Staff Publications

Staff Publications

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    'Staff publications' is the digital repository of Wageningen University & Research

    'Staff publications' contains references to publications authored by Wageningen University staff from 1976 onward.

    Publications authored by the staff of the Research Institutes are available from 1995 onwards.

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Photosynthesis 2.0
Aarts, M.G.M. ; Amerongen, H. van; Bock, R. ; Carmo-Silva, Elizabete ; Croce, Roberta ; Finazzi, Giovanni ; Foyer, C. ; Genty, B. ; Harbinson, J. ; Hibberd, J. ; Klein Lankhorst, R.M. ; Schranz, M.E. ; Struik, P.C. ; Weijers, D. - \ 2019
Wageningen University and Research - 5 p.
Electrochemically Gated Long-Distance Charge Transport in Photosystem I
López-Martínez, Montse ; López-Ortiz, Manuel ; Antinori, Maria Elena ; Wientjes, Emilie ; Nin-Hill, Alba ; Rovira, Carme ; Croce, Roberta ; Díez-Pérez, Ismael ; Gorostiza, Pau - \ 2019
Angewandte Chemie-International Edition 58 (2019)38. - ISSN 1433-7851 - p. 13280 - 13284.
current decay - electrochemical gating - electron transfer - photosynthesis - scanning tunneling microscopy

The transport of electrons along photosynthetic and respiratory chains involves a series of enzymatic reactions that are coupled through redox mediators, including proteins and small molecules. The use of native and synthetic redox probes is key to understanding charge transport mechanisms and to the design of bioelectronic sensors and solar energy conversion devices. However, redox probes have limited tunability to exchange charge at the desired electrochemical potentials (energy levels) and at different protein sites. Herein, we take advantage of electrochemical scanning tunneling microscopy (ECSTM) to control the Fermi level and nanometric position of the ECSTM probe in order to study electron transport in individual photosystem I (PSI) complexes. Current–distance measurements at different potentiostatic conditions indicate that PSI supports long-distance transport that is electrochemically gated near the redox potential of P700, with current extending farther under hole injection conditions.

Light acclimation of the colonial green alga botryococcus braunii strain showa
Berg, Tomas E. van den; Chukhutsina, Volha U. ; Amerongen, Herbert van; Croce, Roberta ; Oort, Bart van - \ 2019
Plant Physiology 179 (2019)3. - ISSN 0032-0889 - p. 1132 - 1143.

In contrast to single cellular species, detailed information is lacking on the processes of photosynthetic acclimation for colonial algae, although these algae are important for biofuel production, ecosystem biodiversity, and wastewater treatment. To investigate differences between single cellular and colonial species, we studied the regulation of photosynthesis and photoprotection during photoacclimation for the colonial green alga Botryococcus braunii and made a comparison with the properties of the single cellular species Chlamydomonas reinhardtii. We show that B. braunii shares some high-light (HL) photoacclimation strategies with C. reinhardtii and other frequently studied green algae: decreased chlorophyll content, increased free carotenoid content, and increased nonphotochemical quenching (NPQ). Additionally, B. braunii has unique HL photoacclimation strategies, related to its colonial form: strong internal shading by an increase of the colony size and the accumulation of extracellular echinenone (a ketocarotenoid). HL colonies are larger and more spatially heterogenous than low-light colonies. Compared with surface cells, cells deeper inside the colony have increased pigmentation and larger photosystem II antenna size. The core of the largest of the HL colonies does not contain living cells. In contrast with C. reinhardtii, but similar to other biofilm-forming algae, NPQ capacity is substantial in low light. In HL, NPQ amplitude increases, but kinetics are unchanged. We discuss possible causes of the different acclimation responses of C. reinhardtii and B. braunii. Knowledge of the specific photoacclimation processes for this colonial green alga further extends the view of the diversity of photoacclimation strategies in photosynthetic organisms.

The Exciton Concept
Valkunas, Leonas ; Chmeliov, Jevgenij ; Amerongen, H. van - \ 2018
In: Light Harvesting in Photosynthesis / Croce, Roberta, van Grondelle, Rienk, van Amerongen, Herbert, van Stokkum, Ivo, CRC Press (Foundations of Biochemistry and Biophysics ) - ISBN 9781482218350 - p. 249 - 268.
The exciton picture is exploited for the description of molecular systems interacting with light. All the spectroscopically observed phenomena—light absorption, emission, electrostatic interaction of molecules, transitions between ground and exited electronic states, transfer of the excitation energy through the molecular aggregate, etc.—directly involve the formation and time evolution of the excitonic states. Generally, exciton is a collective molecular excitation that, depending on the strength of the intermolecular interaction, can be delocalized over several molecules. In this chapter, we discuss the basic aspects of the excitonic states in molecular dimer, aggregate, and crystal that define the spectroscopic properties of these molecular systems. We also outline various theoretical models that are widely used to describe exciton dynamics—Redfield, modified Redfield, Förster, Lindblad, and HEOM theories—as well as the conditions for their applicability.
Light Harvesting in Photosynthesis
Croce, Roberta ; Grondelle, Rienk van; Amerongen, H. van; Stokkum, Ivo H.M. van - \ 2018
Boca Raton : CRC Press - ISBN 9781482218350 - 597 p.
RAF2 is a RuBisCO assembly factor in Arabidopsis thaliana
Fristedt, Rikard ; Hu, Chen ; Wheatley, Nicole ; Roy, Laura M. ; Wachter, Rebekka M. ; Savage, Linda ; Harbinson, Jeremy ; Kramer, David M. ; Merchant, Sabeeha S. ; Yeates, Todd ; Croce, Roberta - \ 2018
The Plant Journal 94 (2018)1. - ISSN 0960-7412 - p. 146 - 156.
Abscisic acid - Atg5 g51110 - Chloroplast - RAF2 - RuBisCO - RuBisCO aggregation - RuBisCO assembly factor - SDIRIP1
Ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBisCO) catalyzes the reaction between gaseous carbon dioxide (CO2) and ribulose-1,5-bisphosphate. Although it is one of the most studied enzymes, the assembly mechanisms of the large hexadecameric RuBisCO is still emerging. In bacteria and in the C4 plant Zea mays, a protein with distant homology to pterin-4α-carbinolamine dehydratase (PCD) has recently been shown to be involved in RuBisCO assembly. However, studies of the homologous PCD-like protein (RAF2, RuBisCO assembly factor 2) in the C3 plant Arabidopsis thaliana (A. thaliana) have so far focused on its role in hormone and stress signaling. We investigated whether A. thalianaRAF2 is also involved in RuBisCO assembly. We localized RAF2 to the soluble chloroplast stroma and demonstrated that raf2 A. thaliana mutant plants display a severe pale green phenotype with reduced levels of stromal RuBisCO. We concluded that the RAF2 protein is probably involved in RuBisCO assembly in the C3 plant A. thaliana.
Introduction: light harvesting for photosynthesis
Pandit, Anjali ; Stokkum, Ivo H.M. van; Amerongen, Herbert van; Croce, Roberta - \ 2018
Photosynthesis Research 135 (2018)1-3. - ISSN 0166-8595 - p. 1 - 2.
Primary Charge Separation in the Photosystem II Reaction Center Revealed by a Global Analysis of the Two-dimensional Electronic Spectra
Duan, Hong Guang ; Prokhorenko, Valentyn I. ; Wientjes, I.E. ; Croce, Roberta ; Thorwart, Michael ; Miller, R.J.D. - \ 2017
Scientific Reports 7 (2017). - ISSN 2045-2322 - 9 p.
The transfer of electronic charge in the reaction center of Photosystem II is one of the key building blocks of the conversion of sunlight energy into chemical energy within the cascade of the photosynthetic reactions. Since the charge transfer dynamics is mixed with the energy transfer dynamics, an effective tool for the direct resolution of charge separation in the reaction center is still missing. Here, we use experimental two-dimensional optical photon echo spectroscopy in combination with the theoretical calculation to resolve its signature. A global fitting analysis allows us to clearly and directly identify a decay pathway associated to the primary charge separation. In particular, it can be distinguished from regular energy transfer and occurs on a time scale of 1.5 ps under ambient conditions. This technique provides a general tool to identify charge separation signatures from the energy transport in two-dimensional optical spectroscopy.
The complex that conquered the land : Cryo–electron microscopy reveals the structure of the plant photosystem II supercomplex
Croce, Roberta ; Amerongen, H. van - \ 2017
Science 357 (2017)6353. - ISSN 0036-8075 - p. 752 - 752.
Photosystem II (PSII) is the powerhouse of all organisms that perform oxygen-generating photosynthesis. It uses sunlight energy to extract electrons and protons from water, which fuel their metabolism. It also provides the oxygen needed by most organisms to extract energy from biomass. On page 815 of this issue, Su et al. (1) report the cryo-electron microscopy structure of the largest PSII complex of vascular plants at 2.7-Å resolution. The structure shows the details and overall organization of 28 proteins, 203 pigments, 34 lipids, and 8 other cofactors, providing the basis for understanding the functional behavior of the PSII supercomplex.
Multiple LHCII antennae can transfer energy efficiently to a single Photosystem I
Bos, Inge ; Bland, Kaitlyn M. ; Tian, Lijin ; Croce, Roberta ; Frankel, Laurie K. ; Amerongen, Herbert van; Bricker, Terry M. ; Wientjes, Emilie - \ 2017
Biochimica et Biophysica Acta. B, Bioenergetics 1858 (2017)5. - ISSN 0005-2728 - p. 371 - 378.
Excitation energy transfer - Light-harvesting complex - State transitions - Time-resolved fluorescence

Photosystems I and II (PSI and PSII) work in series to drive oxygenic photosynthesis. The two photosystems have different absorption spectra, therefore changes in light quality can lead to imbalanced excitation of the photosystems and a loss in photosynthetic efficiency. In a short-term adaptation response termed state transitions, excitation energy is directed to the light-limited photosystem. In higher plants a special pool of LHCII antennae, which can be associated with either PSI or PSII, participates in these state transitions. It is known that one LHCII antenna can associate with the PsaH site of PSI. However, membrane fractions were recently isolated in which multiple LHCII antennae appear to transfer energy to PSI. We have used time-resolved fluorescence-streak camera measurements to investigate the energy transfer rates and efficiency in these membrane fractions. Our data show that energy transfer from LHCII to PSI is relatively slow. Nevertheless, the trapping efficiency in supercomplexes of PSI with ~ 2.4 LHCIIs attached is 94%. The absorption cross section of PSI can thus be increased with ~ 65% without having significant loss in quantum efficiency. Comparison of the fluorescence dynamics of PSI-LHCII complexes, isolated in a detergent or located in their native membrane environment, indicates that the environment influences the excitation energy transfer rates in these complexes. This demonstrates the importance of studying membrane protein complexes in their natural environment.

Invitation to the 17th international congress on photosynthesis research in 2016 : photosynthesis in a changing world
Amerongen, Herbert van; Croce, Roberta - \ 2016
Photosynthesis Research 127 (2016)2. - ISSN 0166-8595 - p. 281 - 284.

The 17th International Congress on Photosynthesis will be held from August 7 to 12, 2016 in Maastricht, The Netherlands. The congress will include an opening reception, 15 plenary lectures, 28 scientific symposia, many poster sessions, displays by scientific companies, excursions, congress dinner, social activities, and the first photosynthesis soccer world championship. See . The congress is organized as an official event of the International Society of Photosynthesis Research (see

PSI-LHCI of Chlamydomonas reinhardtii: Increasing the absorption cross section without losing efficiency
Quiniou, Clothilde Le; Tian, Lijin ; Drop, B. ; Wientjes, Emilie ; Stokkum, I.H.M. van; Oort, Bart van; Croce, R. - \ 2015
Biochimica et Biophysica Acta. B, Bioenergetics 1847 (2015)4-5. - ISSN 0005-2728 - p. 458 - 467.
Photosystem I (PSI) is an essential component of photosynthetic membranes. Despite the high sequence and structural homologies, its absorption properties differ substantially in algae, plants and cyanobacteria. In particular it is characterized by the presence of low-energy chlorophylls (red forms), the number and the energy of which vary in different organisms. The PSI–LHCI (PSI–light harvesting complex I) complex of the green alga Chlamydomonas reinhardtii (C.r.) is significantly larger than that of plants, containing five additional light-harvesting complexes (together binding ≈ 65 chlorophylls), and contains red forms with higher energy than plants. To understand how these differences influence excitation energy transfer and trapping in the system, we studied two PSI–LHCI C.r. particles, differing in antenna size and red-form content, using time-resolved fluorescence and compared them to plant PSI–LHCI. The excited state kinetics in C.r. shows the same average lifetime (50 ps) as in plants suggesting that the effect of antenna enlargement is compensated by higher energy red forms. The system equilibrates very fast, indicating that all Lhcas are well-connected, despite their long distance to the core. The differences between C.r. PSI–LHCI with and without Lhca2 and Lhca9 show that these Lhcas bind red forms, although not the red-most. The red-most forms are in (or functionally close to) other Lhcas and slow down the trapping, but hardly affect the quantum efficiency, which remains as high as 97% even in a complex that contains 235 chlorophylls.
Light-harvesting kinetics in plant leaves visualized by means of fluorescence lifetime imaging microscopy
Iermak, I. ; Vink, J. ; Bielczynski, L. ; Croce, R. ; Bader, A. ; Amerongen, H. van - \ 2014
In: Abstracts of the FOM meeting 2014. - - p. 19 - 19.
Natural strategies for photosynthetic light harvesting
Croce, R. ; Amerongen, H. van - \ 2014
Nature Chemical Biology 10 (2014). - ISSN 1552-4450 - p. 492 - 501.
photosystem-ii antenna - excitation-energy transfer - chlamydomonas-reinhardtii - oxygenic photosynthesis - chlorophyll-d - acaryochloris-marina - angstrom resolution - carotenoid protein - state transitions - crystal-structure
Photosynthetic organisms are crucial for life on Earth as they provide food and oxygen and are at the basis of most energy resources. They have a large variety of light-harvesting strategies that allow them to live nearly everywhere where sunlight can penetrate. They have adapted their pigmentation to the spectral composition of light in their habitat, they acclimate to slowly varying light intensities and they rapidly respond to fast changes in light quality and quantity. This is particularly important for oxygen-producing organisms because an overdose of light in combination with oxygen can be lethal. Rapid progress is being made in understanding how different organisms maximize light harvesting and minimize deleterious effects. Here we summarize the latest findings and explain the main design principles used in nature. The available knowledge can be used for optimizing light harvesting in both natural and artificial photosynthesis to improve light-driven production processes.
State transitions in Chlamydomonas reinhardtii strongly modulate the functional size of photosystem II but not of photosystem I
Ünlü, C. ; Drop, B. ; Croce, R. ; Amerongen, H. van - \ 2014
Proceedings of the National Academy of Sciences of the United States of America 111 (2014)9. - ISSN 0027-8424 - p. 3460 - 3465.
light-harvesting-complex - excitation-energy transfer - resolved chlorophyll fluorescence - alga scenedesmus-obliquus - protein-phosphorylation - thylakoid membrane - charge separation - supramolecular organization - arabidopsis-thaliana - angstrom resolution
Plants and green algae optimize photosynthesis in changing light conditions by balancing the amount of light absorbed by photosystems I and II. These photosystems work in series to extract electrons from water and reduce NADP+ to NADPH. Light-harvesting complexes (LHCs) are held responsible for maintaining the balance by moving from one photosystem to the other in a process called state transitions. In the green alga Chlamydomonas reinhardtii, a photosynthetic model organism, state transitions are thought to involve 80% of the LHCs. Here, we demonstrate with picosecond-fluorescence spectroscopy on C. reinhardtii cells that, although LHCs indeed detach from photosystem II in state 2 conditions, only a fraction attaches to photosystem I. The detached antenna complexes become protected against photodamage via shortening of the excited-state lifetime. It is discussed how the transition from state 1 to state 2 can protect C. reinhardtii in high-light conditions and how this differs from the situation in plants.
Light-harvesting in photosystem I
Croce, R. ; Amerongen, H. van - \ 2013
Photosynthesis Research 116 (2013)2-3. - ISSN 0166-8595 - p. 153 - 166.
excitation-energy transfer - time-resolved fluorescence - ultrafast transient absorption - pigment-pigment interactions - charge separation kinetics - psi-lhci supercomplex - chlamydomonas-reinhardtii - higher-plants - complex-i - synechococcus-elongatus
This review focuses on the light-harvesting properties of photosystem I (PSI) and its LHCI outer antenna. LHCI consists of different chlorophyll a/b binding proteins called Lhca’s, surrounding the core of PSI. In total, the PSI-LHCI complex of higher plants contains 173 chlorophyll molecules, most of which are there to harvest sunlight energy and to transfer the created excitation energy to the reaction center (RC) where it is used for charge separation. The efficiency of the complex is based on the capacity to deliver this energy to the RC as fast as possible, to minimize energy losses. The performance of PSI in this respect is remarkable: on average it takes around 50 ps for the excitation to reach the RC in plants, without being quenched in the meantime. This means that the internal quantum efficiency is close to 100 % which makes PSI the most efficient energy converter in nature. In this review, we describe the light-harvesting properties of the complex in relation to protein and pigment organization/composition, and we discuss the important parameters that assure its very high quantum efficiency. Excitation energy transfer and trapping in the core and/or Lhcas, as well as in the supercomplexes PSI-LHCI and PSI-LHCI-LHCII are described in detail with the aim of giving an overview of the functional behavior of these complexes.
Light harvesting in photosystem II
Amerongen, H. van; Croce, R. - \ 2013
Photosynthesis Research 116 (2013)2-3. - ISSN 0166-8595 - p. 251 - 263.
excitation-energy transfer - plant thylakoid membranes - time-resolved fluorescence - chlorophyll a/b complex - psbs protein controls - charge separation - reaction centers - transient absorption - antenna complexes - electron-transfer
Water oxidation in photosynthesis takes place in photosystem II (PSII). This photosystem is built around a reaction center (RC) where sunlight-induced charge separation occurs. This RC consists of various polypeptides that bind only a few chromophores or pigments, next to several other cofactors. It can handle far more photons than the ones absorbed by its own pigments and therefore, additional excitations are provided by the surrounding light-harvesting complexes or antennae. The RC is located in the PSII core that also contains the inner light-harvesting complexes CP43 and CP47, harboring 13 and 16 chlorophyll pigments, respectively. The core is surrounded by outer light-harvesting complexes (Lhcs), together forming the so-called supercomplexes, at least in plants. These PSII supercomplexes are complemented by some “extra” Lhcs, but their exact location in the thylakoid membrane is unknown. The whole system consists of many subunits and appears to be modular, i.e., both its composition and organization depend on environmental conditions, especially on the quality and intensity of the light. In this review, we will provide a short overview of the relation between the structure and organization of pigment-protein complexes in PSII, ranging from individual complexes to entire membranes and experimental and theoretical results on excitation energy transfer and charge separation. It will become clear that time-resolved fluorescence data can provide invaluable information about the organization and functioning of thylakoid membranes. At the end, an overview will be given of unanswered questions that should be addressed in the near future.
Quantum yield of charge separation in photosystem II: functional effect of changes in the antenna size upon light acclimation
Wientjes, E. ; Amerongen, H. van; Croce, R. - \ 2013
The Journal of Physical Chemistry Part B: Condensed Matter, Materials, Surfaces, Interfaces & Biophysical 117 (2013)38. - ISSN 1520-6106 - p. 11200 - 11208.
excitation-energy transfer - arabidopsis-thaliana - chlorophyll fluorescence - supramolecular organization - harvesting antenna - green plants - chlamydomonas-reinhardtii - photosynthetic apparatus - thylakoid membrane - grana membranes
We have studied thylakoid membranes of Arabidopsis thaliana acclimated to different light conditions and have related protein composition to excitation energy transfer and trapping kinetics in Photosystem II (PSII). In high light: the plants have reduced amounts of the antenna complexes LHCII and CP24, the overall trapping time of PSII is only 180 ps, and the quantum efficiency reaches a value of 91%. In low light: LHCII is upregulated, the PSII lifetime becomes 310 ps, and the efficiency decreases to 84%. This difference is largely caused by slower excitation energy migration to the reaction centers in low-light plants due to the LHCII trimers that are not part of the C2S2M2 supercomplex. This pool of “extra” LHCII normally transfers energy to both photosystems, whereas it transfers only to PSII upon far-red light treatment (state 1). It is shown that in high light the reduction of LHCII mainly concerns the LHCII-M trimers, while the pool of “extra” LHCII remains intact and state transitions continue to occur. The obtained values for the efficiency of PSII are compared with the values of Fv/Fm, a parameter that is widely used to indicate the PSII quantum efficiency, and the observed differences are discussed.
LHCII is an antenna of both photosystems after long-term acclimation
Wientjes, E. ; Amerongen, H. van; Croce, R. - \ 2013
Biochimica et Biophysica Acta. B, Bioenergetics 1827 (2013)3. - ISSN 0005-2728 - p. 420 - 426.
light-harvesting complex - excitation-energy transfer - protein-phosphorylation - state transitions - arabidopsis-thaliana - thylakoid membrane - supramolecular organization - photosynthetic apparatus - dependent regulation - higher-plants
LHCII, the most abundant membrane protein on earth, is the major light-harvesting complex of plants. It is generally accepted that LHCII is associated with Photosystem II and only as a short-term response to overexcitation of PSII a subset moves to Photosystem I, triggered by its phosphorylation (state1 to state2 transition). However, here we show that in most natural light conditions LHCII serves as an antenna of both Photosystem I and Photosystem II and it is quantitatively demonstrated that this is required to achieve excitation balance between the two photosystems. This allows for acclimation to different light intensities simply by regulating the expression of LHCII genes only. It is demonstrated that indeed the amount of LHCII that is bound to both photosystems decreases when growth light intensity increases and vice versa. Finally, time-resolved fluorescence measurements on the photosynthetic thylakoid membranes show that LHCII is even a more efficient light harvester when associated with Photosystem I than with Photosystem II.
Photosynthetic Quantum Yield Dynamics: From Photosystems to Leaves
Hogewoning, S.W. ; Wientjes, E. ; Douwstra, P. ; Trouwborst, G. ; Ieperen, W. van; Croce, R. ; Harbinson, J. - \ 2012
The Plant Cell 24 (2012)5. - ISSN 1040-4651 - p. 1921 - 1935.
chlorophyll-protein complexes - singlet energy-transfer - plastid redox signals - arabidopsis-thaliana - light environment - state transitions - action spectrum - leaf photosynthesis - vascular plants - beta-carotene
The mechanisms underlying the wavelength dependence of the quantum yield for CO2 fixation (a) and its acclimation to the growth-light spectrum are quantitatively addressed, combining in vivo physiological and in vitro molecular methods. Cucumber (Cucumis sativus) was grown under an artificial sunlight spectrum, shade light spectrum, and blue light, and the quantum yield for photosystem I (PSI) and photosystem II (PSII) electron transport and a were simultaneously measured in vivo at 20 different wavelengths. The wavelength dependence of the photosystem excitation balance was calculated from both these in vivo data and in vitro from the photosystem composition and spectroscopic properties. Measuring wavelengths overexciting PSI produced a higher a for leaves grown under the shade light spectrum (i.e., PSI light), whereas wavelengths overexciting PSII produced a higher a for the sun and blue leaves. The shade spectrum produced the lowest PSI:PSII ratio. The photosystem excitation balance calculated from both in vivo and in vitro data was substantially similar and was shown to determine a at those wavelengths where absorption by carotenoids and nonphotosynthetic pigments is insignificant (i.e., >580 nm). We show quantitatively that leaves acclimate their photosystem composition to their growth light spectrum and how this changes the wavelength dependence of the photosystem excitation balance and quantum yield for CO2 fixation. This also proves that combining different wavelengths can enhance quantum yields substantially.
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