Google Scholar 

  • Du Z-Y, Benning C (2016) Triacylglycerol accumulation in photosynthetic cells in plants and algae. In: Nakamura Y, Li-Beisson Y (eds) Lipids in Plant and Algae Development. Subcellular Biochemistry, vol 86.Springer, Cham, pp 179–205

  • Du ZY, Lucker BF, Zienkiewicz K, Miller TE, Zienkiewicz A, Sears BB, Kramer DM, Benning C (2018) Galactoglycerolipid lipase PGD1 is involved in thylakoid membrane remodeling in response to adverse environmental conditions in Chlamydomonas. Plant Cell 30:447–465

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fisher T, Berner T, Iluz D, Dubinsky Z (1998) The kinetics of the photoacclimation response of Nannochloropsis sp.(Eustigmatophyceae): a study of changes in ultrastructure and PSU density. J Phycol 34:818–824

    Article  Google Scholar 

  • Friedberg I, Goldberg I, Ohad I (1971) A prolamellar body-like structure in Chlamydomonas reinhardi. J Cell Biol 50:268–275

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Garab G, Ughy B, Goss R (2016) Role of MGDG and non-bilayer lipid phases in the structure and dynamics of chloroplast thylakoid membranes. In: Nakamura Y, Li-Beisson Y (eds) Lipids in plant and algaedevelopment. Subcellular Biochemistry, vol 86. Springer, Cham, pp 127–157

  • Gorelova O, Baulina O, Solovchenko A, Fedorenko T, Kravtsova T, Chivkunova O, Koksharova O, Lobakova E (2012) Green microalgae from associations with White Sea invertebrates. Microbiology 81:505–507. https://doi.org/10.1134/S002626171204008X

    Article  CAS  Google Scholar 

  • Gorelova O, Baulina O, Solovchenko A, Chekanov K, Chivkunova O, Fedorenko T, Lobakova E (2015a) Similarity and diversity of the Desmodesmus spp. microalgae isolated from associations with White Sea invertebrates. Protoplasma 252:489–503. https://doi.org/10.1007/s00709-014-0694-0

    Article  CAS  PubMed  Google Scholar 

  • Gorelova O, Baulina O, Solovchenko A, Selyakh I, Chivkunova O, Semenova L, Scherbakov P, Burakova O, Lobakova E (2015b) Coordinated rearrangements of assimilatory and storage cell compartments in a nitrogen-starving symbiotic chlorophyte cultivated under high light. Arch Microbiol 197:181–195. https://doi.org/10.1007/s00203-014-1036-5

    Article  CAS  PubMed  Google Scholar 

  • Guiamét JJ, Pichersky E, Nooden LD (1999) Mass exodus from senescing soybean chioroplasts. Plant Cell Physiol 40:986–992

    Article  Google Scholar 

  • Hinder B, Schellenberg M, Rodoni S, Ginsburg S, Vogt E, Martinoia E, Matile P, Hörtensteiner S (1996) How plants dispose of chlorophyll catabolites. Directly energized uptake of tetrapyrrolic breakdown products into isolated vacuoles. J Biol Chem 271:27233–27236

    Article  CAS  PubMed  Google Scholar 

  • Hoober JK, White RA, Marks DB, Gabriel JL (1994) Biogenesis of thylakoid membranes with emphasis on the process in Chlamydomonas. Photosynth Res 39:15–31

    Article  CAS  PubMed  Google Scholar 

  • Hörtensteiner S (2006) Chlorophyll degradation during senescence. Annu Rev Plant Biol 57:55–77

    Article  CAS  PubMed  Google Scholar 

  • Horton P (2014) Developments in research on non-photochemical fluorescence quenching: emergence of key ideas, theories and experimental approaches. In: Demmig-Adams B, Garab G, Adams W III, Govindjee (eds) Non-photochemical quenching and energy dissipation in plants, algae and cyanobacteria. Springer, Netherlands, pp 73–95

    Chapter  Google Scholar 

  • Inoue K (2011) Emerging roles of the chloroplast outer envelope membrane. Trends Plant Sci 16:550–557

    Article  CAS  PubMed  Google Scholar 

  • Ishida H, Izumi M, Wada S, Makino A (2014) Roles of autophagy in chloroplast recycling. Biochim Biophys Acta 1837:512–521. https://doi.org/10.1016/j.bbabio.2013.11.009

    Article  CAS  PubMed  Google Scholar 

  • Ismagulova T, Chekanov K, Gorelova O, Baulina O, Semenova L, Selyakh I, Chivkunova O, Lobakova E, Karpova O, Solovchenko A (2017) A new subarctic strain of Tetradesmus obliquus—part I: identification and fatty acid profiling. J Appl Phycol. https://doi.org/10.1007/s10811-017-1313-1

  • Izumi M, Nakamura S (2017) Partial or entire: distinct responses of two types of chloroplast autophagy. Plant Signal Behav 12:e1393137. https://doi.org/10.1080/15592324.2017.1393137

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Izumi M, Nakamura S (2018) Chloroplast protein turnover: the influence of extraplastidic processes, including autophagy international. Int J Mol Sci 19:828. https://doi.org/10.3390/ijms19030828

    Article  CAS  PubMed Central  Google Scholar 

  • Johnson MP, Brain AP, Ruban AV (2011a) Changes in thylakoid membrane thickness associated with the reorganization of photosystem II light harvesting complexes during photoprotective energy dissipation. Plant Signal Behav 6:1386–1390

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Johnson MP, Goral TK, Duffy CD, Brain AP, Mullineaux CW, Ruban AV (2011b) Photoprotective energy dissipation involves the reorganization of photosystem II light-harvesting complexes in the grana membranes of spinach chloroplasts. The Plant Cell Online 23:1468–1479

    Article  CAS  Google Scholar 

  • Jouhet J, Maréchal E, Block MA (2007) Glycerolipid transfer for the building of membranes in plant cells. Prog Lipid Res 46:37–55

    Article  CAS  PubMed  Google Scholar 

  • Joyard J, Maréchal E, Miège C, Block MA, Dorne AJ, Douce R (2004) Structure, distribution and biosynthesis of glycerolipids from higher plant chloroplasts. In: Siegenthaler PA, Murata N (eds) Lipids in photosynthesis: structure, function and genetics. Springer, Netherlands, pp 21–52

    Chapter  Google Scholar 

  • Joyard J, Ferro M, Masselon C, Seigneurin-Berny D, Salvi D, Garin J, Rolland N (2010) Chloroplast proteomics highlights the subcellular compartmentation of lipid metabolism. Prog Lipid Res 49:128–158. https://doi.org/10.1016/j.plipres.2009.10.003

    Article  CAS  PubMed  Google Scholar 

  • Khozin‐Goldberg I, Didi‐Cohen S, Shayakhmetova I, Cohen Z (2002) Biosynthesis of eicosapentaenoic acid (EPA) in the freshwater eustigmatophyte Monodus subterraneus (Eustigmatophyceae). J Phycol 38:745–756

  • Kimball SL, Salisbury FB (1973) Ultrastructural changes of plants exposed to low temperatures. Am J Bot 60:1028–1033

    Article  Google Scholar 

  • Kirchhoff H (2018) Structure-function relationships in photosynthetic membranes: challenges and emerging fields. Plant Sci 266:76–82. https://doi.org/10.1016/j.plantsci.2017.09.021

    Article  CAS  PubMed  Google Scholar 

  • Klein S, Schiff JA, Holowinsky AW (1972) Events surrounding the early development of Euglena chloroplasts: II. Normal development of fine structure and the consequences of preillumination. Dev Biol 28:253–273

    Article  CAS  PubMed  Google Scholar 

  • Kratsch H, Wise RR (2000) The ultrastructure of chilling stress. Plant Cell Environ 23:337–350

    Article  CAS  Google Scholar 

  • Li F, Vierstra RD (2012) Autophagy: a multifaceted intracellular system for bulk and selective recycling. Trends Plant Sci 17:526–537

    Article  CAS  PubMed  Google Scholar 

  • Lichtenthaler HK, Prenzel U, Douce R, Joyard J (1981) Localization of prenylquinones in the envelope of spinach chloroplasts. Biochim Biophys Acta 641:99–105. https://doi.org/10.1016/0005-2736(81)90572-1

    Article  CAS  PubMed  Google Scholar 

  • Maeda M, Thompson GA (1986) On the mechanism of rapid plasma membrane and chloroplast envelope expansion in Dunaliella salina exposed to hypoosmotic shock. J Cell Biol 102:289–297

    Article  CAS  PubMed  Google Scholar 

  • Majeran W, Olive J, Drapier D, Vallon O, Wollman F-A (2001) The light sensitivity of ATP synthase mutants of Chlamydomonas reinhardtii. Plant Physiol 126:421–433

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marty F (1999) Plant vacuoles. Plant Cell 11:587–599

  • Matile P, Hörtensteiner S, Thomas H (1999) Chlorophyll degradation. Annu Rev Plant Biol 50:67–95

    Article  CAS  Google Scholar 

  • Moellering ER, Muthan B, Benning C (2010) Freezing tolerance in plants requires lipid remodeling at the outer chloroplast membrane. Science 330:226–228

    Article  CAS  PubMed  Google Scholar 

  • Mueller D, Vincent W, Bonilla S, Laurion I (2005) Extremotrophs, extremophiles and broadband pigmentation strategies in a high arctic ice shelf ecosystem. FEMS Microbiol Ecol 53:73–87

    Article  CAS  PubMed  Google Scholar 

  • Neuhaus H, Wagner R (2000) Solute pores, ion channels, and metabolite transporters in the outer and inner envelope membranes of higher plant plastids. BBA-Biomembranes 1465:307–323

    Article  CAS  PubMed  Google Scholar 

  • Nordhues A, Schöttler MA, Unger AK, Geimer S, Schönfelder S, Schmollinger S, Rütgers M, Finazzi G, Soppa B, Sommer F, Mühlhaus T (2012) Evidence for a role of VIPP1 in the structural organization of the photosynthetic apparatus in Chlamydomonas. Plant Cell 24:637–659. https://doi.org/10.1105/tpc.111.092692

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pal D, Khozin-Goldberg I, Cohen Z, Boussiba S (2011) The effect of light, salinity, and nitrogen availability on lipid production by Nannochloropsis sp. Appl Microbiol Biotechnol 90:1429–1441. https://doi.org/10.1007/s00253-011-3170-1

    Article  CAS  PubMed  Google Scholar 

  • Park H, Kreunen SS, Cuttriss AJ, DellaPenna D, Pogson BJ (2002) Identification of the carotenoid isomerase provides insight into carotenoid biosynthesis, prolamellar body formation, and photomorphogenesis. Plant Cell 14:321–332

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pribil M, Labs M, Leister D (2014) Structure and dynamics of thylakoids in land plants. J Exp Bot 65:1955–1972. https://doi.org/10.1093/jxb/eru090

    Article  CAS  PubMed  Google Scholar 

  • Reynolds E (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17:208–212

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rippka R, Deruelles J, Waterbury JB, Herdman M, Stanier RY (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J Gen Microbiol 111:1–61

    Google Scholar 

  • Ruban AV (2016) Non-photochemical chlorophyll fluorescence quenching: mechanism and effectiveness in protection against photodamage. Plant Physiol 170:1903–1916

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Scherbakov P, Ismagulova T, Chernov T, Gorelova O, Selyakh I, Semenova L, Baulina O, Chivkunova O, Lobakova E, Solovchenko A (2017) A new subarctic strain of Tetradesmus obliquus. Part II: comparative studies of CO2-stress tolerance. J Appl Phycol. https://doi.org/10.1007/s10811-017-1334-9

  • Selstam E, Schelin J, Williams WP, Brain AP (2007) Structural organisation of prolamellar bodies (PLB) isolated from Zea mays. Parallel TEM, SAXS and absorption spectra measurements on samples subjected to freeze–thaw, reduced pH and high-salt perturbation. Biochim Biophys Acta Biomembr 1768:2235–2245

    Article  CAS  Google Scholar 

  • Shebanova A, Ismagulova T, Solovchenko A, Baulina O, Lobakova E, Ivanova A, Moiseenko A, Shaitan K, Polshakov V, Nedbal L, Gorelova O (2017) Versatility of the green microalga cell vacuole function as revealed by analytical transmission electron microscopy. Protoplasma 254:1323–1340

    Article  CAS  PubMed  Google Scholar 

  • Simionato D, Block MA, La Rocca N, Jouhet J, Maréchal E, Finazzi G, Morosinotto T (2013) Response of nannochloropsis gaditana to nitrogen starvation includes a de novo biosynthesis of triacylglycerols, a decrease of chloroplast galactolipids and a reorganization of the photosynthetic apparatus. Eukaryot Cell 12:392–400

    Article  CAS  Google Scholar 

  • Solovchenko A, Neverov K (2017) Carotenogenic response in photosynthetic organisms: a colorful story. Photosynth Res 133:31–47

    Article  CAS  PubMed  Google Scholar 

  • Solovchenko A, Merzlyak M, Khozin-Goldberg I, Cohen Z, Boussiba S (2010) Coordinated carotenoid and lipid syntheses induced in Parietochloris incisa (Chlorophyta, Trebouxiophyceae) mutant deficient in Δ5 desaturase by nitrogen starvation and high light. J Phycol 46:763–772. https://doi.org/10.1111/j.1529-8817.2010.00849.x

    Article  CAS  Google Scholar 

  • Solovchenko A, Chivkunova O, Maslova I (2011) Pigment composition, optical properties, and resistance to photodamage of the microalga Haematococcus pluvialis cultivated under high light. Russ J Plant Physiol 58:9–17. https://doi.org/10.1134/S1021443710061056

    Article  CAS  Google Scholar 

  • Solovchenko A, Chivkunova O, Semenova L, Selyakh I, Shcherbakov P, Karpova E, Lobakova E (2013) Stress-induced changes in pigment and fatty acid content in the microalga Desmodesmus sp. isolated from a White Sea hydroid. Russ J Plant Physiol 60:313–321. https://doi.org/10.1007/s00253-012-4677-9

    Article  CAS  Google Scholar 

  • Solovchenko A, Gorelova O, Selyakh I, Semenova L, Chivkunova O, Baulina O, Lobakova E (2014) Desmodesmus sp. 3Dp86E-1-a novel symbiotic chlorophyte capable of growth on pure CO2. Mar Biotechnol 16:495–501. https://doi.org/10.1007/s10126-014-9572-1

    Article  CAS  Google Scholar 

  • Solovchenko A, Gorelova O, Baulina O, Selyakh I, Semenova L, Chivkunova O, Scherbakov P, Lobakova E (2015a) Physiological plasticity of symbiotic Desmodesmus (Chlorophyceae) isolated from taxonomically distant White Sea invertebrates. Russ J Plant Physiol 62:653–663. https://doi.org/10.1134/S1021443715050167

    Article  CAS  Google Scholar 

  • Solovchenko A, Gorelova O, Selyakh I, Pogosyan S, Baulina O, Semenova L, Chivkunova O, Voronova E, Konyukhov I, Scherbakov P, Lobakova E (2015b) A novel CO2-tolerant symbiotic Desmodesmus (Chlorophyceae, Desmodesmaceae): acclimation to and performance at a high carbon dioxide level. Algal Res 11:399–410

    Article  Google Scholar 

  • Solovchenko A, Gorelova O, Selyakh I, Baulina O, Semenova L, Logacheva M, Chivkunova O, Scherbakov P, Lobakova E (2016) Nitrogen availability modulates CO2 tolerance in a symbiotic chlorophyte. Algal Res 16:177–188. https://doi.org/10.1016/j.algal.2016.03.002

    Article  Google Scholar 

  • Takamiya KI, Tsuchiya T, Ohta H (2000) Degradation pathway(s) of chlorophyll: what has gene cloning revealed? Trends Plant Sci 5:426–431

    Article  CAS  PubMed  Google Scholar 

  • Topf J, Gong H, Timberg R, Mets L, Ohad I (1992) Thylakoid membrane energization and swelling in photoinhibited Chlamydomonas cells is prevented in mutants unable to perform cyclic electron flow. Photosynth Res 32:59–69

    Article  CAS  PubMed  Google Scholar 

  • Treves H, Raanan H, Kedem I, Murik O, Keren N, Zer H, Berkowicz SM, Giordano M, Norici A, Shotland Y, Ohad I (2016) The mechanisms whereby the green alga Chlorella ohadii, isolated from desert soil crust, exhibits unparalleled photodamage resistance. New Phytol 210:1229–1243

    Article  CAS  PubMed  Google Scholar 

  • Varshney P, Mikulic P, Vonshak A, Beardall J, Wangikar PP (2014) Extremophilic micro-algae and their potential contribution in biotechnology. Bioresour Technol 184:363–372

    Article  CAS  PubMed  Google Scholar 

  • Velikanov G, Ponomareva A, Belova L, Ilyina T (2011) Stromule-like protrusions of plastid membrane envelope in root cells. Cell Tissue Biol 5:305–310

    Article  Google Scholar 

  • Wang ZT, Ullrich N, Joo S, Waffenschmidt S, Goodenough U (2009) Algal lipid bodies: stress induction, purification, and biochemical characterization in wild-type and starchless Chlamydomonas reinhardtii. Eukaryot Cell 8:1856–1868. https://doi.org/10.1128/ec.00272-09

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xie Q, Michaeli S, Peled-Zehavi H, Galili G (2015) Chloroplast degradation: one organelle, multiple degradation pathways. Trends Plant Sci 20:264–265

    Article  CAS  PubMed  Google Scholar 

  • Yoshimoto K (2012) Beginning to understand autophagy, an intracellular self-degradation system in plants. Plant Cell Physiol 53:1355–1365. https://doi.org/10.1093/pcp/pcs099

    Article  CAS  PubMed  Google Scholar 

  • Zorin B, Pal-Nath D, Lukyanov A, Smolskaya S, Kolusheva S, Didi-Cohen S, Boussiba S, Cohen Z, Khozin-Goldberg I, Solovchenko A (2017) Arachidonic acid is important for efficient use of light by the microalga Lobosphaera incisa under chilling stress. Biochim Biophys Acta 1862:853–868

    Article  CAS  Google Scholar 

Download references

Acknowledgements

High-pressure freezing and freeze-substitution of microalgal samples was performed in the research resource center “Molecular and cell technologies” of St. Petersburg State University.

Funding

The electron microscopy studies were carried out at the User Facilities Center of M.V. Lomonosov Moscow State University and jointly funded by the Russian Foundation for Basic Research and the Ministry of Science, Technology and Space, Israel (grant 15-54-06004). Cultivation of microalgae was supported by the Ministry of Science and Education of the Russian Federation (the Agreement number 02.a03.21.0008 of 24 June 2016).

Author information

Authors and Affiliations

  1. Department of Bioengineering, Faculty of Biology, Moscow State University, GSP-1, Moscow, 119234, Russia

    Olga Gorelova, Olga Baulina, Tatiana Ismagulova, Elena Lobakova, Irina Selyakh, Larisa Semenova, Olga Chivkunova, Olga Karpova, Pavel Scherbakov & Alexei Solovchenko

  2. Microalgal Biotechnology Laboratory, The French Associates Institute for Agriculture and Biotechnology for Drylands, The J. Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Sede-Boqer Campus, 8499000, Midreshet Ben Gurion, Israel

    Kamilya Kokabi & Inna Khozin-Goldberg

  3. Peoples Friendship University of Russia (RUDN University), Moscow, 117198, Russia

    Alexei Solovchenko

Authors
  1. Olga Gorelova
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Olga Baulina
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tatiana Ismagulova
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kamilya Kokabi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Elena Lobakova
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Irina Selyakh
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Larisa Semenova
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Olga Chivkunova
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Olga Karpova
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Pavel Scherbakov
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Inna Khozin-Goldberg
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Alexei Solovchenko
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Alexei Solovchenko.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Handling Editor: Andreas Holzinger

Electronic supplementary material

Online Resource 1

(DOCX 728 kb)

Online Resource 2

(DOCX 16 kb)

Online Resource 3

(DOCX 13 kb)

Online Resource 4

(DOCX 14 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gorelova, O., Baulina, O., Ismagulova, T. et al. Stress-induced changes in the ultrastructure of the photosynthetic apparatus of green microalgae. Protoplasma 256, 261–277 (2019). https://doi.org/10.1007/s00709-018-1294-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00709-018-1294-1

Keywords

Search

Navigation