The Light Reactions: A Guide to Recent Acquisitions for the Picture Gallery

The past two years have brought major additions to the steadily growing collection of molecular pictures of the components of the photosynthetic apparatus: new structural work on photosystem II (PSII; Biesiadka et al., 2004; Ferreira et al., 2004) and of light-harvesting complex II (LHCII; Liu et al., 2004), solved at higher resolution than those previously available, thus allowing for more refined models of key features, a long-awaited view of the cytochrome b6f complex, in two pleasingly concordant versions by two independent groups (Kurisu et al., 2003; Stroebel et al., 2003), and finally a portrait of a supercomplex of a reaction center associated with its antenna—PSI with LHCI (Ben-Shem et al., 2003). The virtual identity of the composition and arrangement of cofactors in complexes that are separated by a billion years of evolution is striking, justifying fully the absence of organism-specific bias in photosynthesis research. On the other hand, the differences in protein–protein interactions show that the structures presented for complexes represent “a” structure rather than “the” structure, emphasizing the unique biological adaptations to ecological niches and environmental variation. At the mechanistic level, the structural advances provide the basis for new hypotheses that in turn suggest experiments that will occupy biophysicists and molecular geneticists alike for the next decade. The light reactions of photosynthesis describe the pathway in which electrons are removed from water and transferred to NADP+ or ferredoxin to generate reduced cofactors for biosynthetic metabolism (reviewed in Nelson and Ben-Shem, 2004). This process, which makes use of abundant resources on the planet—water and sunlight—is responsible for the creation and maintenance of aerobic life on earth, directly through the generation of oxygen and indirectly through the subsequent biosynthesis (dark reactions) of reduced organic compounds that serve as fuels for heterotrophic life. Intuitively, without an appreciation of thermodynamics, one understands that water is a weak reductant because the product of its oxidation (i.e., removal of electrons), oxygen, is a powerful oxidant. Therefore, an oxidant that is more oxidizing (i.e., more positive redox potential) than molecular oxygen is required to drive water oxidation in vivo. This is accomplished by the primary reactions of PSII, which generate the most powerful oxidant known in biology, P680+. Likewise, the function of PSI is to generate a reductant that is more reducing (i.e., more negative redox potential) than ferredoxin and NADP+. An Updated Z-Scheme Describing Photosynthetic Electron Transfer. Each carrier is shown in both its oxidized and reduced form to facilitate the readers' understanding of the sequence of steps, in which each carrier accepts an electron from a donor to become reduced and is reoxidized as it gives an electron to an acceptor. The midpoint potentials of the carriers in this version of the scheme have been updated to reflect the recent literature but are yet only approximate, owing in part to artistic aesthetics and in part to the intrinsic difficulty of estimating these numbers. In the cytochrome b6f complex (shown in pink to distinguish it as a heme-containing complex), the donor (reduced plastoquinol PQH2) provides two electrons: one is transferred through the Rieske FeS protein and cytochrome f to plastocyanin (or cytochrome c6) to photosystem I, while the other is transferred through the b-hemes to a bound on the The to and from of the redox carrier from the that electron The from the to the with an of a of the carriers to have in and and in and these have a in that the carriers been as In this is as and as to the from and have a for the electron cofactors in the of biological reactions in the but rather in the of and these use of light it is that the only by electron rather than through other and this is accomplished through the structure of the which are for is more that the electrons from carriers in the transferred to the of the makes it that is a for the of an electron from or or to but this reaction is The electron transferred in the sequence shown for An the of other groups or compounds in the of The midpoint potentials of the primary in PSI of a at in to for the reaction is but are in to these in of and electron the is the the of electron in each is to electron PSII, the of the oxidation of a of water is to electron a for structural and are with the of the of the photosynthetic which for is to to a or is the of the its components generate that the the light is the of these the and of is a of the view of the photosynthetic at resolution is a for understanding its and or is the in the pathway The models of the with to the cofactors in on the structural and of to the reaction in the structures years et al., et al., and these and refined by structural models of from at and resolution et al., in and and 2003). the that in the unique water oxidation of in those recent describe structures on Ferreira et at and Biesiadka et at a view of the and provide for the differences and primary and the reaction and both show models for the and of the the of electron from the of cytochrome and a to and suggest for the The structural from Ferreira et at resolution than the one from Biesiadka et a more arrangement of in the which of and on the reaction for water oxidation and 2004). The reactions of separated for the of the primary which is the of and the of an electron from the to a in the to generate the separated electron from to the in the reaction center to generate the product of the and the of by water through a the and a in The cofactors in PSII, on are The view is to the The scheme of Ferreira et is are in with the shown as a The are from reaction center by the use of for the for the and are in to distinguish from and in cytochrome is in in in and in The of is for The are shown as for for and for The of and the are shown as for for and for The an of the as by Ferreira et with on the and on the and a on are as Ferreira et that is the structure of the The and the of the The is and for the that most of the cofactors in are because been as in and for with the as from The is cytochrome the of the of the and other are as to generate this and other In to the are in a while those that are more are in a The electron from is transferred to and from to the is reduced by a electron and the for the cytochrome b6f in the reaction is an the two Electron this been to to a which electron and on for the and which facilitate of reduced et al., 2004). the structural for the the reaction center and PSII, is a key and in The a more positive redox to for electron from water than in the reaction center to The structures suggest an et al., 2004; Ferreira et al., 2004). The and is than that of the in the reaction which and the is more This that the is in with the reaction and this to a more positive redox the is of other with the in a for the oxidizing P680+. of of redox and to of the in P680+. This reaction to a which will the of the water oxidation The of oxidation is of it as removal (i.e., electron this to to a for of the from to the and both of the recent models show a and a for and water the but the and this is the that the is only a that one of the oxidation in the oxidation of water and 2004). 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Therefore, for reducing have in a are of the and of the electron from the to is the of cytochrome and in these with as the donor to P680+. of the recent structures on the of an cytochrome and to P680+. 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The of these molecular are in structural and with are The new which is the in arrangement in Biesiadka et al., 2004), provides a structural for the of and at the center of the for in and and which are with and et al., 2004). will and by and the structure will from that will more of electron which is for the that to the et al., 2004). a the of the structure and of cofactors and makes the of and the of the more and for the primary reactions of photosynthesis is a light-harvesting or which to the of the for The associated with the reaction center is to as the but are that with each The in of or allowing photosynthetic to of a of the and ecological niches with a of light and 2003). In the of protein complexes through and through the “a” to the of LHCI and to the of and and and et al., The most abundant of for of the in the is a of and in and are the most abundant and more to each to have unique et al., 2004; and 2004). the and is to the of the that of and function is a of only because of its and light-harvesting but because it is a key of that light The of the is by as a to light At a more level, the complex is by on the redox of a carrier the two a in the cytochrome b6f that it and with the carrier is more oxidized but with PSI the carrier is more reduced and recent work a for in of light et al., et al., for a mechanistic understanding of function in light as as of light is a structure the identity and of This been through the work of Liu et a structural of at resolution on of the complex in This structure that in the structural et al., of bound the a and and the for of in The is the from the The is from the as in a to facilitate of in the two The of for for the for the from to and of the as a two of and with a which the of the is from Liu et The are in for for and for the in the to the than those are shown as in the The in that are the in the The is in the of the to the as in The show the on the of The structure of is shown with of and In the is a is the of The of the through the of and and the through the of and the the is to as a both as function as a for the structure, and these are for structural and for in of the protein and et al., to a and a that the to the of the for this The known with and is The in the of are known as the or and the in the of the as the The is the of the and is known as the This is the that is most for the in complexes of the the of a for the of a light-harvesting from to the the two is a for understanding the of The of the and the for of but to electron is a of with each other and to the and this of structural in the work by Liu et for understanding the of view of to the that the are in two one to the with and the other to the with the The of the arrangement of in the of the a with view the from the the arrangement of in the in two The of and these are to function in In the a of with a is Liu et suggest that this light from in a with to a is of in the complex), from it for the reaction center and The and of a and a in the structural gives the and the of this acceptor. On the the is and and it is that the function of the with to light of the two and function in light the are for to a and the to two and this is with The of as light-harvesting the of to the of a light and is in the are for of the to the Electron is one and this is to as the pathway is light the for use of reducing in the is a that the to as are the An part of is a that is associated with and light will for or as et al., et al., et al., 2004). The on of the a a in a and the of the of to and one on in PSII, to a an as yet by its to a and to the et al., is of the of directly in because the is in an et al., Liu et models for an in on in one suggest that on the of the groups in which and of the and the This in turn a to the of a a a from in the are but the of and the for in the of new the of the recent et al., 2004), the with to light-harvesting protein function is are of at the of with and of with to which to the of and will structural differences the in in the the that are to the reaction center and the The of the and of from the to to structural of a The in the the cytochrome b6f complex, or plastoquinol to the plastoquinol product from The product of the reaction is reduced plastocyanin in and reduced cytochrome which in turn will (reviewed in et al., Electron through the cytochrome b6f complex is to which makes its a major to the generation of a for of the plastoquinol to the product two electrons and two but the cofactors in plastocyanin and cytochrome are only the of electron and in the complex is a key of b6f is a the two electrons the cytochrome b6f complex while PSI electrons of the cytochrome b6f complex a in light use by the redox of the electron to The of in which the with or PSI is on the cytochrome b6f complex 2004). electron the complex is than electron from the complex the from to PSI to the The of is by its which is by a is by of one of the plastoquinol in the cytochrome b6f complex the redox of the et al., 2003). The cytochrome b6f complex electrons from components that are reduced by the primary of a in the cytochrome b6f complex is directly reduced or the complex only indirectly the is a et al., 2004). the of electron through the cytochrome b6f and cytochrome this electron pathway is to as electron is oxidation or in the the of the by PSI is to generate a the cytochrome b6f complex, and this is to The use of PSI provides a for the of reducing and reduced and by the light the of the for understanding its in redox to and for the of electron a view of the cytochrome b6f complex is a groups have that view by the structure of and complexes (Kurisu et al., 2003; Stroebel et al., 2003). the of the with the the cytochrome b6f complex is the complex in the to at this of resolution and this because of its to the from a to and the of for of the (Kurisu et al., 2003), the other a one of the to facilitate et al., 2003). in the b6f The from the structure to generate the (Kurisu et al., 2003). The complex is in form in the of the with the on the as in is shown in of cytochrome and the of cytochrome f in the in and and as and The is shown in and a at the in of the Rieske is as a to show the of its with the other The of the is the in one work or the in and the is or the in of cofactors and of the The of electron cofactors in the cytochrome b6f complex is with the which to for the of oxidized in 2004; et al., 2004). The plastoquinol is bound at the its oxidation and the electron from the is transferred to the Rieske center from it is transferred to the of cytochrome f and to plastocyanin or cytochrome The of the Rieske protein from a to the the center is oxidized electron from to a to cytochrome f the center is reduced of cytochrome The of the Rieske protein is to the for each electron and is by to the in the cytochrome complex of the of the Rieske protein have been in the form et al., 2004). The cytochrome b6f are as to have a view of both but are experiments that et al., and The other electron from the at the is transferred the two b-hemes to a at the from the and is from of the structure that the is in the of electron from the to the is that this the electron with et al., 2003). that is structural basis for electron the is to the to the of the electrons of the and to is the two The function of the and in the complex is and the structure suggest are to in to to from the and are in the with other for is one cofactors are to other in redox reactions the cytochrome b6f complex is the new for as electron cofactors in have been as to the of the one in the cytochrome b6f complex is to for that but a of the is on this The of the new on the other hand, suggest in redox with the as more with its and to the is that the new an for to in electron but are in of electron that without of the cytochrome b6f complex in et al., 2004). The of the new the of a in redox et al., 2004). The complexes of which a electron pathway are to the cytochrome b6f complexes of and the of and The of the function of the the for the of unique to with the cytochrome of these are is an in the resolution of this The of the new a and a with to the of the complex, of which is the molecular identity of the responsible for the of the cytochrome et al., the of in the of the complex in and the in the cytochrome pathway the and one of the as et al., and a to The cytochrome b6f complex been as the to the complexes in and but with the of its structure, it as the more and will a of with to electron and and a of from the of PSI or to ferredoxin is the in the In plastocyanin is the donor of the and reduced ferredoxin the PSI in to with the of an cytochrome an and an or et al., et al., et al., The of a cytochrome in the to the that the on the donor to et al., but the new cytochrome a in that is from the cytochrome of which plastocyanin as the only donor to PSI in The product of reduced is a key reductant in the it NADP+ for biosynthetic and for redox it directly provide electrons for or and as it electrons to the cytochrome b6f complex in a electron pathway PSI for the generation of a and and et al., of PSI a years with the of a structure of the et al., The structure of the as and with of the the two and The of the in the and the of one of as a to an to in the of cofactors rather than as bound from the or from the other reaction the cofactors in the electron are in bound by a of the and is the and and are bound to on the of the with PSI on the with and and plastocyanin and cytochrome with PSI on the with and of the in a and function in the The a are in two on the and to of The are in with a which is with a function in light from to or in of The PSI reaction is by of the primary from the The electron is transferred to the primary of in the electron of two and and from it PSI to In with other known reaction the of that are to is and the to is of is that the two of the electron are both and the are a of et al., Nelson and solved the structure of a supercomplex from (Ben-Shem et al., 2003). the resolution is it is for the of the LHCI PSI and for a structural basis for a arrangement of PSI a arrangement in The structure provides with a view of LHCI structure and and reaction are The use a structural the and to generate the evolution of PSI interactions that are with its in to and environmental (Ben-Shem et al., 2004). a for the in the more reaction of LHCI with The complex is the from the The are shown as with the as a is shown as a and as a The are shown as The of PSI are with the that to the PSI are of and is shown in and in et al., for a of PSI The are of to generate the from by and Nelson (Ben-Shem et al., 2003). The resolution at is to and the of is on to et al., 2003). the of in with the by et al., the and that are in two and on known is in sequence to and is to have by the on the basis of the known of the to the of the complex LHCI makes a with PSI through protein–protein on the other and PSI is to the the from an which is known to for interactions with the electron or cytochrome et al., the in the view shown in this is as a that an on that of the this new a that donor of cytochrome in major of this recent structure from the of which provides a structural basis for interactions and the LHCI and The with each other through the and of the and the as from rather than through the The in LHCI for are because of the of at the of a and is a of at the LHCI and which that are to each are the are and to of new evolution are on the of the LHCI or PSI and occupy the experiments in the of the and for and of with PSI et al., et that the form the for from the to PSI and suggest that the of the that PSI in to from the or from (Ben-Shem et al., 2003). for the b6f complex, the of the electron cofactors in the and are the light-harvesting in the of the are in the an of most of the directly to are new to PSI that interactions (i.e., LHCI and and the that this a to the reaction center with a in the of at light of the is its as a The structure that the from to is a of the of the that is required for to PSI in II of The of The from to the for and An of the is that the is on the an of with of is to the This is because it a for LHCI composition is in to the or removed from the on for light-harvesting and this is by the weak interactions In it that is from PSI with of and of at the of et al., The for this is that reduced light is to serve a function in the the electron in PSI and fully a the two of and reduced from in that the is with the structural of (Ben-Shem et al., 2003). of PSI the of both the and with to one the of PSI at the electron from water to and electron the of is that the of will the of and structural that of light the In this it is that from the of the structures of the complexes represent “a” structure rather than “the” structure, and it is the of metabolism that makes and the photosynthetic The structures an of in the photosynthetic The of the and but Ferreira et that the and the photosynthesis reaction center from is only for The of photosynthetic to understanding metabolism is The of in these structures provides a for and This is for the and the structural the structures of other of the On the other hand, are differences with to the of the and this is the of the PSI structure from and are differences in in interactions with or with other electron and in the in the structural one on or environmental and in that the structures are a for new as to the of from the mechanistic of the structures suggest new as from the of a new in cytochrome b6f and the of and of biophysicists and to molecular and as the of the most on The are to and for in photosynthesis for this to and for on the and to and Nelson for the to from the the of and the of for work on is by the