Chemical tools to study photosynthesis
Figure 1. Schematic representation of the electron transfer chain with commonly used chemical tools. Figure adapted from: http://jonnield.com/en/science/psII_images.html
DCMU (3-(3′,4′-dichlorophenyl)-1,1-dimethylurea)
DCMU displaces the secondary quinone acceptor, QB, from its binding site at the D1 protein of Photosystem II (PSII) [1], [2]. DCMU is not redox active and prevents the re-oxidation of QA− by forward electron transport.[3]
Electron-dependent competition between plastoquinone and inhibitors for binding to Photosystem II. FEBS Lett., 126 (1981), pp. 277-281
Oxidation-reduction physical chemistry of the acceptor quinone complex in bacterial photosynthetic reaction centers: evidence for a new model of herbicide activity. Isr. J. Chem., 21 (1981), pp. 348-354
In intact leaves, the maximum fluorescence level (FM) is independent of the redox state of the plastoquinone pool: a DCMU-inhibition study." Biochimica et Biophysica Acta (BBA)-Bioenergetics 1708.2 (2005): 275-282.
DBMIB (dibromothymoquinone)
DBMIB inhibits the reoxidation of plastoquinol by binding to the cytochrome b6/f complex [1]. DBMIB is an artificial quinone introduced in 1970 by Trebst et al. [2] and Böhme et al. [3] as an inhibitor of photosynthetic electron transport and an antagonist of PQ. It was shown that cyt b6/f can accept only one electron from DBMIB. As a semiquinone it remains tightly bound to the cyt b6/f complex preventing in this way the reoxidation of other PQH2 molecules by cyt b6/f[4].
Methylviologen and dibromothymoquinone treatments of pea leaves reveal the role of photosystem I in the Chl a fluorescence rise OJIP. Biochimica et Biophysica Acta (BBA)-Bioenergetics 1706.3 (2005): 250-261.
On a new inhibitor of photosynthetic electron-transport in isolated chloroplasts. Z. Naturforsch., 25b (1970), pp. 1157-1159
The effect of dibromothymoquinone, an antagonist of plastoquinone, on non cyclic and cyclic electron flow systems in isolated chloroplasts. Z. Naturforsch., 26b (1971), pp. 341-352
The interactions of duroquinol, DBMIB and NQNO with the chloroplast cytochrome bf complex. Biochim. Biophys. Acta, 1058 (1991), pp. 312-328
MV (methylviologen; paraquat)
MV accepts electrons from the FeS clusters of PSI and it allows electrons to bypass the block that is transiently imposed by ferredoxin-NADP+-reductase (FNR) (inactive in dark-adapted chloroplasts) [1]. MV is thought to be a very effective electron acceptor that competes strongly with ferredoxin for electrons from the FeS clusters of PSI and, as a consequence, strongly suppresses cyclic electron transfer around PSI [2], [3].
MV is not a direct inhibitors of the electron transport system, but rather a drain off electrons from photosystem I, preventing NADP reduction [4].
Methylviologen and dibromothymoquinone treatments of pea leaves reveal the role of photosystem I in the Chl a fluorescence rise OJIP." Biochimica et Biophysica Acta (BBA)-Bioenergetics 1706.3 (2005): 250-261.
Flexible coupling between light-dependent electron and vectorial proton transport in illuminated leaves of C3 plants; role of photosystem I-dependent proton pumping. Planta, 210 (2000), pp. 468-477
Irrungen, Wirrungen The Mehler reaction in relation to cyclic electron transport in C3 plants. Photosynth. Res., 73 (2002), pp. 223-231
Inhibitors in the functional dissection of the photosynthetic electron transport system. Photosynthesis research 92.2 (2007): 217-224.
Sulfo-DSPD (disulfodisalicylidenepropanediamine)
Sulfo-DSPD has been shown to inhibit ferredoxin-dependent reactions with both chloroplast and membrane-free systems [1,2,3]. Its site of inhibition has been placed before ferredoxin reduction in the electron transport sequence [2] or at ferredoxin itself [3].
Sulfo-DSPD inhibits at the acceptor side of photosystem I (lipophilic DSPD does not), but because of its very hydrophilic nature, it is active only in exposed thylakoid membrane preparations [4].
Electron transport pathways in spinach chloroplasts. Reduction of the primary acceptor of photosystem II by reduced nicotinamide adenine dinucleotide phosphate in the dark. Biochimica et Biophysica Acta (BBA)-Bioenergetics 547.1 (1979): 127-137.
Trebst, A., and M. Burba. "Über die Hemmung photosynthetischer Reaktionen in isolierten Chloroplasten und in Chlorella durch Disalicylidenpropandiamin." Z. Pflanzenphysiol 57 (1967): 419-433.
Is nicotinamide adenine dinucleotide phosphate an obligatory intermediate in photosynthesis?. Plant physiology 49.2 (1972): 244-248.
Inhibitors in the functional dissection of the photosynthetic electron transport system. Photosynthesis research 92.2 (2007): 217-224.
AA (Antimycin A3)
AA inhibits PGR5–PGRL1-dependent PSI cyclic electron transport [1]. Chloroplast NDH also accepts electrons from ferredoxin (Fd) but is resistant to AA [2]. AA was originally discovered to inhibit respiratory electron transport by binding to the Qi site of the cytochrome (Cyt) bc1 complex [3]. However, AA does not bind to the corresponding site of the Cyt b6f complex in chloroplasts. AA was shown to inhibit electron transport from recombinant PGRL1 to the plastoquinone (PQ) analog 2,6-dimethyl-p-benzoquinone in vitro [4], and PGR5 may function in the Fd-dependent reduction of PGRL1 in vivo [5]. Consistent with these results, a single amino acid alteration in PGR5 confers resistance of PSI cyclic electron transport to AA [6]. AA most likely inhibits the function of the PGR5–PGRL1 protein complex, although the exact mode of inhibition is still unclear [1].
Antimycin A‐like molecules inhibit cyclic electron transport around photosystem I in ruptured chloroplasts." FEBS Open Bio 3.1 (2013): 406-410.
An Src homology 3 domain-like fold protein forms a ferredoxin-binding site for the chloroplast NADH dehydrogenase-like complex in Arabidopsis. Plant Cell. 2011;23:1480–1493.
Crystal structure of the cytochrome bc1 complex from bovine heart mitochondria. Science. 1997;277:60–66
PGRL1 is the elusive ferredoxin–plastoquinone reductase in photosynthetic cyclic electron flow. Mol. Cell. 2013;49:511–523
A complex containing PGRL1 and PGR5 is involved in the switch between linear and cyclic electron flow in Arabidopsis. Cell. 2008;132:273–285.
A single amino acid alteration in PGR5 confers resistance to antimycin A in cyclic electron transport around PSI. Plant Cell Physiol. 2013
Asc (Ascorbate, vitamin C)
Asc has been shown to support DCMU-sensitive photoreduction of NADP+ in thylakoids isolated from heat-treated Euglena gracilis cells [1] and it has also been shown to donate electrons to PSII in tris(hydroxymethyl)aminomethane (Tris)-washed thylakoids [2]. Asc donates electrons to TyrZ+ as shown by electron paramagnetic resonance [3] and thermoluminescence measurements [4, 5]. When PSII is inhibited by DCMU in isolated thylakoid membranes, Asc can act as an electron donor to PSI [6].
Ascorbate-supported NADP photoreduction by heated Euglena chloroplasts. Arch Biochem Biophys 122: 144–152
Photoreduction and photophosphorylation with Tris-washed chloroplasts. Plant Physiol 43: 1978–1986
Photosystem II oxidation of charged electron donors. Surface charge effects. Biochim Biophys Acta 590: 360–372
Experimental evidence for ascorbate-dependent electron transport in leaves with inactive oxygen-evolving complexes. Plant Physiol 149: 1568–1578
The physiological roles and metabolism of ascorbate in chloroplasts. Physiologia plantarum 148.2 (2013): 161-175.
Ascorbate in thylakoid lumen functions as an alternative electron donor to photosystem II and photosystem I. Arch Biochem Biophys 429: 71–80
DCPIP (Dichlorophenol-indophenol)
DAD (Diaminodurene = 2,3,5,6-tetramethyl-pphenylenediamine)
TMPD (N-tetramethyl-p-phenylenediamine)
Donor systems for photosystem I such as DCPIP, DAD or TMPD, kept reduced by ascorbate, are not inhibited by either DCMU or DBMIB. They are coupled to ATP formation [1].
Trebst, Achim. "Inhibitors in the functional dissection of the photosynthetic electron transport system." Photosynthesis research 92.2 (2007): 217-224.Photoreduction and photophosphorylation with Tris-washed chloroplasts. Plant Physiol 43: 1978–1986
DPC (Diphenylcarbazide)
Donor systems for photosystem I such as DCPIP, DAD or TMPD, kept reduced by ascorbate, are not inhibited by either DCMU or DBMIB. They are coupled to ATP formation [1].
Rashid, Abdur, and Radovan Popovic. "Electron donation to photosystem II by diphenylcarbazide is inhibited both by the endogenous manganese complex and by exogenous manganese ions." Biochemistry and cell biology 73.5-6 (1995): 241-245.
Hydroxylamine (NH2OH)
CCCP (carbonylcyanide-phenylhyrazones)
Hydroxylamine and carbonylcyanide-phenylhyrazones (CCCP) act on the donor side of photosystem II both as inhibitor and donor. [1]. Hydroxylamine action on PSII occurs in two steps: an initial reversible reduction of manganese by two electrons at low concentrations (≤5 NH2OH / PSII) followed by, at higher concentrations, further reduction that is irreversible due to the release of 3 out of 4 Mn/PSII [2, 3]. Hydroxylamine can also be used for manganese-depletion accomplished by incubating thawed Ca-depleted PSII membranes (0.5 mg Chl/ml) for 5 min at 5 °C in the dark with 1 mM hydroxylamine [4, 5].
CCCP is oxidized by the photosystem II donor side and is reduced by the plastoquinon pool [6]. CCCP is additionally an effective protonophone which can be used to disipathe the DeltapH [7].
Trebst, Achim. "Inhibitors in the functional dissection of the photosynthetic electron transport system." Photosynthesis research 92.2 (2007): 217-224.Photoreduction and photophosphorylation with Tris-washed chloroplasts. Plant Physiol 43: 1978–1986
Sivaraja, M., and G. Charles Dismukes. "Binding of hydroxylamine to the water-oxidizing complex and the ferroquinone electron acceptor of spinach photosystem II." Biochemistry 27.9 (1988): 3467-3475.
Radmer, Richard, and Otto Ollinger. "Topography of the O2-evolving site determined with water analogs." FEBS Letters 152.1 (1983): 39-43.
An improved procedure for photoactivation of photosynthetic oxygen evolution: effect of artificial electron acceptors on the photoactivation yield of NH2OH-treated wheat Photosystem II membranes. Biochim Biophys Aсta 1056:47–56
Semin, Boris K., et al. "The extrinsic PsbO protein modulates the oxidation/reduction rate of the exogenous Mn cation at the high-affinity Mn-binding site of Mn-depleted PSII membranes." Journal of bioenergetics and biomembranes 47.4 (2015): 361-367.
Samuilov, Vitaly D., and Eugene L. Barsky. "Interaction of carbonyl cyanide m-chlorophenylhydrazone with the photosystem II acceptor side." FEBS letters 320.2 (1993): 118-120.
Bottomley, P. J., and W. D. P. Stewart. "ATP and nitrogenase activity in nitrogen‐fixing heterocystous blue‐green algae." New Phytologist 79.3 (1977): 625-638.
mercuric chloride (HgCl2)
Incubation of chloroplasts with HgCl2 at a molar ratio of HgCl2 to chlorophyll of about unity, induced a complete inhibition of the methylviologen Hill reaction, as well as methylviologen photoreduction with reduced DCPIP as electron donor. [1].
Kimimura, Mamiko, and Sakae Katoh. "Studies on electron transport associated with photosystem II Functional site of plastocyanin: inhibitory effects of HgCl2 on electron transport and plastocyanin in chloroplasts." Biochimica et Biophysica Acta (BBA)-Bioenergetics 283.2 (1972): 279-292.
ionophores
Nigericin
Nigericin dissipates chloroplast thylakoid membrane proton gradient by transferring H+ ions into the lumen [1]. Nigericin is a linear molecule with heterocyclic oxygen-containing rings together with a hydroxyl group. It catalyses the overall electroneutral exchange of K+ for H+ [2].
Allnutt, F. C. T., et al. "Nigericin and hexylamine effects on localized proton gradients in thylakoids." Biochimica et Biophysica Acta (BBA)-Bioenergetics 1059.1 (1991): 28-36.
Nicholls, D. G., and S. J. Ferguson. "Ion transport across energy-conserving membranes." Bioenergetics (Elsevier, Amsterdam), (2013): 13-25.
FCCP (carbonylcyanide-p-(trifluoromethoxy) phenylhydrazone)
The protonophore FCCP has been shown to be able to decrease the cellular ATP content and to increase the NADPH concentration [1, 2, 3]. FCCP is the most commonly employed example of a protonophore [4].
Bulté, Laurence, et al. "ATP control on state transitions in vivo in Chlamydomonas reinhardtii." Biochimica et Biophysica Acta (BBA)-Bioenergetics 1020.1 (1990): 72-80.
Forti, Giorgio, et al. "In vivo changes of the oxidation-reduction state of NADP and of the ATP/ADP cellular ratio linked to the photosynthetic activity in Chlamydomonas reinhardtii." Plant physiology 132.3 (2003): 1464-1474.
Forti, Giorgio. "The role of respiration in the activation of photosynthesis upon illumination of dark adapted Chlamydomonas reinhardtii." Biochimica et Biophysica Acta (BBA)-Bioenergetics 1777.11 (2008): 1449-1454.
Nicholls, D. G., and S. J. Ferguson. "Ion transport across energy-conserving membranes." Bioenergetics (Elsevier, Amsterdam), (2013): 13-25.
Valinomycin
Exposure of biological membranes to the ionophore valinomycin selectively increases K+ conductance and allows for rapid electrochemical gradient-driven K+ fluxes. [1, 2]
Wu, Weihua, and Gerald A. Berkowitz. "Stromal pH and photosynthesis are affected by electroneutral K+ and H+ exchange through chloroplast envelope ion channels." Plant Physiology 98.2 (1992): 666-672.
Ort, Donald. "On the mechanism of control of photosynthetic electron transport by phosphorylation." FEBS letters 69.1-2 (1976): 81-85
Good learning resource from Larry Orr and Govindjee:
https://www.life.illinois.edu/govindjee/photoweb/individual.html