Characterization of Arabidopsis thaliana SufE2 and SufE3

Abstract

In this study we characterize two novel chloroplast SufE-like proteins from Arabidopsis thaliana. Other SufE-like proteins, including the previously described A. thaliana CpSufE, participate in sulfur mobilization for Fe-S biosynthesis through activation of cysteine desulfurization by NifS-like proteins. In addition to CpSufE, the Arabidopsis genome encodes two other proteins with SufE domains, SufE2 and SufE3. SufE2 has plastid targeting information. Purified recombinant SufE2 could activate the cysteine desulfurase activity of CpNifS 40-fold. SufE2 expression was flower-specific and high in pollen; we therefore hypothesize that SufE2 has a specific function in pollen Fe-S cluster biosynthesis. SufE3, also a plastid targeted protein, was expressed at low levels in all major plant organs. The mature SufE3 contains two domains, one SufE-like and one with similarity to the bacterial quinolinate synthase, NadA. Indeed SufE3 displayed both SufE activity (stimulating CpNifS cysteine desulfurase activity 70-fold) and quinolinate synthase activity. The full-length protein was shown to carry a highly oxygen-sensitive (4Fe-4S) cluster at its NadA domain, which could be reconstituted by its own SufE domain in the presence of CpNifS, cysteine and ferrous iron. Knock-out of SufE3 in Arabidopsis is embryolethal. We conclude that SufE3 is the NadA enzyme of A. thaliana, involved in a critical step during NAD biosynthesis. In this study we characterize two novel chloroplast SufE-like proteins from Arabidopsis thaliana. Other SufE-like proteins, including the previously described A. thaliana CpSufE, participate in sulfur mobilization for Fe-S biosynthesis through activation of cysteine desulfurization by NifS-like proteins. In addition to CpSufE, the Arabidopsis genome encodes two other proteins with SufE domains, SufE2 and SufE3. SufE2 has plastid targeting information. Purified recombinant SufE2 could activate the cysteine desulfurase activity of CpNifS 40-fold. SufE2 expression was flower-specific and high in pollen; we therefore hypothesize that SufE2 has a specific function in pollen Fe-S cluster biosynthesis. SufE3, also a plastid targeted protein, was expressed at low levels in all major plant organs. The mature SufE3 contains two domains, one SufE-like and one with similarity to the bacterial quinolinate synthase, NadA. Indeed SufE3 displayed both SufE activity (stimulating CpNifS cysteine desulfurase activity 70-fold) and quinolinate synthase activity. The full-length protein was shown to carry a highly oxygen-sensitive (4Fe-4S) cluster at its NadA domain, which could be reconstituted by its own SufE domain in the presence of CpNifS, cysteine and ferrous iron. Knock-out of SufE3 in Arabidopsis is embryolethal. We conclude that SufE3 is the NadA enzyme of A. thaliana, involved in a critical step during NAD biosynthesis. Characterization of Arabidopsis thaliana SufE2 and SufE3. Functions in chloroplast iron-sulfur cluster assembly and NAD synthesis.Journal of Biological ChemistryVol. 284Issue 39PreviewVOLUME 282 (2007) PAGES 18254–18264 Full-Text PDF Open Access Fe-S clusters are one of the most common and functionally diverse types of prosthetic groups that can be found in all living organisms (1Beinert H. Holm R.H. Munck E. Science. 1997; 277: 653-659Crossref PubMed Scopus (1531) Google Scholar). Fe-S proteins are involved in processes such as electron transport, redox and non-redox catalysis, sensing of environmental stimuli, DNA repair, and regulation of gene expression (2Johnson D.C. Dean D.R. Smith A.D. Johnson M.K. Annu. Rev. Biochem. 2005; 74: 247-281Crossref PubMed Scopus (1110) Google Scholar, 3Lill R. Muhlenhoff U. Trends Biochem. Sci. 2005; 30: 133-141Abstract Full Text Full Text PDF PubMed Scopus (299) Google Scholar, 4Balk J. Lobreaux S. Trends Plant Sci. 2005; 10: 324-331Abstract Full Text Full Text PDF PubMed Scopus (192) Google Scholar). Although Fe-S clusters are derived from two of the most abundant elements on earth, they are not formed spontaneously in cells but arise by controlled biosynthesis requiring an intricate interplay of numerous proteins (5Frazzon J. Dean D.R. Curr. Opin. Chem. Biol. 2003; 7: 166-173Crossref PubMed Scopus (189) Google Scholar, 6Lill R. Kispal G. Trends Biochem. Sci. 2000; 25: 352-356Abstract Full Text Full Text PDF PubMed Scopus (319) Google Scholar). In plants, Fe-S proteins are particularly important for photosynthesis. In the chloroplast thylakoid membrane, Fe-S cluster proteins function in photosynthetic electron transport leading to the production of ATP and NADPH (7Raven J. Evans M.C.W. Korb R.E. Photosynth. Res. 1999; 60: 111-149Crossref Google Scholar). These molecules provide the energy and reducing power for photosynthetic carbon reduction and as as for sulfur and reduction and which Fe-S prosthetic groups as for and a H. PubMed Scopus Google Scholar). Fe-S cluster can be sulfur assembly of and sulfur a and cluster (2Johnson D.C. Dean D.R. Smith A.D. Johnson M.K. Annu. Rev. Biochem. 2005; 74: 247-281Crossref PubMed Scopus (1110) Google Scholar, 3Lill R. Muhlenhoff U. Trends Biochem. Sci. 2005; 30: 133-141Abstract Full Text Full Text PDF PubMed Scopus (299) Google Scholar). sulfur is from cysteine by the of a a cysteine desulfurase enzyme Dean D.R. J. Biol. Chem. Full Text Full Text PDF PubMed Scopus Google Scholar, Dean D.R. J. Biol. Chem. Full Text PDF PubMed Google Scholar). The sulfur is with of which the is on a a Fe-S cluster is to Fe-S proteins Smith A.D. J. Dean D.R. Johnson M.K. Biochem. PubMed Scopus Google Scholar, G. R. J. Biol. Chem. 7: PubMed Scopus Google Scholar, Johnson M.K. Dean D.R. Sci. U. S. A. 2000; PubMed Scopus Google Scholar, S. J. Biol. Chem. Full Text Full Text PDF PubMed Scopus Google Scholar, S. J. Biol. Chem. 2003; Full Text Full Text PDF PubMed Scopus Google Scholar). In Fe-S assembly described which are Fe-S quinolinate high and of Dean D.R. J. Biol. Chem. Full Text Full Text PDF PubMed Scopus Google Scholar, U. J. Biol. Chem. 277: Full Text Full Text PDF PubMed Scopus Google Scholar, D.C. Dean D.R. Biochem. 2005; PubMed Scopus Google Scholar, 2005; PubMed Scopus Google contains a cysteine the has a function in in the is to be involved in the Fe-S cluster biosynthesis Dean D.R. J. Biol. Chem. Full Text Full Text PDF PubMed Scopus Google Scholar). The to an for the assembly of Fe-S clusters and U. J. Biol. Chem. 277: Full Text Full Text PDF PubMed Scopus Google Scholar, J. 2003; PubMed Scopus Google Scholar). In plants, own Fe-S cluster S. Plant PubMed Scopus Google Scholar, A. H. Sci. U. S. A. PubMed Google Scholar). is that the redox in the chloroplast are particularly for the and of Fe-S cluster proteins, Fe-S clusters are to and (1Beinert H. Holm R.H. Munck E. Science. 1997; 277: 653-659Crossref PubMed Scopus (1531) Google Scholar). for Fe-S cluster to is therefore not on the plastid Fe-S biosynthesis to are most to the bacterial cluster to function J. Lobreaux S. Trends Plant Sci. 2005; 10: 324-331Abstract Full Text Full Text PDF PubMed Scopus (192) Google Scholar). Characterization of the Fe-S with the and of the cysteine desulfurase CpNifS, also as S. Lobreaux S. Biochem. J. PubMed Scopus Google Scholar, S. H. Plant PubMed Scopus Google Scholar). The cysteine desulfurase activity of CpNifS is for Fe-S cluster in the chloroplast protein in H. 2005; PubMed Scopus Google Scholar). Other of the Fe-S cluster are the proteins S. Lobreaux S. Biochem. J. 2003; PubMed Scopus Google Scholar, A. G. Lobreaux S. Plant J. PubMed Scopus Google Scholar, S. Plant PubMed Scopus Google and H. Plant 2005; PubMed Scopus Google Scholar, Biochem. Res. PubMed Scopus Google Scholar). In other in Fe-S in PubMed Scopus Google Scholar, S. J. Biol. Chem. 2005; Full Text Full Text PDF PubMed Scopus Google Scholar, Sci. U. S. A. PubMed Scopus Google Scholar). The is an that be involved in the Fe-S cluster from the protein to the protein S. J. Biol. Chem. 2005; Full Text Full Text PDF PubMed Scopus Google Scholar, Sci. U. S. A. PubMed Scopus Google Scholar). Arabidopsis CpNifS is a cysteine desulfurase and has a low of desulfurase activity in S. H. Plant PubMed Scopus Google to its bacterial The cysteine desulfurase activity of was in the presence of bacterial SufE cysteine desulfurase activity S. J. Biol. Chem. 2003; Full Text Full Text PDF PubMed Scopus Google Scholar, G. J. Biol. Chem. 2003; Full Text Full Text PDF PubMed Scopus Google Scholar). The cysteine of bacterial SufE is critical for the of cysteine desulfurase activity of S. J. Biol. Chem. 2003; Full Text Full Text PDF PubMed Scopus Google Scholar, G. J. Biol. Chem. 2003; Full Text Full Text PDF PubMed Scopus Google Scholar). In a protein was shown to to to a S. J. Biol. Chem. 2003; Full Text Full Text PDF PubMed Scopus Google Scholar). of SufE are found in a of including and of proteins a cysteine that is to function as a during sulfur cysteine desulfurization by proteins, the cysteine of SufE the sulfur from the and an S. J. Biol. Chem. 2003; Full Text Full Text PDF PubMed Scopus Google Scholar, G. J. Biol. Chem. 2003; Full Text Full Text PDF PubMed Scopus Google Scholar, S. E. 2003; Scopus Google Scholar). from the sulfur is to an protein for of a such as a Fe-S a SufE-like protein was in A. thaliana that can the cysteine desulfurase activity of CpNifS J. 25: PubMed Scopus Google Scholar, H. J. Biol. Chem. Full Text Full Text PDF PubMed Scopus Google Scholar). protein, which was J. 25: PubMed Scopus Google Scholar, H. J. Biol. Chem. Full Text Full Text PDF PubMed Scopus Google be to as from Arabidopsis an SufE protein that can the in E. J. 25: PubMed Scopus Google Scholar). was to both J. 25: PubMed Scopus Google Scholar, H. J. Biol. Chem. Full Text Full Text PDF PubMed Scopus Google and J. 25: PubMed Scopus Google Scholar). to and a with CpNifS, its cysteine desulfurase activity and the of CpNifS cysteine H. J. Biol. Chem. Full Text Full Text PDF PubMed Scopus Google Scholar). In that the of CpNifS to clusters in was in the presence of H. J. Biol. Chem. Full Text Full Text PDF PubMed Scopus Google Scholar). The cysteine of Arabidopsis is for this and is the for in with E. SufE H. J. Biol. Chem. Full Text Full Text PDF PubMed Scopus Google Scholar). The of of Arabidopsis that is an protein J. 25: PubMed Scopus Google Scholar, H. J. Biol. Chem. Full Text Full Text PDF PubMed Scopus Google Scholar). that to Arabidopsis contains two that proteins with SufE-like In this we characterize two proteins, which we SufE2 and SufE3. SufE2 of a and to function in SufE3 is a protein of an SufE domain to a domain with to bacterial NadA. E. NadA is involved in the biosynthesis of a in numerous redox In all living NAD from Rev. PubMed Google Scholar, Trends Biochem. Sci. Full Text Full Text PDF PubMed Scopus Google Scholar). In most to is the of in E. is from and as the of the of two by the and quinolinate synthase by the NadA gene S. J. Biol. Chem. Full Text PDF PubMed Google Scholar, J. PubMed Google Scholar). that E. NadA is an Fe-S enzyme with a cluster for activity S. 2005; PubMed Scopus Google Scholar, J. Chem. 2005; PubMed Scopus Google Scholar). in E. in Arabidopsis is in the A. Plant PubMed Scopus Google Scholar). the of this the Arabidopsis quinolinate synthase was shown to be to and to an E. in the NadA gene A. Plant PubMed Scopus Google but the activity was not in we that this protein, which we SufE3, has both SufE and the of which on a highly oxygen-sensitive cluster in the NadA The SufE domain on the protein can this cluster through with Plant thaliana was for all in at with a and are in for SufE2 and SufE3 from the Arabidopsis Biological and The A. thaliana SufE2 and SufE3 by as a SufE2 expression in E. the mature of SufE2 was and The was with and and for expression as The mature of SufE3 was and The was with and and to for expression as The was for of the E. the cysteine to in the SufE domain of SufE3, recombinant was In the two with and and and was as a from the of and with and The was with and and the expression to also for of the E. the expression in E. the SufE domain of SufE3 was the and The was with and and expression protein the full-length protein of SufE2 was with and and SufE3 was the and The of SufE2 and SufE3 with and and the S. J. J. J. Biol. Chem. 277: Full Text Full Text PDF PubMed Scopus Google of Open in a was from and by the of was on a to a membrane, and with SufE2 SufE3 as described S. H. Plant PubMed Scopus Google Scholar). The was to R. R.E. Smith in and and the was with a as a one of from and was to with an and in a of this was for as and to a from and in as an The in a of and at The by in a and was for similarity the by the for was the of of the of SufE2 and SufE3 the S. J. J. J. Biol. Chem. 277: Full Text Full Text PDF PubMed Scopus Google the of the to with a These expressed in Arabidopsis as described Plant 2005; PubMed Scopus Google Scholar). proteins a was at was at of E. that the mature of SufE3 in E. which has a in the NadA gene quinolinate synthase S. E. J. Biol. Chem. 2005; Full Text Full Text PDF PubMed Scopus Google Scholar). on with on with with was from was a as described by S. H. Plant PubMed Scopus Google Scholar). Characterization of Knock-out for SufE3 was by the H. J. R. A. E. H. H. E. R. E. A. Science. 2003; PubMed Scopus Google and from the Arabidopsis Biological the of the a DNA was by specific for the and for the SufE3 the of the was the of with to the that the to by the presence of a a in with a was to the for in SufE3 in a in the of on that also in a that all a in SufE3. These the presence of a in this of the SufE of SufE2 and SufE3, the for the SufE domain of SufE2 of SufE3 to an E. of was with of at to an of and expression was by addition of by for at The SufE2 and SufE3 by the by H. J. Biol. Chem. Full Text Full Text PDF PubMed Scopus Google to this SufE2 by a with The SufE2 protein, was with an of to the The was with of and the SufE2 protein was with in The proteins and at E. NadA protein was as described S. 2005; PubMed Scopus Google Scholar). CpNifS and the as described S. H. Plant PubMed Scopus Google Scholar, H. J. Biol. Chem. Full Text Full Text PDF PubMed Scopus Google Scholar). of SufE3 mature protein for quinolinate synthase activity was as the of full-length SufE3, a of E. with was of SufE3 expression by addition of at was for at the in a in and and The was and by for the was a with A. of SufE3 was with by and at of SufE3 was by an to to a protein The was in and at a of of protein to the of was the was by a with of in the presence of the protein was by through a with was in with CpNifS and a of in the presence of of the Fe-S cluster was by during was and the was for The protein was by on a and the by on at desulfurase activity was as described by H. J. Biol. Chem. Full Text Full Text PDF PubMed Scopus Google Scholar). NadA activity was a at and the of was by The in a of of SufE3 protein a of the at the was by the addition of the of at and to of to the proteins by at for of the was the The was and by a a The was with at a of was by its at and was with a of of the was by a from to in at and of the was to a from of and was by the of Biochem. PubMed Scopus Google Scholar). was reducing with of the protein PubMed Scopus Google and by the of H. Biochem. PubMed Scopus Google Scholar). NadA was with a the A. thaliana SufE3 in with and protein expression was by addition of of SufE3 was as described of protein from of in on a in an that from to and a in are to at on a with an of the and with the the of a SufE and a SufE-like was by a the Arabidopsis genome and J. 25: PubMed Scopus Google Scholar, H. J. Biol. Chem. Full Text Full Text PDF PubMed Scopus Google Scholar). protein was shown to be targeted to the chloroplast and to CpNifS desulfurase activity H. J. Biol. Chem. Full Text Full Text PDF PubMed Scopus Google Scholar). In the we to as for two and J. 25: PubMed Scopus Google found that also to in this study we characterize two other SufE-like proteins in E. SufE as a we found two SufE-like proteins in the Arabidopsis and and The of Arabidopsis SufE2 contains a the was from The Arabidopsis of the the presence of a in the The is to a full-length protein of including a chloroplast targeting of The mature is with a of and an of SufE2 has similarity to previously SufE proteins and The of SufE3 is to a full-length protein of including a chloroplast targeting The mature is with a of and an of In SufE3, the of the mature protein a SufE-like and SufE domain is in with a of and an of The of SufE3 similarity to the E. NadA protein and which encodes a and is involved in NAD biosynthesis. that the domain contains which in E. for an Fe-S was to the similarity of the SufE domain of Arabidopsis proteins and E. SufE SufE in the mature protein including a highly cysteine that was shown to be critical for function in bacterial SufE and also in Arabidopsis H. J. Biol. Chem. Full Text Full Text PDF PubMed Scopus Google Scholar). In the SufE domain to the of the mature protein The domain of similarity to bacterial H. J. Biol. Chem. Full Text Full Text PDF PubMed Scopus Google Scholar). and of SufE2 and that SufE2 and SufE3 are targeted to the H. S. G. J. Biol. 2000; PubMed Scopus Google Scholar). the of Arabidopsis proteins we the and expressed by was as a Arabidopsis and the in cells was of to the as The for both SufE2 and SufE3 to the as by the of and from and the expression of SufE2 and SufE3 we the in plant that SufE2 expression was high in was expression in and SufE2 levels also by for from and pollen low was for and with These that SufE2 expression is and are in with In the SufE3 a of for all major plant that SufE3 is The SufE of SufE2 and SufE3 CpNifS was shown to the cysteine desulfurase activity of CpNifS, was that its SufE2 and SufE3 a activity. the SufE to a and a for by The in cysteine desulfurase activity The SufE of SufE2 and SufE3 and as on and the SufE of SufE2 and SufE3 not cysteine desulfurase activity by CpNifS cysteine desulfurase activity was in the of SufE-like proteins. in the presence of of the SufE2 domain, cysteine desulfurization CpNifS cysteine desulfurase activity in the presence of the SufE domain of SufE3 in a The of CpNifS activity by the SufE was the SufE domain to CpNifS was SufE in SufE3 for of an E. SufE3 an protein and encodes a the full-length SufE3 was and expressed in an E. in to the of the cysteine in its SufE domain for this was to and the was also to E. We the of with its own E. NadA with an In the presence of a of all of the E. to on in the of the E. SufE3 the E. NadA to to E. that SufE3 is an Arabidopsis protein with activity. The that protein its to its to the as SufE3 that the in the SufE domain of SufE3 is for activity. The expressed NadA domain of SufE3 could not the E. this expressed NadA domain not in the that the SufE domain is for expression in this the expression of the full-length SufE3 the cysteine in E. not bacterial is for SufE3 for the function of the SufE3 gene in we the of a with a in this The in this is in the of SufE3. SufE3 on the We and the in a SufE3 to that of the In of SufE3 one of was in the of the We could not that for the SufE3 in the and that the to of SufE3 and that SufE3 function is and Characterization of the SufE3 Arabidopsis SufE3, with a at the was by a of the by an of on was to the of SufE3. SufE3 protein in a major to a but a of could also be the two SufE3, of SufE3 could be from of in a as from not The protein was the presence of an Fe-S the of and was with to the protein and that the protein in an was in the that the low cluster was to the of the protein and the of the as for the E. SufE3 was a such a protein to was as by in The protein was in and its shown in is for a cluster with one in the at to SufE3 and the with a of the not the presence of a Fe-S cluster and to its and protein was both and and was for its and for a with a the and to of and with and the of a SufE3 expression in and at and and both the are by a with (2Johnson D.C. Dean D.R. Smith A.D. Johnson M.K. Annu. Rev. Biochem. 2005; 74: 247-281Crossref PubMed Scopus (1110) Google and J. Lobreaux S. Trends Plant Sci. 2005; 10: 324-331Abstract Full Text Full Text PDF PubMed Scopus (192) Google this for of iron. These are with a for E. NadA S. 2005; PubMed Scopus Google Scholar, J. Chem. 2005; PubMed Scopus Google Scholar). The at an of with and which is in the at this is to a a and the be The of is to be and is to of SufE3 protein and expression in and a at and as are the with and with as The at the to the to of SufE3 with from this the presence of at and to and for of iron. of this with to a of the with of the this we a which was as the of two (1Beinert H. Holm R.H. Munck E. Science. 1997; 277: 653-659Crossref PubMed Scopus (1531) Google was by at and the one (2Johnson D.C. Dean D.R. Smith A.D. Johnson M.K. Annu. Rev. Biochem. 2005; 74: 247-281Crossref PubMed Scopus (1110) Google by at and and power of the two are and in with not These two a for (4Fe-4S) The to of iron. of the to for the The SufE a for Fe-S in the NadA of is a the SufE and NadA of SufE3, we the of SufE3 to an Fe-S cluster in its NadA domain in the presence of the chloroplast cysteine desulfurase CpNifS, cysteine and and in the of SufE3 was with a of CpNifS, in the presence of cysteine and a of ferrous and the by the with a in the at was in this the protein was with for to and and on a The protein was in and displayed a to that of the not and the presence of and in this reconstituted the was with the SufE3 protein the NadA domain with which the cysteine of the cysteine desulfurase has to a in at was and was that Fe-S was These and the E. that the Fe-S cluster is in the NadA domain of SufE3, the cysteine desulfurase activity of CpNifS is to provide the sulfur for this and the SufE domain of SufE3, the is for Fe-S cluster on the NadA domain of the The Fe-S of SufE3 for of both and reconstituted SufE3 proteins to of was a but of quinolinate synthase of at and was from by the of the protein as the electron in the presence of a of at and the enzyme the of with a specific activity of in an that was In E. NadA a specific activity in the of J. Chem. 2005; PubMed Scopus Google Scholar). and that the is that the Fe-S cluster of SufE3. production of was a was as an enzyme the SufE domain of SufE3 the NadA was not SufE3 was for the of production to of the for the not shown in the displayed a with to in which is a of and a of for the E. NadA a of and a of and In this we characterize two novel SufE-like proteins from which we SufE2 and SufE3. SufE-like Arabidopsis proteins the cysteine desulfurase activity of was found to be expressed in all with a expression in with H. J. Biol. Chem. Full Text Full Text PDF PubMed Scopus Google Scholar). The of expression in is for proteins involved in photosynthesis. SufE2 expression is in all for and particularly CpNifS is expressed in expression in pollen is low The that SufE2 a specific but function in Fe-S assembly in the of in the of other is the of pollen and to Fe-S proteins with a function in this not of as are to a function in the and of to be important in pollen The and of The Scholar). The SufE3 was but in to the abundant the SufE3 was mature SufE3 of both a SufE-like domain and a domain to the bacterial quinolinate synthase NadA. SufE3 both a SufE activity and a quinolinate synthase activity. The provide the that SufE3 is the A. thaliana quinolinate its with NadA from E. is SufE3 contains a highly oxygen-sensitive by and to that in NadA from E. S. 2005; PubMed Scopus Google Scholar, J. Chem. 2005; PubMed Scopus Google SufE3 a quinolinate synthase activity on the presence of the SufE3 a E. this the SufE domain of SufE3. The cluster of SufE3 can be reconstituted by its own SufE domain in the presence of CpNifS, cysteine and ferrous iron. Knock-out of SufE3 was We conclude that SufE3 is the quinolinate synthase enzyme of involved in a critical step during NAD biosynthesis. of sulfur mobilization by CpNifS, be that of can one the of and SufE3 that they SufE3 has quinolinate synthase activity. SufE2 of function in is expressed in be for the of the in the presence of SufE3, which has a expression as The SufE3 expression be low to for of to both and J. 25: PubMed Scopus Google SufE3, as as is from is in the we that the most important for the of SufE3 of a is that the SufE activity of SufE3 is to Fe-S cluster in its own quinolinate synthase is to that the of a SufE domain and a NadA domain in a protein in SufE3 has a We that in A. thaliana the protein contains a SufE domain to sulfur from CpNifS to the NadA domain, for the assembly of the through an sulfur from the cysteine to the of the NadA the expression of the SufE3 in which cysteine was to a could not an E. is to that also in E. NadA not to the Fe-S cluster In E. is with a SufE domain to sulfur but a specific cysteine desulfurase is S. E. J. Biol. Chem. 2005; Full Text Full Text PDF PubMed Scopus Google Scholar). is but be a of the of the NAD which a highly In the chloroplast this is SufE3 is highly In a chloroplast the levels are and the protein its activity to the SufE domain of SufE3 has a in the Fe-S cluster in the NadA domain of the protein, to protein the this protein its own SufE is its to with its in an The previously contains a domain at its J. 25: PubMed Scopus Google Scholar, H. J. Biol. Chem. Full Text Full Text PDF PubMed Scopus Google Scholar). was that proteins with 2005; PubMed Scopus Google proteins with that are by an in Photosynth. Res. 2005; Scopus Google Scholar). are the of cysteine in plants, be a to CpNifS cysteine desulfurase activity and of the cysteine We is that the domain of a in the regulation of cysteine desulfurase activity in to the for Fe-S cluster biosynthesis and a domain is not in SufE3, bacterial SufE proteins. In the expression of in cysteine can be as to the cysteine in to the for Fe-S proteins. In SufE2 not regulation of its presence in which is not a major of cysteine The SufE domain of SufE3 CpNifS cysteine desulfurase activity to a SufE2 and with NAD is to be at the the Fe-S of SufE3 is to be for SufE3 to to SufE3 therefore be through the of the Fe-S cluster in its NadA The but low expression levels that in the SufE3 is at levels and SufE3 to CpNifS not The of CpNifS for Fe-S cluster assembly in has both in H. 2005; PubMed Scopus Google and in S. Sci. U. S. A. PubMed Scopus Google Scholar). of CpNifS was shown to photosynthetic electron transport, and sulfur and carbon S. Sci. U. S. A. PubMed Scopus Google Scholar). The an of the cysteine desulfurase CpNifS in NAD We are to for the of the E. NadA We also for and for pollen with