Biosynthesis of Sulfur-Containing Small Biomolecules in Plants

1.

2.

3.

4.

5.

6.

7.

8.

9.

10.

11.

12.

13.

14.

15.

16.

17.

18.

19.

20.

21.

22.

Beinert, H. A tribute to sulfur. Eur. J. Biochem. 2000, 267, 657–664. [CrossRef] [PubMed]

Long, S.; Kahn, M.; Seefeldt, L.; Tsay, Y.; Kopriva, S. Nitrogen and sulfur. In Biochemistry and Molecular Biology

of Plants; Buchanan, B.B., Gruissem, W., Jones, R.L., Eds.; WILEY: Blackwell, NJ, USA, 2015; pp. 746–768.

Maruyama-Nakashita, A.; Ohkama-Ohtsu, N. Sulfur assimilation and glutathione metabolism in plants.

In Glutathione in Plant Growth, Development, and Stress Tolerance; Hossain, M.A., Ed.; Springer: New York, NY, USA,

2017; pp. 287–308.

Koprivova, A.; North, K.A.; Kopriva, S. Complex signaling network in regulation of adenosine

5’-phosphosulfate reductase by salt stress in Arabidopsis roots. Plant Physiol. 2008, 146, 1408–1420. [CrossRef]

[PubMed]

Hirai, M.Y.; Yano, M.; Goodenowe, D.B.; Kanaya, S.; Kimura, T.; Awazuhara, M.; Arita, M.; Fujiwara, T.;

Saito, K. Integration of transcriptomics and metabolomics for understanding of global responses to nutritional

stresses in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 2004, 101, 10205–10210. [CrossRef]

Maruyama-Nakashita, A.; Inoue, E.; Watanabe-Takahashi, A.; Yamaya, T.; Takahashi, H. Transcriptome

Profiling of Sulfur-Responsive Genes in Arabidopsis Reveals Global Effects of Sulfur Nutrition on Multiple

Metabolic Pathways. Plant Physiol. 2003, 132, 597–605. [CrossRef] [PubMed]

Takahashi, H.; Yamazaki, M.; Sasakura, N.; Watanabe, A.; Leustek, T.; Engler, J.A.; Engler, G.; Van Montagu, M.;

Saito, K. Regulation of sulfur assimilation in higher plants: A sulfate transporter induced in sulfate-starved

roots plays a central role in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 1997, 94, 11102–11107. [CrossRef]

[PubMed]

Takahashi, H.; Kopriva, S.; Giordano, M.; Saito, K.; Hell, R. Sulfur assimilation in photosynthetic organisms:

Molecular functions and regulations of transporters and assimilatory enzymes. Annu. Rev. Plant Biol. 2011,

62, 157–184. [CrossRef]

Maruyama-Nakashita, A. Metabolic changes sustain the plant life in low-sulfur environments. Curr. Opin.

Plant. Biol. 2017, 39, 144–151. [CrossRef]

Hell, R.; Wirtz, M. Molecular Biology, Biochemistry and Cellular Physiology of Cysteine Metabolism in

Arabidopsis thaliana. Arabidopsis Book. 2011, 9, e0154. [CrossRef]

Zagorchev, L.; Seal, C.E.; Kranner, I.; Odjakova, M. A central role for thiols in plant tolerance to abiotic stress.

Int J. Mol. Sci. 2013, 14, 7405–7432. [CrossRef]

Meyer, A.J.; Hell, R. Glutathione homeostasis and redox-regulation by sulfhydryl groups. Photosynth. Res.

2005, 86, 435–457. [CrossRef]

Noctor, G.; Mhamdi, A.; Chaouch, S.; Han, Y.; Neukermans, J.; Marquez-Garcia, B.; Queval, G.; Foyer, C.H.

Glutathione in plants: An integrated overview. Plant. Cell Environ. 2012, 35, 454–484. [CrossRef] [PubMed]

Nakai, Y.; Nakai, M.; Yano, T. Sulfur Modifications of the Wobble U34 in tRNAs and their Intracellular

Localization in Eukaryotic Cells. Biomolecules. 2017, 7, 17. [CrossRef] [PubMed]

Iciek, M.; Bilska-Wilkosz, A.; Górny, M. Sulfane sulfur—New findings on an old topic. Acta Biochim. Pol.

2019, 66, 533–544. [CrossRef]

Mueller, E.G. Trafficking in persulfides: Delivering sulfur in biosynthetic pathways. Nat. Chem. Biol. 2006, 2,

185–194. [CrossRef]

Subrahmanian, N.; Remacle, C.; Hamel, P.P. Plant mitochondrial Complex I composition and assembly:

A review. Biochim. Biophys. Acta 2016, 1857, 1001–1014. [CrossRef] [PubMed]

Müh, F.; Glöckner, C.; Hellmich, J.; Zouni, A. Light-induced quinone reduction in photosystem II.

Biochim. Biophys. Acta 2012, 1817, 44–65. [CrossRef]

Yang, H.; Liu, J.; Wen, X.; Lu, C. Molecular mechanism of photosystem I assembly in oxygenic organisms.

Biochim. Biophys. Acta 2015, 1847, 838–848. [CrossRef]

Przybyla-Toscano, J.; Roland, M.; Gaymard, F.; Couturier, J.; Rouhier, N. Roles and maturation of iron–sulfur

proteins in plastids. J. Biol. Inorg. Chem. 2018, 23, 545–566. [CrossRef]

Balk, J.; Schaedler, T.A. Iron cofactor assembly in plants. Annu Rev. Plant. Biol. 2014, 65, 125–153. [CrossRef]

Frazzon, A.P.; Ramirez, M.V.; Warek, U.; Balk, J.; Frazzon, J.; Dean, D.R.; Winkel, B.S. Functional analysis of

Arabidopsis genes involved in mitochondrial iron-sulfur cluster assembly. Plant. Mol. Biol. 2007, 64, 225–240.

[CrossRef]

Int. J. Mol. Sci. 2020, 21, 3470

23.

24.

25.

26.

27.

28.

29.

30.

31.

32.

33.

34.

35.

36.

37.

38.

39.

40.

41.

42.

10 of 13

Turowski, V.R.; Busi, M.V.; Gomez-Casati, D.F. Structural and functional studies of the mitochondrial

cysteinedesulfurase from Arabidopsis thaliana. Mol. Plant. 2012, 5, 1001–1010. [CrossRef]

Léon, S.; Touraine, B.; Briat, J.F.; Lobréaux, S. Mitochondrial localization of Arabidopsis thaliana Isu Fe-S

scaffold proteins. FEBS Lett. 2005, 579, 1930–1934. [CrossRef]

Uzarska, M.A.; Przybyla-Toscano, J.; Spantgar, F.; Zannini, F.; Lill, R.; Mühlenhoff, U.; Rouhier, N. Conserved

functions of Arabidopsis mitochondrial late-acting maturation factors in the trafficking of iron-sulfur clusters.

Biochim. Biophys. Acta Mol. Cell Res. 2018, 1865, 1250–1259. [CrossRef] [PubMed]

Xu, X.M.; Lin, H.; Latijnhouwers, M.; Møller, S.G. Dual localized AtHscB involved in iron sulfur protein

biogenesis in Arabidopsis. PLoS ONE 2009, 4, e7662. [CrossRef] [PubMed]

Léon, S.; Touraine, B.; Ribot, C.; Briat, J.F.; Lobréaux, S. Iron-sulphur cluster assembly in plants: Distinct NFU

proteins in mitochondria and plastids from Arabidopsis thaliana. Biochem J. 2003, 371, 823–830. [CrossRef]

[PubMed]

Zannini, F.; Roret, T.; Przybyla-Toscano, J.; Dhalleine, T.; Rouhier, N.; Couturier, J. Mitochondrial Arabidopsis

thaliana TRXo Isoforms Bind an Iron-Sulfur Cluster and Reduce NFU Proteins In Vitro. Antioxidants (Basel)

2018, 7, 142. [CrossRef]

Bych, K.; Kerscher, S.; Netz, D.J.; Pierik, A.J.; Zwicker, K.; Huynen, M.A.; Lill, R.; Brandt, U.; Balk, J.

The iron-sulphur protein Ind1 is required for effective complex I assembly. EMBO J. 2008, 27, 1736–1746.

[CrossRef]

Moseler, A.; Aller, I.; Wagner, S.; Nietzel, T.; Przybyla-Toscano, J.; Mühlenhoff, U.; Lill, R.; Berndt, C.;

Rouhier, N.; Schwarzländer, M.; et al. The mitochondrial monothiol glutaredoxin S15 is essential for

iron-sulfur protein maturation in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 2015, 112, 13735–13740.

[CrossRef]

Takahashi, Y.; Tokumoto, U. A third bacterial system for the assembly of iron-sulfur clusters with homologs

in archaea and plastids. J. Biol. Chem. 2002, 277, 28380–28383. [CrossRef]

Chahal, H.K.; Dai, Y.; Saini, A.; Ayala-Castro, C.; Outten, F.W. The SufBCD Fe-S scaffold complex interacts

with SufA for Fe-S cluster transfer. Biochem. 2009, 48, 10644–10653. [CrossRef]

Hu, X.; Kato, Y.; Sumida, A.; Tanaka, A.; Tanaka, R. The SUFBC2 D complex is required for the biogenesis of

all major classes of plastid Fe-S proteins. Plant. J. 2017, 90, 235–248. [CrossRef]

Ye, H.; Abdel-Ghany, S.E.; Anderson, T.D.; Pilon-Smits, E.A.; Pilon, M. CpSufE activates the cysteine

desulfurase CpNifS for chloroplastic Fe-S cluster formation. J. Biol. Chem. 2006, 281, 8958–8969. [CrossRef]

[PubMed]

Xu, X.M.; Møller, S.G. AtSufE is an essential activator of plastidic and mitochondrial desulfurases in

Arabidopsis. EMBO J. 2006, 25, 900–909. [CrossRef] [PubMed]

Narayana Murthy, U.M.; Ollagnier-de-Choudens, S.; Sanakis, Y.; Abdel-Ghany, S.E.; Rousset, C.; Ye, H.;

Fontecave, M.; Pilon-Smits, E.A.; Pilon, M. Characterization of Arabidopsis thaliana SufE2 and SufE3: Functions

in chloroplast iron-sulfur cluster assembly and NAD synthesis. J. Biol. Chem. 2007, 282, 18254–18264.

Chahal, H.K.; Outten, F.W. Separate FeS scaffold and carrier functions for SufB2 C2 and SufA during in vitro

maturation of [2Fe2S] Fdx. J. Inorg Biochem. 2012, 116, 126–134. [CrossRef]

Abdel-Ghany, S.E.; Ye, H.; Garifullina, G.F.; Zhang, L.; Pilon-Smits, E.A.; Pilon, M. Iron-sulfur cluster

biogenesis in chloroplasts. Involvement of the scaffold protein CpIscA. Plant. Physiol. 2005, 138, 161–172.

[CrossRef]

Yabe, T.; Nakai, M. Arabidopsis AtIscA-I is affected by deficiency of Fe-S cluster biosynthetic scaffold AtCnfU-V.

Biochem. Biophys. Res. Commun. 2006, 340, 1047–1052. [CrossRef]

Py, B.; Gerez, C.; Angelini, S.; Planel, R.; Vinella, D.; Loiseau, L.; Talla, E.; Brochier-Armanet, C.; Garcia

Serres, R.; Latour, J.M.; et al. Molecular organization, biochemical function, cellular role and evolution of

NfuA, an atypical Fe-S carrier. Mol. Microbiol. 2012, 86, 155–171. [CrossRef]

Gao, H.; Subramanian, S.; Couturier, J.; Naik, S.G.; Kim, S.K.; Leustek, T.; Knaff, D.B.; Wu, H.C.; Vignols, F.;

Huynh, B.H.; et al. Arabidopsis thaliana Nfu2 accommodates [2Fe-2S] or [4Fe-4S] clusters and is competent for

in vitro maturation of chloroplast [2Fe-2S] and [4Fe-4S] cluster-containing proteins. Biochemistry 2013, 52,

6633–6645. [CrossRef]

Nath, K.; O’Donnell, J.P.; Lu, Y. Chloroplastic iron-sulfur scaffold protein NFU3 is essential to overall plant

fitness. Plant. Signal. Behav. 2017, 12, e1282023. [CrossRef]

Int. J. Mol. Sci. 2020, 21, 3470

43.

44.

45.

46.

47.

48.

49.

50.

51.

52.

53.

54.

55.

56.

57.

58.

59.

60.

61.

62.

11 of 13

Schwenkert, S.; Netz, D.J.; Frazzon, J.; Pierik, A.J.; Bill, E.; Gross, J.; Lill, R.; Meurer, J. Chloroplast HCF101 is

a scaffold protein for [4Fe-4S] cluster assembly. Biochem. J. 2009, 425, 207–214. [CrossRef] [PubMed]

Waller, J.C.; Ellens, K.W.; Alvarez, S.; Loizeau, K.; Ravanel, S.; Hanson, A.D. Mitochondrial and plastidial

COG0354 proteins have folate-dependent functions in iron-sulphur cluster metabolism. J. Exp. Bot. 2012, 63,

403–411. [CrossRef] [PubMed]

Bandyopadhyay, S.; Gama, F.; Molina-Navarro, M.M.; Gualberto, J.M.; Claxton, R.; Naik, S.G.; Huynh, B.H.;

Herrero, E.; Jacquot, J.P.; Johnson, M.K.; et al. Chloroplast monothiol glutaredoxins as scaffold proteins for

the assembly and delivery of [2Fe-2S] clusters. EMBO J. 2008, 27, 1122–1133. [CrossRef] [PubMed]

Biederbick, A.; Stehling, O.; Rösser, R.; Niggemeyer, B.; Nakai, Y.; Elsässer, H.P.; Lill, R. Role of human

mitochondrial Nfs1 in cytosolic iron-sulfur protein biogenesis and iron regulation. Mol. Cell Biol. 2006, 26,

5675–5687. [CrossRef]

Lill, R. Function and biogenesis of iron-sulphur proteins. Nature 2009, 460, 831–838. [CrossRef]

Kispal, G.; Csere, P.; Prohl, C.; Lill, R. The mitochondrial proteins Atm1p and Nfs1p are essential for

biogenesis of cytosolic Fe/S proteins. EMBO J. 1999, 18, 3981–3989. [CrossRef]

Pondarré, C. , Antiochos, B.B.; Campagna, D.R.; Clarke, S.L.; Greer, E.L.; Deck, K.M.; McDonald, A.; Han, A.P.;

Medlock, A.; Kutok, J.L.; et al. The mitochondrial ATP-binding cassette transporter Abcb7 is essential in

mice and participates in cytosolic iron-sulfur cluster biogenesis. Hum. Mol. Genet. 2006, 15, 953–964.

Chen, S.; Sánchez-Fernández, R.; Lyver, E.R.; Dancis, A.; Rea, P.A. Functional characterization of AtATM1,

AtATM2, and AtATM3, a subfamily of Arabidopsis half-molecule ATP-binding cassette transporters implicated

in iron homeostasis. J. Biol. Chem. 2007, 282, 21561–21571. [CrossRef]

Verrier, P.J.; Bird, D.; Burla, B.; Dassa, E.; Forestier, C.; Geisler, M.; Klein, M.; Kolukisaoglu, U.; Lee, Y.;

Martinoia, E.; et al. Plant ABC proteins–a unified nomenclature and updated inventory. Trends Plant. Sci.

2008, 13, 151–159. [CrossRef]

Bernard, D.G.; Netz, D.J.; Lagny, T.J.; Pierik, A.J.; Balk, J. Requirements of the cytosolic iron-sulfur cluster

assembly pathway in Arabidopsis. Philos. Trans. R Soc. Lond. B Biol. Sci. 2013, 368, 20120259. [CrossRef]

Bych, K.; Netz, D.J.; Vigani, G.; Bill, E.; Lill, R.; Pierik, A.J.; Balk, J. The essential cytosolic iron-sulfur protein

Nbp35 acts without Cfd1partner in the green lineage. J. Biol. Chem. 2008, 283, 35797–35804. [CrossRef]

Kohbushi, H.; Nakai, Y.; Kikuchi, S.; Yabe, T.; Hori, H.; Nakai, M. Arabidopsis cytosolic Nbp35 homodimer

can assemble both [2Fe-2S] and [4Fe-4S] clusters in two distinct domains. Biochem Biophys Res. Commun.

2009, 378, 810–815. [CrossRef]

Varadarajan, J.; Guilleminot, J.; Saint-Jore-Dupas, C.; Piégu, B.; Chabouté, M.E.; Gomord, V.; Coolbaugh, R.C.;

Devic, M.; Delorme, V. ATR3 encodes a diflavin reductase essential for Arabidopsis embryo development.

New Phytol. 2010, 187, 67–82. [CrossRef]

Bastow, E.L.; Bych, K.; Crack, J.C.; Le Brun, N.E.; Balk, J. NBP35 interacts with DRE2 in the maturation of

cytosolic iron-sulphur proteins in Arabidopsis thaliana. Plant J. 2017, 89, 590–600. [CrossRef]

Zandalinas, S.I.; Song, L.; Sengupta, S.; McInturf, S.A.; Grant, D.G.; Marjault, H.B.; Castro-Guerrero, N.A.;

Burks, D.; Azad, R.K.; Mendoza-Cozatl, D.G.; et al. Expression of a dominant-negative AtNEET-H89C

protein disrupts iron-sulfur metabolism and iron homeostasis in Arabidopsis. Plant J. 2020, 101, 1152–1169.

[CrossRef] [PubMed]

Su, L.W.; Chang, S.H.; Li, M.Y.; Huang, H.Y.; Jane, W.N.; Yang, J.Y. Purification and biochemical

characterization of Arabidopsis At-NEET, an ancient iron-sulfur protein, reveals a conserved cleavage

motif for subcellular localization. Plant. Sci. 2013, 213, 46–54. [CrossRef] [PubMed]

Nechushtai, R.; Conlan, A.R.; Harir, Y.; Song, L.; Yogev, O.; Eisenberg-Domovich, Y.; Livnah, O.; Michaeli, D.;

Rosen, R.; Ma, V.; et al. Characterization of Arabidopsis NEET reveals an ancient role for NEET proteins in

iron metabolism. Plant. Cell. 2012, 24, 2139–2154. [CrossRef] [PubMed]

Luo, D.; Bernard, D.G.; Balk, J.; Hai, H.; Cui, X. The DUF59 family gene AE7 acts in the cytosolic iron-sulfur

cluster assembly pathway to maintain nuclear genome integrity in Arabidopsis. Plant Cell. 2012, 24, 4135–4148.

[CrossRef]

Couturier, J.; Jacquot, J.P.; Rouhier, N. Evolution and diversity of glutaredoxins in photosynthetic organisms.

Cell Mol. Life Sci. 2009, 66, 2539–2557. [CrossRef]

Iñigo, S.; Durand, A.N.; Ritter, A.; Le Gall, S.; Termathe, M.; Klassen, R.; Tohge, T.; De Coninck, B.; Van Leene, J.;

De Clercq, R.; et al. Glutaredoxin GRXS17 Associates with the Cytosolic Iron-Sulfur Cluster Assembly

Pathway. Plant. Physiol. 2016, 172, 858–873.

Int. J. Mol. Sci. 2020, 21, 3470

63.

64.

65.

66.

67.

68.

69.

70.

71.

72.

73.

74.

75.

76.

77.

78.

79.

80.

81.

82.

12 of 13

Cheng, N.H.; Liu, J.Z.; Liu, X.; Wu, Q.; Thompson, S.M.; Lin, J.; Chang, J.; Whitham, S.A.; Park, S.;

Cohen, J.D.; et al. Arabidopsis monothiol glutaredoxin, AtGRXS17, is critical for temperature-dependent

postembryonic growth and development via modulating auxin response. J. Biol. Chem. 2011, 286, 20398–20406.

[PubMed]

Yu, H.; Yang, J.; Shi, Y.; Donelson, J.; Thompson, S.M.; Sprague, S.; Roshan, T.; Wang, D.L.; Liu, J.; Park, S.; et al.

Arabidopsis Glutaredoxin S17 Contributes to Vegetative Growth, Mineral Accumulation, and Redox Balance

during Iron Deficiency. Front. Plant Sci. 2017, 8, 1045. [CrossRef] [PubMed]

Rey, P.; Taupin-Broggini, M.; Couturier, J.; Vignols, F.; Rouhier, N. Is There a Role for Glutaredoxins and

BOLAs in the Perception of the Cellular Iron Status in Plants? Front. Plant Sci. 2019, 10, 712. [CrossRef]

[PubMed]

Schwarz, G. Molybdenum cofactor biosynthesis and deficiency. Cell Mol. Life Sci. 2005, 62, 2792–2810.

[CrossRef] [PubMed]

Nakai, Y.; Harada, A.; Hashiguchi, Y.; Nakai, M.; Hayashi, H. Arabidopsis molybdopterin biosynthesis protein

Cnx5 collaborateswith the ubiquitin-like protein Urm11 in the thio-modification of tRNA. J. Biol. Chem. 2012,

287, 30874–30884. [CrossRef] [PubMed]

Zhang, Y.; Gladyshev, V.N. Molybdoproteomes and evolution of molybdenum utilization. J. Mol. Biol. 2008,

379, 881–899. [CrossRef] [PubMed]

Mendel, R.R.; Bittner, F. Cell biology of molybdenum. Biochim. Biophys. Acta 2006, 1763, 621–635. [CrossRef]

[PubMed]

Bauer, M.; Papenbrock, J. Identification and characterization of single-domain thiosulfate sulfurtransferases

from Arabidopsis thaliana. FEBS Lett. 2002, 532, 427–431. [CrossRef]

Bartels, A.; Mock, H.P.; Papenbrock, J. Differential expression of Arabidopsis sulfurtransferases under various

growth conditions. Plant. Physiol. Biochem. 2007, 45, 178–187. [CrossRef]

Krepinsky, K.; Leimkühler, S. Site-directed mutagenesis of the active site loop of the rhodanese-likedomain

of the human molybdopterin synthase sulfurase MOCS3. Major differences in substrate specificity between

eukaryotic and bacterial homologs. FEBS J. 2007, 274, 2778–2787. [CrossRef]

Leimkühler, S.; Rajagopalan, K.V. A sulfurtransferase is required in the transfer of cysteine sulfur in the

in vitro synthesis of molybdopterin from precursor Z in Escherichia coli. J. Biol. Chem. 2001, 276, 22024–22031.

[CrossRef] [PubMed]

Matthies, A.; Rajagopalan, K.V.; Mendel, R.R.; Leimkühler, S. Evidence for the physiological role of a

rhodanese-like protein for the biosynthesis of the molybdenum cofactor in humans. Proc. Natl. Acad.

Sci. USA 2004, 101, 5946–5951. [CrossRef] [PubMed]

Phizicky, E.M.; Hopper, A.K. tRNA biology charges to the front. Genes Dev. 2010, 24, 1832–1860. [CrossRef]

Nakai, Y.; Nakai, M.; Hayashi, H. Thio-modification of yeast cytosolic tRNA requires a ubiquitin-related

system that resembles bacterial sulfur transfer systems. J. Biol. Chem. 2008, 283, 27469–27476. [CrossRef]

[PubMed]

Chowdhury, M.M.; Dosche, C.; Löhmannsröben, H.-G.; Leimkühler, S. Dual Role of the Molybdenum

Cofactor Biosynthesis Protein MOCS3 in tRNA Thiolation and Molybdenum Cofactor Biosynthesis in

Humans. J. Biol. Chem. 2012, 287, 17297–17307. [CrossRef]

Wollers, S.; Heidenreich, T.; Zarepour, M.; Zachmann, D.; Kraft, C.; Zhao, Y.; Mendel, R.R.; Bittner, F. Binding

of sulfurated molybdenum cofactor to the C-terminal domain of ABA3 from Arabidopsis thaliana provides

insight into the mechanism of molybdenum cofactor sulfuration. J. Biol. Chem. 2008, 283, 9642–9650.

[CrossRef]

Schwarz, G.; Mendel, R.R.; Ribbe, M.W. Molybdenum cofactors, enzymes and pathways. Nature 2009, 460,

839–847. [CrossRef]

Maruyama-Nakashita, A.; Nakamura, Y.; Watanabe-Takahashi, A.; Inoue, E.; Yamaya, T.; Takahashi, H.

Identification of a novel cis-acting element conferring sulfur deficiency response in Arabidopsis roots. Plant J.

2005, 42, 305–314. [CrossRef]

Burroughs, A.M.; Iyer, L.M.; Aravind, L. Natural history of the E1-like superfamily: Implication for

adenylation, sulfur transfer, and ubiquitin conjugation. Proteins 2009, 75, 895–910. [CrossRef]

Xu, J.; Zhang, J.; Wang, L.; Zhou, J.; Huang, H.; Wu, J.; Zhong, Y.; Shi, Y. Solution structure of Urm1 and its

implications for the origin of protein modifiers. Proc. Natl. Acad. Sci. USA 2006, 103, 11625–11630. [CrossRef]

Int. J. Mol. Sci. 2020, 21, 3470

83.

84.

13 of 13

Schulman, B.A.; Harper, J.W. Ubiquitin-like protein activation by E1 enzymes: The apex for downstream

signalling pathways. Nat. Rev. Mol. Cell Biol. 2009, 10, 319–331. [CrossRef] [PubMed]

Selles, B.; Moseler, A.; Rouhier, N.; Couturier, J. Rhodanese domain-containing sulfurtransferases:

Multifacetedproteins involved in sulfur trafficking in plants. J. Exp. Bot. 2019, 70, 4139–4154. [CrossRef]

[PubMed]

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