GET THE APP
Journal of Plant Biochemistry & Physiology

Journal of Plant Biochemistry & Physiology
Open Access

ISSN: 2329-9029

+44 1478 350008

Mini Review Article - (2022)Volume 10, Issue 11

View PDF Download PDF

Stadnichuk IN*
 
*Correspondence: Stadnichuk IN, Timiryazev Institute of Plant Physiology, Russian Academy of Sciences, Russia, Email:

Author info »

Abstract

Phycobiliproteins are photosynthetic antenna pigments of cyanobacteria and red algae, where they are assembled in macromolecular supercomplexes of phycobilisomes (PBS)s, as well as of cryptophyte algae, where they exist in the form of dimers. The absorbed light energy transfer from phycobiliprotein antenna to the photosystem II (PS II) is well known since the first studies in this field and is highly effective reaching 95-100%. However, interaction of phycobiliproteins with the photosystem I (PS I) is subject for discussion. Here, various data on energetic coupling of PBSs and phycobiliproteins with the PS II and PS I in photosynthetic organisms are discussed.
 

Keywords

Cryptophyte algae; Cyanobacteria; Energy transfer; Photosystem I; Photosystem II; Phycobilisome;
Phycobiliproteins; Red algae

Introduction

All oxygenic photosynthetics have three types of pigment-protein complexes in their photosynthetic apparatus. First and foremost come complexes of photosystem I (PS I) and photosystem II (PS II) with reaction centers; second, there are various kinds of antennae fulfilling the role of light energy absorption and its subsequent transfer to photoactive complexes. Three groups of photosynthetics, cyanobacteria, red and cryptophyte algae possess the water-soluble phycobiliprotein antennae. In cyanobacteria and red algae, phycobiliproteins are organized in giant macrocomplexes of phycobilisomes (PBS)s , while in chloroplasts of cryptophyte algae the bphycobiliproteins are present in the form of relatively small protein dimers. To ensure the effective energy transfer, phycoiliproteins are attached to the thylakoid membrane in regions of intra-membrane PS I and PS II arrangement. PBSs are localized on the cytoplasmic side of the membrane; phycobiliprotein dimers of cryptophytes are revealed to be inside the chloroplast lumen.

Energy Transfer from Pbs To Ps Ii

PBS is unconditionally considered to be an external antenna of PSII, which was demonstrated several times by different spectral methods in cyanobacteria and red algae. The energy transfer was demonstrated in vivo by: i) the action spectra of photoreaction II revealing PBS activity, ii) the low temperature fluorescence emission spectra containing PS II-chlorophyll bands under excitation in the PBS absorption region, iii) the fluorescence excitation spectra of PSII antennal chlorophyll dominated by PBS-belonging bands. It was also revealed for various species of cyanobacteria by the time-resolved fluorescence spectroscopy [1-4].

The hemidiscoidal cyanobacterial PBS and PS II interact within the flat cytoplasmic surface of PS II dimer and the bottom surface of the PBS core [1,5,6]. Only the dimeric form of PS II being equal to PBS surface guaranties a stable binding, whereas monomeric PS II is not able to bind PBS properly [1,7]. A supercomplex of the PBS core and PS II can be isolated by mild detergent treatment [8], although its fine structure has not been determined experimentally, as well as the molecular structure of the PBS core remains not fully elucidated [5,8]. Some structural details of PBS-PS II megacomplex were revealed by cryo-EM and cross-linking/mass-spectrometry techniques [3,6,7]. Two longwavelength chromophorylated ApcD and ApcE polypeptides present in bottom allophycocyanin cylinders of the PBS core are known as the terminal emitters functioning as the final steps of energy transfer from PBS to PS II [3,4]. Besides that, ApcE, also known as LCM or anchor protein, forms a special docking site in PBS attachment to the PS II dimer [9]. At present, determining the docking sites between PBS and PSII and the energy transfer calculations are limited to spatial modeling based on the existing crystallographic data of PS II dimers and highresolution EM data of hemidiscoidal PBS structure [6,10,11].

Energy Transfer from Pbs To Ps I

Earlier assumptions of the PBS role as an external antenna of PS II were based on the putative compensation that antennal pigments provide for both relatively high PS I/PS II ratio in the cyanobacterial and red algal cells and on the shortage in chlorophyll content of PSII [12]. Later, this opinion changed when it became to reveal photooxydation P700 being the exceptional for PS I in the light absorbed by PBSs [13,14]. These results were supplemented as well by measuring the action spectra of PS I-dependent reversible photoinhibition of respiration in cells of cyanobateria irrefutably proving the energy transfer PBS → PS I [2]. All other spectral methods used in studies of PBS-PS II interaction turned out to be useful in case of PS I and had also shown, that PBSs transfer the absorbed energy to PS I. 77 K emission spectra of chlorophyll measured under the excitation of PBSs, in addition to fluorescence peaks of PS II, usually reveal a distinct peak at 715-730 nm belonging to PS I, while the long-wavelength PS I fluorescence excitation spectra exhibit maxima attributed to phycobiliproteins. Timeresolved 77 K fluorescence emission spectra of cyanobacteria measured under excitation of PBSs show an increase of PS I and PS II chlorophyll emissions developed in parallel [2,15]. Efficient energy transfer from PBSs to chlorophyll has been found in cyanobacterial heterocysts that lack PS II and possess PS I [16]. In the obtained PS II-less mutants of cyanobacteria PBSs stay bound in the intact form to the photosynthetic membrane [17]. Besides, the purified PBS samples incorporate significant amounts of ferredoxin: NADP+ reductase, an extrinsic membrane protein functionally connected to PS I [18].

In summary, the contribution of PBSs feeding energy to PS I is considered to be proved giving rise to three models of energy transfer from PBS to PS I, reviewed in [14]: i) “spillover” model; ii) ternary PBS-PSII-PS I complex formation; iii) direct energy migration from the PBS to PS I without PS II being involved. It should be specified that, in red algae thylakoids, the PS I exists in a monomeric form [19] and, in cyanobacteria, PS I mainly forms trimers with a certain share of monomers [20]. Computer modeling demonstrated the docking of PBS to PS I monomer only, corresponding to a realization of energy transfer between these two pigment-protein complexes [10]. In contrast to the PSII dimers [1], the surface of the PSI shows a major protrusion of three hydrophilic polypeptide subunits (PsaC, PsaD, and PsaE), which extends into the cytoplasm [21] and prevents a tight binding of PBS to PS I trimer due to its threefold symmetry [10].

ApcD is necessary for efficient energy transfer from PBSs to PS I [22]. PS I is highly sensitive to any shortcomings in PBS functioning. When, for some reason, altered conventional PBSs in the mutant cyanobacterial cells cannot properly attach to the thylakoid membrane the energy feeding of PS I is realized by small cylindrical PBS anchored to PS I by the synthesized special linker CpcG2 polypeptide [23-27].

Energy Transfer from Phycobiliproteins to Ps Ii In Cryptophytes Algae

Unlike cyanobacteria or red algae, the phycobiliproteins of cryptophytes do not assemble in PBS megacomplexes with the mass of several million Daltons but form (α1βα2β)- polypeptide heterodimers with the relatively small mass of ~60 kDa [11]. Each species possess one of seven unique for cryptophyte algae phycobiliproteins that complement in antenna function the Chl a/c-protein also present in chloroplasts, like in all other representatives of Chromophyta [3]. In contrast to PBSs, the heterodimers are not localized on the stromal surface of the thylakoid membrane but occupy the entire space of the lumen and are most likely assembled into cylindrical structures oriented perpendicular to the thylakoid membrane [16,17]. Isolation of the thylakoid membrane fragments followed by cryo- EM microscopy demonstrated that antennal chlorophyll a/cproteins are connected in thylakoids with the PSI monomers and PS II dimers [28]. Unfortunately, simultaneous isolation of water-soluble phycobiliproteins and membrane proteins (the PS II, PS I, or Chl a/c-protein) is challenging [29]. Thus, further studies are required to find an answer to this conundrum.

Migration of energy from phycobiliproteins to total chlorophyll a in the cell was revealed using steady state spectroscopy [30]. Stationary fluorescence emission and excitation spectra of cells were recorded at room and low temperature, when the fluorescence was associated either predominantly with chlorophyll a of the PS II or with chlorophyll of both photosystems [31,32]. The energy transfer pathways either direct or mediated through chlorophyll a/c-protein were suggested but the possibility of energy migration exclusively to the PS II or also to the PS I remained under examination [33]. Superfast fluorescence measurements and global spectral analysis of the fluorescence emission were performed in a wide spectral range [34] that allowed the possible distribution of the absorbed energy between the photosystems.

Therefore, several factors did not allow to draw the definite conclusions about the possible association between phycobiliproteins and photosystems. First, the presence of two antennae, Chl a/c-protein and phycobiproteins, is unique for chloroplasts and provide for their hinder overlapping absorption and fluorescence spectral bands. Second, standard for many cryptophyte algae species absence of long-wavelength chlorophyll a forms in PS I does not allow to discriminate between PS I and PS II. Therefore, the stationary fluorescence emission spectra, the degree of photooxidation of the reaction center P700, and the action spectra of both photosystems were measured simultaneously and compared in one species, Rhodomonas salina [35].

Only in the third case, recording of the action spectra of photosynthetic activities, which has not been used earlier for investigating the pigment apparatus in cryptophytes, finally yielded conclusive evidence (Figure 1).

Plant-Biochemistry-Physiology-Action-spectra

Figure 1. Action spectra for photoreactions I (PS1, red) and II (PS2, blue) normalized to the red chlorophyll a peak of the Rhodomonas salina absorption spectrum (1-T, green). Bands belonged to phycobiliprotein (PE - phycoerythrin) and chlorophyll c (Chl c) of chlorophyll a/c-protein are designated. Absence of phycobiliprotein association with PS1 is seen clearly. The figure taken from [35] with alteration. For details of measurements see [35,36].

An advantage of this method over the others, is that the pattern of the action spectrum containing all pigment bands of each photosystem repeats the spectrum of its absorption in vivo not influenced by the presence of the other photosystem [2,36]. As a result, it was established that the exceptional association of phycobiliproteins with the PS II is the defying difference from PBSs, present in cyanobacteria and red algae [37].

References

References

  1. Bald D, Kruip J, Rogner M. Supramolecular architecture of cyanobacterial thylakoid membranes: how is the phycobilisome connected with the photosystems? Photosynth Res. 1996;49:103-118.
  2. Rakhimberdieva MG, Boichenko VA, Karapetyan NV, Stadnichuk IN. Interaction of phycobilisomes with photosystem II dimers and photosystem I monomers and trimers in the cyanobacterium Spirulina platensis. Biochemistry. 2001;40:15780-15788.
  3. Gantt E, Grabowski B, Cunningham FX. Antenna systems of red algae: Phycobilisomes with photosystem II and chlorophyll complexes with photosystem I. In: Green BR, Parson WW (eds.) Light-harvesting Antennas in Photosynthesis. Kluwert, New York. 2003;307-322.
  4. Bryant DA, Canniffe DP. How nature designs light-harvesting antenna systems: design principles and functional realization in chlorophototrophic prokaryotes. J Phys B: At Mol Opt Phys. 2018;51:033001.
  5. Arteni AA, Ajlani G, Boekema EJ. Structural organization of phycobilisomes from Synechocystis strain PCC 6803 and their interaction with the membrane. Biochim Biophys Acta. 2009;1787:272-279.
  6. Chang L, Liu X, Li Y, Liu C, Yang F. Structural organization of an intact phycobilisome and its association with photosystem II. Cell Res. 2015;25:726-737.
  7. Zlenko DV, Galochkina TV, Krasilnikov PM, Stadnichuk IN. Coupled rows of PBS cores and PSII dimers in cyanobacteria: symmetry and structure. Photosynth Res. 2017;133:245-260.
  8. Barber J, Morris EP, da Fonseca PCA. Interaction of the allophycocyanin core complex with photosystem II. Photochem Photobiol Sci. 2003;2:536-541.
  9. Elanskaya IV, Zlenko DV, Lukashev EP, Suzina NE, Stadnichuk IN. Phycobilisomes from the mutant cyanobacterium Synechocystis sp. PCC 6803 missing chromophore domain of ApcE. Biochim Biophys Acta. 2018;1859:280-291.
  10. Zlenko DV, Krasilnikov PM, Stadnichuk IN. Structural modeling of the phycobilisome core and its association with the photosystems. Photosynth Res. 2016;130:347-356.
  11. Krasilnikov PM, Zlenko DV, Stadnichuk IN. Rates and pathways of energy migration from the phycobilisome to the photosystem II and to the orange carotenoid protein in cyanobacteria. FEBS Letters. 2020;594:1145-1154.
  12. Melis A. Dynamics of photosynthetic membrane composition and function. Biochim Biophys Acta. 1991;1058:87-106.
  13. Mullineaux CW. Excitation energy transfer from phycobilisomes to photosystem I in a cyanobacterium. Biochim Biophys Acta. 1992;1100:285-292.
  14. Glazer AN, Gindt Y, Chan C F, Sauer K. Selective disruption of energy flow from phycobilisomes to Photosystem I. Photosynth. Res. 1994;40:167-173.
  15. Rakhimberdieva MG, Boichenko VA, Karapetyan NV, Stadnichuk IN. Interaction of phycobilisomes with photosystem II dimers and photosystem I monomers and trimers in the cyanobacterium Spirulina platensis. Biochemistry. 2001;40:15780-15788.
  16. Ueno Y, Aikawa S, Niwa K, Abe T, Murakami A. Variety in excitation energy transfer processes from phycobilisomes to photosystems I and II. Photosynthesis Research. 2017;133:235-243.
  17. Ke B, Fang Z-X, Lu R-Z, Calvert HE, Dolan E. The presence of phycobilisomes in heterocysts of Anabaena variabilis. Photobiochem Photobiophys. 1983;6:25-31.
  18. Bittersmann E, Vermaas W. Fluorescence lifetime studies of cyanobacterial photosystem II mutants. Biochim Biophys Acta. 1991;1098:105-116.
  19. Van Thor JJ, Gruters OWM, Matthijs HCP, Hellingwerf KJ. Localization and function of ferredoxin:NADP(+) reductase bound to the phycobilisomes of Synechocystis. EMBO J. 1999;18:4128-4136.
  20. Vanselow C, Weber APM, Krause K, Fromme P. Genetic analysis of the photosystem I subunits from the red alga, Galdieria sulphuraria, Biochim Biophys Acta. 2009;1787:46-59.
  21. Chitnis V, Chitnis P. Psal subunit is required for the formation of photosystem I trimers in the cyanobacterium Synechocystis sp. PCC 6803. FEBS Lett. 1993;336:330-334.
  22. Kruip J, Chitnis P, Lagoutte B, Rogner M, Boekema E. Structural organization of the major subunits in cyanobacterial photosystem I. Localization of subunits PsaC, -D, -E, -F, and -JJ Biol Chem. 1997;272:17061-17069.
  23. Dong C, Tang A, Zhao J, Mullineaux CW, Shen G, Bryant DA. ApcD is necessary for efficient energy transfer from phycobilisomes to photosystem I and helps to prevent photoinhibition in the cyanobacterium Synechococcus sp. PCC 7002. Biochim Biophys Acta. 2009;1787:1122-1128.
  24. Kondo K, Ochiai Y, M. Katayama M, Ikeuchi M. The membrane-associated CpcG2-phycobilisome in Synechocystis: a new photosystem I antenna. Plant Physiol. 2007;144:1200-1210.
  25. Glazer AN, Wedemayer GJ. Cryptomonad biliproteins: an evolutionary perspective. Photosynth Res. 1995;46:93-105.
  26. Hoef-Emden K, Archibald JM. Cryptophyta (Cryptomonads), in Handbook of the Protists Archibald JM (eds) Springer International Publishing AG. 2017:851-891.
  27. Mörschel E, Wehrmeyer W. Elektronen-mikroskopische feinstrukturanalyse von nativen biliproteidaggregaten und deren räumliche ordnung. Ber Dtsch Bot Ges. 1979;92:393-402.
  28. Vesk M, Dwarte D, Fowler S, Hiller RG. Freeze fracture immunocytochemistry of light-harvesting pigment complexes in a cryptophytes. Protoplasma. 1992;170:166-176.
  29. Kereiche S, Kouril R, Oostergetel GT, Fusetti F, Boekema EJ. Association of chlorophyll a/c2 complexes to photosystem I and photosystem II in the cryptophyte Rhodomonas CS24. Biochim Biophys Acta. 2008;1777:1122-1128.
  30. Chen M, Li S. H, Sun L. A novel phycocyanin-Chl a/c2-protein complex isolated from chloroplasts of Chroomonas placoidea. Chinese Chem Lett. 2007;18:1374-1378.
  31. Haxo FT, Fork DC. Photosynthetically active accessory pigments of cryptomonads. Nature. 1959;184:1051-1052.
  32. Lichtle C, Jupin CH, Duval IC. Energy transfer from PSII to PSI in Cryptomonas rufescens (Cryptophyceae). Biochim Biophys Acta. 1980;591:104-112.
  33. Bruce D, Biggins J, Steiner T, Thewalt M. Excitation energy transfer in the cryptophytes. Fluorescence excitation spectra and picosecond time-resolved emission spectra of intact algae at 77 K. Photochem Photobiol. 1986;44:519-525.
  34. Mimuro M, Tamai N, Murakami A, Watanabe M, Erata M. Multiple pathways of excitation energy flow in the photosynthetic pigment system of a cryptophyte, Cryptomonas sp. (CR-1). Phycol Res. 1998;46:155-164.
  35. Van der Weij-de Wit CD, Doust AB, Van Stokkum IHM, Dekker JP, Wilk KE. How energy funnels from the phycoerythrin antenna complex to photosystem I and photosystem II in cryptophyte Rhodomonas CS24 cells. J Phys Chem Part B. 2006;110:25066-25073.
  36. Stadnichuk IN, Novikova TM, Miniuk GS, Boichenko VA, Bolychevtseva YV. Phycoerythrin association with photosystem II in the cryptophyte alga Rhodomonas salina. Biochemistry (Moscow). 2020;85:679-688.
  37. Boichenko VA. Action spectra and functional antenna sizes of photosystems I and II in relation to the thylakoid membrane organization and pigment composition. Photosynth Res. 1998;58:163-174.

Author Info

Stadnichuk IN*
 
Timiryazev Institute of Plant Physiology, Russian Academy of Sciences, 127726 Moscow, Russia
 

Citation: Stadnichuk IN (2020) Consideration for Initial Pulse of Germination. J Plant Biochem Physiol. 8:251. DOI: 10.35248/2329-9029.20.8.251

Received: 14-Aug-2020 Accepted: 21-Aug-2020 Published: 28-Aug-2020 , DOI: 10.35248/2329-9029.20.8.251

Copyright: �??�?�© 2020 Stadnichuk IN. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Top