ID   UBP16_ARATH             Reviewed;        1008 AA.
AC   Q9SB51; Q9FPS8;
DT   15-JAN-2008, integrated into UniProtKB/Swiss-Prot.
DT   01-MAY-2000, sequence version 1.
DT   27-MAR-2024, entry version 142.
DE   RecName: Full=Ubiquitin carboxyl-terminal hydrolase 16;
DE            EC=3.4.19.12;
DE   AltName: Full=Deubiquitinating enzyme 16;
DE            Short=AtUBP16;
DE   AltName: Full=Ubiquitin thioesterase 16;
DE   AltName: Full=Ubiquitin-specific-processing protease 16;
GN   Name=UBP16; OrderedLocusNames=At4g24560; ORFNames=F22K18.240;
OS   Arabidopsis thaliana (Mouse-ear cress).
OC   Eukaryota; Viridiplantae; Streptophyta; Embryophyta; Tracheophyta;
OC   Spermatophyta; Magnoliopsida; eudicotyledons; Gunneridae; Pentapetalae;
OC   rosids; malvids; Brassicales; Brassicaceae; Camelineae; Arabidopsis.
OX   NCBI_TaxID=3702;
RN   [1]
RP   NUCLEOTIDE SEQUENCE [MRNA], GENE FAMILY ORGANIZATION, AND NOMENCLATURE.
RC   STRAIN=cv. Columbia;
RX   PubMed=11115897; DOI=10.1104/pp.124.4.1828;
RA   Yan N., Doelling J.H., Falbel T.G., Durski A.M., Vierstra R.D.;
RT   "The ubiquitin-specific protease family from Arabidopsis. AtUBP1 and 2 are
RT   required for the resistance to the amino acid analog canavanine.";
RL   Plant Physiol. 124:1828-1843(2000).
RN   [2]
RP   NUCLEOTIDE SEQUENCE [LARGE SCALE GENOMIC DNA].
RC   STRAIN=cv. Columbia;
RX   PubMed=10617198; DOI=10.1038/47134;
RA   Mayer K.F.X., Schueller C., Wambutt R., Murphy G., Volckaert G., Pohl T.,
RA   Duesterhoeft A., Stiekema W., Entian K.-D., Terryn N., Harris B.,
RA   Ansorge W., Brandt P., Grivell L.A., Rieger M., Weichselgartner M.,
RA   de Simone V., Obermaier B., Mache R., Mueller M., Kreis M., Delseny M.,
RA   Puigdomenech P., Watson M., Schmidtheini T., Reichert B., Portetelle D.,
RA   Perez-Alonso M., Boutry M., Bancroft I., Vos P., Hoheisel J.,
RA   Zimmermann W., Wedler H., Ridley P., Langham S.-A., McCullagh B.,
RA   Bilham L., Robben J., van der Schueren J., Grymonprez B., Chuang Y.-J.,
RA   Vandenbussche F., Braeken M., Weltjens I., Voet M., Bastiaens I., Aert R.,
RA   Defoor E., Weitzenegger T., Bothe G., Ramsperger U., Hilbert H., Braun M.,
RA   Holzer E., Brandt A., Peters S., van Staveren M., Dirkse W., Mooijman P.,
RA   Klein Lankhorst R., Rose M., Hauf J., Koetter P., Berneiser S., Hempel S.,
RA   Feldpausch M., Lamberth S., Van den Daele H., De Keyser A., Buysshaert C.,
RA   Gielen J., Villarroel R., De Clercq R., van Montagu M., Rogers J.,
RA   Cronin A., Quail M.A., Bray-Allen S., Clark L., Doggett J., Hall S.,
RA   Kay M., Lennard N., McLay K., Mayes R., Pettett A., Rajandream M.A.,
RA   Lyne M., Benes V., Rechmann S., Borkova D., Bloecker H., Scharfe M.,
RA   Grimm M., Loehnert T.-H., Dose S., de Haan M., Maarse A.C., Schaefer M.,
RA   Mueller-Auer S., Gabel C., Fuchs M., Fartmann B., Granderath K., Dauner D.,
RA   Herzl A., Neumann S., Argiriou A., Vitale D., Liguori R., Piravandi E.,
RA   Massenet O., Quigley F., Clabauld G., Muendlein A., Felber R., Schnabl S.,
RA   Hiller R., Schmidt W., Lecharny A., Aubourg S., Chefdor F., Cooke R.,
RA   Berger C., Monfort A., Casacuberta E., Gibbons T., Weber N., Vandenbol M.,
RA   Bargues M., Terol J., Torres A., Perez-Perez A., Purnelle B., Bent E.,
RA   Johnson S., Tacon D., Jesse T., Heijnen L., Schwarz S., Scholler P.,
RA   Heber S., Francs P., Bielke C., Frishman D., Haase D., Lemcke K.,
RA   Mewes H.-W., Stocker S., Zaccaria P., Bevan M., Wilson R.K.,
RA   de la Bastide M., Habermann K., Parnell L., Dedhia N., Gnoj L., Schutz K.,
RA   Huang E., Spiegel L., Sekhon M., Murray J., Sheet P., Cordes M.,
RA   Abu-Threideh J., Stoneking T., Kalicki J., Graves T., Harmon G.,
RA   Edwards J., Latreille P., Courtney L., Cloud J., Abbott A., Scott K.,
RA   Johnson D., Minx P., Bentley D., Fulton B., Miller N., Greco T., Kemp K.,
RA   Kramer J., Fulton L., Mardis E., Dante M., Pepin K., Hillier L.W.,
RA   Nelson J., Spieth J., Ryan E., Andrews S., Geisel C., Layman D., Du H.,
RA   Ali J., Berghoff A., Jones K., Drone K., Cotton M., Joshu C., Antonoiu B.,
RA   Zidanic M., Strong C., Sun H., Lamar B., Yordan C., Ma P., Zhong J.,
RA   Preston R., Vil D., Shekher M., Matero A., Shah R., Swaby I.K.,
RA   O'Shaughnessy A., Rodriguez M., Hoffman J., Till S., Granat S., Shohdy N.,
RA   Hasegawa A., Hameed A., Lodhi M., Johnson A., Chen E., Marra M.A.,
RA   Martienssen R., McCombie W.R.;
RT   "Sequence and analysis of chromosome 4 of the plant Arabidopsis thaliana.";
RL   Nature 402:769-777(1999).
RN   [3]
RP   GENOME REANNOTATION.
RC   STRAIN=cv. Columbia;
RX   PubMed=27862469; DOI=10.1111/tpj.13415;
RA   Cheng C.Y., Krishnakumar V., Chan A.P., Thibaud-Nissen F., Schobel S.,
RA   Town C.D.;
RT   "Araport11: a complete reannotation of the Arabidopsis thaliana reference
RT   genome.";
RL   Plant J. 89:789-804(2017).
RN   [4]
RP   FUNCTION, DISRUPTION PHENOTYPE, INDUCTION BY SALT, TISSUE SPECIFICITY,
RP   MUTAGENESIS OF CYS-551, CATALYTIC ACTIVITY, INTERACTION WITH SHM1 AND SHM4,
RP   AND SUBCELLULAR LOCATION.
RX   PubMed=23232097; DOI=10.1105/tpc.112.106393;
RA   Zhou H., Zhao J., Yang Y., Chen C., Liu Y., Jin X., Chen L., Li X.,
RA   Deng X.W., Schumaker K.S., Guo Y.;
RT   "Ubiquitin-specific protease16 modulates salt tolerance in Arabidopsis by
RT   regulating Na(+)/H(+) antiport activity and serine hydroxymethyltransferase
RT   stability.";
RL   Plant Cell 24:5106-5122(2012).
RN   [5]
RP   FUNCTION, AND INTERACTION WITH HIPP27.
RX   PubMed=23857362; DOI=10.4161/psb.25680;
RA   Zhao J., Zhou H., Li Y.;
RT   "UBIQUITIN-SPECIFIC PROTEASE16 interacts with a HEAVY METAL ASSOCIATED
RT   ISOPRENYLATED PLANT PROTEIN27 and modulates cadmium tolerance.";
RL   Plant Signal. Behav. 8:E25680-E25680(2013).
RN   [6]
RP   INDUCTION BY NAC045 AND NAC086, AND TISSUE SPECIFICITY.
RX   PubMed=25081480; DOI=10.1126/science.1253736;
RA   Furuta K.M., Yadav S.R., Lehesranta S., Belevich I., Miyashima S.,
RA   Heo J.O., Vaten A., Lindgren O., De Rybel B., Van Isterdael G.,
RA   Somervuo P., Lichtenberger R., Rocha R., Thitamadee S., Taehtiharju S.,
RA   Auvinen P., Beeckman T., Jokitalo E., Helariutta Y.;
RT   "Plant development. Arabidopsis NAC45/86 direct sieve element morphogenesis
RT   culminating in enucleation.";
RL   Science 345:933-937(2014).
CC   -!- FUNCTION: Recognizes and hydrolyzes the peptide bond at the C-terminal
CC       Gly of ubiquitin. Involved in the processing of poly-ubiquitin
CC       precursors as well as that of ubiquitinated proteins. Involved in salt
CC       tolerance by modulating sodium transport activity and repressing cell
CC       death at least partially through modulating SHM1 stability and activity
CC       (PubMed:23232097). Involved in cadmium tolerance by interacting with
CC       HIPP27 and probably modulating its stability (PubMed:23857362).
CC       {ECO:0000269|PubMed:23232097, ECO:0000269|PubMed:23857362}.
CC   -!- CATALYTIC ACTIVITY:
CC       Reaction=Thiol-dependent hydrolysis of ester, thioester, amide, peptide
CC         and isopeptide bonds formed by the C-terminal Gly of ubiquitin (a 76-
CC         residue protein attached to proteins as an intracellular targeting
CC         signal).; EC=3.4.19.12; Evidence={ECO:0000269|PubMed:23232097};
CC   -!- SUBUNIT: Interacts with SHM1 and SHM4 (PubMed:23232097). Interacts with
CC       HIPP27 (PubMed:23857362). {ECO:0000269|PubMed:23232097,
CC       ECO:0000269|PubMed:23857362}.
CC   -!- INTERACTION:
CC       Q9SB51; Q9SZJ5: SHM1; NbExp=3; IntAct=EBI-6589403, EBI-2292536;
CC       Q9SB51; O23254: SHM4; NbExp=3; IntAct=EBI-6589403, EBI-6589432;
CC   -!- SUBCELLULAR LOCATION: Membrane {ECO:0000305}; Single-pass membrane
CC       protein {ECO:0000305}.
CC   -!- TISSUE SPECIFICITY: Expressed in flowers, siliques, rosette leaves,
CC       cauline leaves, stems and at a lower level in roots. In roots,
CC       expressed in the sieve elements. {ECO:0000269|PubMed:23232097,
CC       ECO:0000269|PubMed:25081480}.
CC   -!- INDUCTION: Regulated by the transcription factors NAC045 and NAC086 and
CC       up-regulated by salt stress. {ECO:0000269|PubMed:23232097,
CC       ECO:0000269|PubMed:25081480}.
CC   -!- DISRUPTION PHENOTYPE: Exhibits reduced salt tolerance. Reduced shoot
CC       growth in response to salt stress. {ECO:0000269|PubMed:23232097}.
CC   -!- SIMILARITY: Belongs to the peptidase C19 family. {ECO:0000305}.
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DR   EMBL; AF302666; AAG42757.1; -; mRNA.
DR   EMBL; AL035356; CAA23007.1; -; Genomic_DNA.
DR   EMBL; AL161561; CAB79366.1; -; Genomic_DNA.
DR   EMBL; CP002687; AEE84926.1; -; Genomic_DNA.
DR   PIR; T05578; T05578.
DR   RefSeq; NP_567705.1; NM_118589.3.
DR   AlphaFoldDB; Q9SB51; -.
DR   SMR; Q9SB51; -.
DR   BioGRID; 13847; 4.
DR   IntAct; Q9SB51; 2.
DR   STRING; 3702.Q9SB51; -.
DR   MEROPS; C19.A07; -.
DR   PaxDb; 3702-AT4G24560-1; -.
DR   ProteomicsDB; 228481; -.
DR   EnsemblPlants; AT4G24560.1; AT4G24560.1; AT4G24560.
DR   GeneID; 828558; -.
DR   Gramene; AT4G24560.1; AT4G24560.1; AT4G24560.
DR   KEGG; ath:AT4G24560; -.
DR   Araport; AT4G24560; -.
DR   TAIR; AT4G24560; UBP16.
DR   eggNOG; KOG1865; Eukaryota.
DR   HOGENOM; CLU_007397_1_1_1; -.
DR   InParanoid; Q9SB51; -.
DR   OMA; LFYARCT; -.
DR   OrthoDB; 227085at2759; -.
DR   PhylomeDB; Q9SB51; -.
DR   PRO; PR:Q9SB51; -.
DR   Proteomes; UP000006548; Chromosome 4.
DR   ExpressionAtlas; Q9SB51; baseline and differential.
DR   GO; GO:0016020; C:membrane; IEA:UniProtKB-SubCell.
DR   GO; GO:0004843; F:cysteine-type deubiquitinase activity; IDA:UniProtKB.
DR   GO; GO:0046872; F:metal ion binding; IEA:UniProtKB-KW.
DR   GO; GO:0051301; P:cell division; IGI:TAIR.
DR   GO; GO:0009908; P:flower development; IGI:TAIR.
DR   GO; GO:0048366; P:leaf development; IGI:TAIR.
DR   GO; GO:0016579; P:protein deubiquitination; IDA:UniProtKB.
DR   GO; GO:0006508; P:proteolysis; IEA:UniProtKB-KW.
DR   GO; GO:1901000; P:regulation of response to salt stress; IMP:UniProtKB.
DR   GO; GO:0009651; P:response to salt stress; IEP:UniProtKB.
DR   GO; GO:0048364; P:root development; IGI:TAIR.
DR   GO; GO:0048367; P:shoot system development; IGI:TAIR.
DR   Gene3D; 6.10.140.2220; -; 1.
DR   Gene3D; 3.90.70.10; Cysteine proteinases; 1.
DR   InterPro; IPR038765; Papain-like_cys_pep_sf.
DR   InterPro; IPR001394; Peptidase_C19_UCH.
DR   InterPro; IPR018200; USP_CS.
DR   InterPro; IPR028889; USP_dom.
DR   InterPro; IPR002893; Znf_MYND.
DR   PANTHER; PTHR24006; UBIQUITIN CARBOXYL-TERMINAL HYDROLASE; 1.
DR   PANTHER; PTHR24006:SF874; UBIQUITIN CARBOXYL-TERMINAL HYDROLASE 16; 1.
DR   Pfam; PF00443; UCH; 1.
DR   Pfam; PF01753; zf-MYND; 1.
DR   SUPFAM; SSF54001; Cysteine proteinases; 1.
DR   SUPFAM; SSF144232; HIT/MYND zinc finger-like; 1.
DR   PROSITE; PS00972; USP_1; 1.
DR   PROSITE; PS50235; USP_3; 1.
DR   PROSITE; PS01360; ZF_MYND_1; 1.
DR   PROSITE; PS50865; ZF_MYND_2; 1.
DR   Genevisible; Q9SB51; AT.
PE   1: Evidence at protein level;
KW   Hydrolase; Membrane; Metal-binding; Protease; Reference proteome;
KW   Thiol protease; Transmembrane; Transmembrane helix;
KW   Ubl conjugation pathway; Zinc; Zinc-finger.
FT   CHAIN           1..1008
FT                   /note="Ubiquitin carboxyl-terminal hydrolase 16"
FT                   /id="PRO_0000313042"
FT   TRANSMEM        7..27
FT                   /note="Helical"
FT                   /evidence="ECO:0000255"
FT   DOMAIN          542..847
FT                   /note="USP"
FT   ZN_FING         74..111
FT                   /note="MYND-type"
FT                   /evidence="ECO:0000255|PROSITE-ProRule:PRU00134"
FT   REGION          122..149
FT                   /note="Disordered"
FT                   /evidence="ECO:0000256|SAM:MobiDB-lite"
FT   REGION          159..178
FT                   /note="Disordered"
FT                   /evidence="ECO:0000256|SAM:MobiDB-lite"
FT   REGION          187..233
FT                   /note="Disordered"
FT                   /evidence="ECO:0000256|SAM:MobiDB-lite"
FT   REGION          275..309
FT                   /note="Disordered"
FT                   /evidence="ECO:0000256|SAM:MobiDB-lite"
FT   REGION          326..379
FT                   /note="Disordered"
FT                   /evidence="ECO:0000256|SAM:MobiDB-lite"
FT   REGION          859..905
FT                   /note="Disordered"
FT                   /evidence="ECO:0000256|SAM:MobiDB-lite"
FT   REGION          952..1008
FT                   /note="Disordered"
FT                   /evidence="ECO:0000256|SAM:MobiDB-lite"
FT   COMPBIAS        189..208
FT                   /note="Polar residues"
FT                   /evidence="ECO:0000256|SAM:MobiDB-lite"
FT   COMPBIAS        209..233
FT                   /note="Basic and acidic residues"
FT                   /evidence="ECO:0000256|SAM:MobiDB-lite"
FT   COMPBIAS        281..297
FT                   /note="Polar residues"
FT                   /evidence="ECO:0000256|SAM:MobiDB-lite"
FT   COMPBIAS        332..362
FT                   /note="Polar residues"
FT                   /evidence="ECO:0000256|SAM:MobiDB-lite"
FT   COMPBIAS        874..905
FT                   /note="Polar residues"
FT                   /evidence="ECO:0000256|SAM:MobiDB-lite"
FT   COMPBIAS        962..998
FT                   /note="Polar residues"
FT                   /evidence="ECO:0000256|SAM:MobiDB-lite"
FT   ACT_SITE        551
FT                   /note="Nucleophile"
FT                   /evidence="ECO:0000255|PROSITE-ProRule:PRU10092"
FT   ACT_SITE        807
FT                   /note="Proton acceptor"
FT                   /evidence="ECO:0000255|PROSITE-ProRule:PRU10092"
FT   BINDING         74
FT                   /ligand="Zn(2+)"
FT                   /ligand_id="ChEBI:CHEBI:29105"
FT                   /ligand_label="1"
FT                   /evidence="ECO:0000255|PROSITE-ProRule:PRU00134"
FT   BINDING         77
FT                   /ligand="Zn(2+)"
FT                   /ligand_id="ChEBI:CHEBI:29105"
FT                   /ligand_label="1"
FT                   /evidence="ECO:0000255|PROSITE-ProRule:PRU00134"
FT   BINDING         85
FT                   /ligand="Zn(2+)"
FT                   /ligand_id="ChEBI:CHEBI:29105"
FT                   /ligand_label="2"
FT                   /evidence="ECO:0000255|PROSITE-ProRule:PRU00134"
FT   BINDING         88
FT                   /ligand="Zn(2+)"
FT                   /ligand_id="ChEBI:CHEBI:29105"
FT                   /ligand_label="2"
FT                   /evidence="ECO:0000255|PROSITE-ProRule:PRU00134"
FT   BINDING         94
FT                   /ligand="Zn(2+)"
FT                   /ligand_id="ChEBI:CHEBI:29105"
FT                   /ligand_label="1"
FT                   /evidence="ECO:0000255|PROSITE-ProRule:PRU00134"
FT   BINDING         98
FT                   /ligand="Zn(2+)"
FT                   /ligand_id="ChEBI:CHEBI:29105"
FT                   /ligand_label="1"
FT                   /evidence="ECO:0000255|PROSITE-ProRule:PRU00134"
FT   BINDING         107
FT                   /ligand="Zn(2+)"
FT                   /ligand_id="ChEBI:CHEBI:29105"
FT                   /ligand_label="2"
FT                   /evidence="ECO:0000255|PROSITE-ProRule:PRU00134"
FT   BINDING         111
FT                   /ligand="Zn(2+)"
FT                   /ligand_id="ChEBI:CHEBI:29105"
FT                   /ligand_label="2"
FT                   /evidence="ECO:0000255|PROSITE-ProRule:PRU00134"
FT   MUTAGEN         551
FT                   /note="C->S: Abolishes deubiquitination activity."
FT                   /evidence="ECO:0000269|PubMed:23232097"
FT   CONFLICT        183
FT                   /note="K -> N (in Ref. 1; AAG42757)"
FT                   /evidence="ECO:0000305"
SQ   SEQUENCE   1008 AA;  110600 MW;  F2DF3BD6E9039B9E CRC64;
     MLLVLDLGIS SLVLVVSLVL PLIGLFVRHK WRVAAQRREE IRRLLIHASE EAARAELEAS
     VEFSSVAVSN VFHCPVCYCL ATTRCSRCKA VRYCSGKCQI IHWRQGHKDE CHPASIVYDS
     EDESDSDLRL GEENGQNTPE ETLLVGPEPV TIPIGESLLS NRARSPEDGN GDIADNKDDL
     IDKEEAVSVA ETSGSSFSGF SSSPRNDSGD EISRCESFSS SESERSESLL DAHVSVEPED
     TCFSTIEDAP SKLLSPKFVH LVESVDNLAN LPKLSVHKPE DDAGQNQSQS RSLHSLVTDR
     HPVSADPSLK SSDFWGTALG SAERVSDSCV KSKSGRPGNS SLHFSFGSGS SRDTSAAKVS
     EQRSSILKEA PRGTGYISDG VNLRERNAKR FDEAEIALPI SSSTDALSPL DSSNLSHVTL
     PKSKSASSEN GSMLAPLKVG EVQLLASKAS NTKKCADLMK HSPLGAKSVR VLDHQKQNGA
     VVQHINSLHG RSGLKASVLK VVDQWTRPKS ENEMAGRHGH KGLFPYEVFA KLYTYKIEFQ
     PCGLINVGNS CFANVVFQCL MFTPPLTTYF LQQFHSRACT KKEQCFTCGF EKLVVKAKEE
     KSPLSPNGLL SQLQNIGIFL GNGKEEDAHE FLRFVVDTMQ SVCIKASEYD MTKSSKLEDT
     TLIGLTFGGY LRSKIKCMKC QVKSELREKM MDLTVEIDGD ISTLDDALRR FTRTEILDGE
     NKYRCGSCKS YERAKKKLKI TEPPNVLTIA LKRFQAGKFG KLNKLIRFPE TLDLAPYVSG
     GSEKSHDYKL YGVIVHLDVM NAAFSGHYVC YIRNQNKWYK ADDSTVVTSD VERILTKGAY
     MLFYARCTPT PPRLAVCTKT EASNKKSRVP LPKANEKSTI SRSVSTSSPE LSSNTPGGGR
     SGNIQSFYSS FQRLQKILEE DSASDSSSLF DSNSDECSCS TDSTSMDDFA DFIFGDHQGR
     AHGQSETPSP TSSSSSSSPP FTRRSPLSRS SPETYGTSRH QLPLGGER
//