Quantitative redox proteomics revealed molecular mechanisms of salt tolerance in the roots of sugar beet monomeric addition line M14

Liu, He; Du, Xiaoxue; Zhang, Jialin; Li, Jinna; Chen, Sixue; Duanmu, Huizi; Li, Haiying

doi:10.1186/s40529-022-00337-w

Botanical Studies

Table 1 A list of 95 differential redox proteins in BvM14 roots between control and NaCl-treated groups

From: Quantitative redox proteomics revealed molecular mechanisms of salt tolerance in the roots of sugar beet monomeric addition line M14

No.	Protein ID^a	Description	Abbreviation	Sequence with modification^b	Plant species	iodoTMT salt200/control ratio^c	iodoTMT salt400/control ratio^d	p-value	Protein location^e
Metabolism
Carbohydrate metabolism
1	A0A2H5P1K5	6-Phosphogluconate dehydrogenase, decarboxylating	PGDH	IC²SYAQGMNILR	Citrus unshiu	–	1.38	0.05	Chloroplast
2	731322678	Beta-fructofuranosidase, soluble isoenzyme I	β-FFase	NWFC⁴TDQSR	Beta vulgaris subsp. vulgaris	–	0.76	0.03	Vacuole
3	Q41140	Pyrophosphate–fructose 6-phosphate 1-phosphotransferase subunit alpha	PFP1	SLYKPELPPC¹⁰LQGTTVR	Ricinus communis	–	0.74	0.03	Cytoplasm
4	1108966238	Sucrose synthase isoform X2	SUS	LLPDAVGTTC¹⁰GQR	Beta vulgaris subsp. vulgaris	–	0.64	0.05	Chloroplast
5	731323052	Probable fructokinase-4	FRK	LLLVTLGDQGC¹¹R	Beta vulgaris subsp. vulgaris	0.75	–	0.04	Cytoplasm
6	A0A0S3T1M9	UDP-glucose 6-dehydrogenase	UGDH	VFDC⁴MQKPAFVFDGR	Vigna angularis var. angularis	–	1.30	0.02	Cytoplasm
7	731364471	Trypsin inhibitor BvTI	TI	NPELPC⁶PYYITR	Beta vulgaris subsp. vulgaris	0.30	–	0.04	Extracellular
8	731344067	Kunitz trypsin inhibitor 1-like	KTI	C¹PYYSVVQSQDDR	Beta vulgaris subsp. vulgaris	–	1.50	0.01	Vacuole
9	731331165	Alpha-amylase/trypsin inhibitor	α-TI	ANGGC⁵NNAYNYSYSR	Beta vulgaris subsp. vulgaris	0.52	0.49	0.01	Extracellular
Amino acid metabolism
10	731353768	Aspartate aminotransferase	AST	VASAQC⁶LSGTGSLR	Beta vulgaris subsp. vulgaris	–	1.20	0.03	Cytoplasm
11	A0A2P5X5J0	Aspartate aminotransferase	AST	IAAVQALSGTGAC¹³R	Gossypium barbadense	–	1.26	0.04	Cytoplasm
12	731351009	Aspartic proteinase A1-like	AP	VGEGPAAQC⁹ISGFTALDVPPPR	Beta vulgaris subsp. vulgaris	1.35	–	0.02	Vacuole
13	731353609	3-Hydroxyisobutyryl-CoA hydrolase-like protein 3, mitochondrial isoform X1	H2BCH	C¹VLIESSSPR	Beta vulgaris subsp. vulgaris	–	1.21	0.01	Mitochondrial
14	A0A2I0XB93	Aspartate-semialdehyde dehydrogenase	ASDH	IRQDLSQEGNHGLDIFVC¹⁸GDQIR	Dendrobium catenatum	–	1.41	0.02	Cytoplasm
15	A0A0M3TGF7	Acetolactate synthase	ALS	C¹GISDVFAYPGGASMEIHQALTR	Poa annua	–	1.33	0.03	Chloroplast
16	731325199	Serine hydroxymethyl transferase 4	SHMT	MLIC⁴GGSAYPR	Beta vulgaris subsp. vulgaris	0.59	–	0.04	Cytoplasm
17	731317741	LL-diaminopimelate aminotransferase, chloroplastic	DAPL	TELIFFC⁷SPNNPTGAAATR	Beta vulgaris subsp. vulgaris	–	0.80	0.05	Chloroplast
18	A0A0K9RN52	Glutamate-1-semialdehyde 2,1-aminomutase	GSAM	FVNSGTEAC⁹MGVLR	Spinacia oleracea	1.21	–	0.00	Chloroplast
Other metabolism
19	A0A0B2RAS0	Proteasome subunit alpha type-5	PSAM5	FSYGEPMTVESTTQAIC¹⁷DLALR	Glycine soja	0.76	–	0.05	Nucleus
20	731363918	Proteasome subunit alpha type-5	PSAM5	FSYGEPMTVESTTQALC¹⁷DLALR	Beta vulgaris subsp. vulgaris	–	1.24	0.00	Nucleus
21	731361751	Proteasome subunit alpha type-5	PSAM5	FSYGEPMNVESTTQALC¹⁷DLALR	Beta vulgaris subsp. vulgaris	–	1.46	0.03	Nucleus
22	A0A287HDI6	Proteasome subunit beta type-6	PSAM6	QLTDNVYVC⁹R	Hordeum vulgare subsp. vulgare	1.23	1.57	0.05	Nucleus
23	M0UCJ4	ATP synthase subunit beta	ATPsny	VC²QVIGAVVDVR	Musa acuminata subsp. malaccensis	0.74	–	0.04	Mitochondrion
24	M8C108	ATP synthase subunit alpha, mitochondrial	ATPsny	MTNFC⁵TNFQVDEIGR	Aegilops tauschii	–	1.76	0.01	Mitochondrial
ROS homeostasis
25	A0A287X935	Peroxidase	POD	ASVEAVC⁷PGVVSC¹³ADILAITAR	Hordeum vulgare subsp. vulgare	–	2.13	0.01	Extracellular
26	A0A2G9HTZ9	Peroxidase	POD	QAVEAQC⁷PGVVSC¹³SDILAIAAR	Handroanthus impetiginosus	–	2.05	0.01	Extracellular
27	A0A1S2YYJ3	Peroxidase	POD	SDLENAC⁷PSTVSC¹³ADILTLAAR	Cicer arietinum	–	1.70	0.01	Extracellular
28	A0A2G2WVY9	Peroxidase	POD	IKTMC⁵PGAAVSC¹²ADILALAAR	Capsicum baccatum	0.46	–	0.05	Extracellular
29	J3L3F3	Peroxidase	POD	LEAAC⁵PKTVSC¹¹ADILALAAR	Oryza brachyantha	–	1.65	0.01	Extracellular
30	A0A0J8CS88	Peroxidase	POD	QC²PAGNAGANIVVPMDPISPTISDTAYYR	Beta vulgaris subsp. vulgaris	–	1.50	0.04	Extracellular
31	731316487	Peroxidase 4	POD4	TC²PQLFPTIR	Beta vulgaris subsp. vulgaris	–	0.56	0.01	Extracellular
32	731313635	Peroxidase 12	POD12	VVSC⁴ADITSLAAR	Beta vulgaris subsp. vulgaris	0.42	–	0.05	Extracellular
33	731313633	Peroxidase 12	POD12	VVSC⁴ADITTLAAR	Beta vulgaris subsp. vulgaris	–	0.69	0.04	Extracellular
34	731313639	Peroxidase 12	POD12	VVSC⁴ADLTALAAR	Beta vulgaris subsp. vulgaris	0.64	–	0.03	Vacuole
35	A0A0A9MG34	Peroxidase 72	POD72	AALEAAC⁷PSTVSC¹³ADILALTAR	Arundo donax	–	1.55	0.05	Extracellular
36	731337443	Peroxidase 72	POD72	AAVEQAC⁷PHTVSC¹³ADILALTAR	Beta vulgaris subsp. vulgaris	–	2.32	0.03	Extracellular
37	731331163	Protein P21	P21	TDNYC⁵C⁶NSGSC11GPTDYSR	Beta vulgaris subsp. vulgaris	4.09	1.44	0.02	Extracellular
38	A0A1S3TTL2	DSBA domain-containing protein	DSBA	NVGLEYC⁷MSGLTGNTIDSHR	Vigna radiata var. radiata	0.55	1.63	0.04	Chloroplast
39	731339890	EG45-like domain containing protein 2	EG45	VTDLC⁵DSC⁸AGDLNLSQEAFNVIADTR	Beta vulgaris subsp. vulgaris	–	0.44	0.00	Extracellular
40	731352762	EG45-like domain containing protein	EG45	VTC³VSGTNQGVPQPC¹⁵R	Beta vulgaris subsp. vulgaris	–	1.32	0.04	Extracellular
41	A0A0J8B2W2	Fe2OG dioxygenase domain-containing protein	Fe2OG	VAIYPEC⁷PNPELVR	Beta vulgaris subsp. vulgaris	–	0.59	0.02	Cytoplasm
42	M0RV51	Glutathione S-transferase DHAR2	GST	AAVGAPDVLGDC¹²PFSQR	Musa acuminata subsp. malaccensis	0.64	–	0.01	Cytoplasm
43	A0A199UJ48	3-Ketoacyl-CoA thiolase 2, peroxisomal	HT	IELFAQARDC¹⁰LLPMGITSENVAHR	Ananas comosus	–	1.45	0.00	Peroxisome
44	731355863	l-Ascorbate oxidase-like	AOX	QLGTPWADGTASISQC¹⁶PINPGETFTYR	Beta vulgaris subsp. vulgaris	0.51	1.58	0.01	Plasma Membrane
45	A0A151QMI1	Nitrate reductase [NADH] 2	NR	QSGALHVC⁸FEGAEDLPGGGGSKYGTSVTR	Cajanus cajan	–	1.54	0.00	Peroxisome
46	731357289	NADH dehydrogenase [ubiquinone] 1 alpha subcomplex subunit 8-B	NADH	C¹VFSLLR	Beta vulgaris subsp. vulgaris	–	1.29	0.04	Mitochondrion
47	731359814	Peptide methionine sulfoxide reductase B5-like	MSR	FDSGC⁵GWPAFYEGLPGAITR	Beta vulgaris subsp. vulgaris	–	0.75	0.02	Cytoplasm
48	731312054	Cysteine protease RD19A	RD19A	LVSLSEQQLVDC¹²DHEC¹⁶DPEER	Beta vulgaris subsp. vulgaris	1.63	–	0.04	Vacuole
Stress and defense
49	731330989	Probable polygalacturonase	PGs	VIDNFEYSAINC¹²R	Beta vulgaris subsp. vulgaris	1.5	–	0.04	Plasma Membrane
50	731338906	PLAT domain-containing protein 3	PITI	GPC³LNAPVC⁹AMR	Beta vulgaris subsp. vulgaris	–	1.26	0.01	Vacuole
51	A0A166FTZ6	Heat shock cognate 70 kDa protein	Hsp70	MDIC⁴SVHDVVLVGGSTR	Daucus carota subsp. sativus	–	1.21	0.05	Endoplasmic reticulum
52	Q9XFW7	Chitinase	–	FGFC⁴GSTDAYC¹¹GEGC¹⁵R	Beta vulgaris subsp. vulgaris	2.05	–	0.01	Extracellular
53	731352263	Endochitinase EP3	EP3	VGYYTQYC⁸QQLGVSPGNNLR	Beta vulgaris subsp. vulgaris	–	0.65	0.02	Cell Wall
54	731352251	Endochitinase EP3	EP3	AINGGEC⁷GGGNTPAVNAR	Beta vulgaris subsp. vulgaris	–	0.45	0.00	Cell Wall
55	731352259	Endochitinase EP3	EP3	LEC³DGGNPATVNAR	Beta vulgaris subsp. vulgaris	0.71	–	0.01	Cell Wall
56	731329194	Pathogenesis-related protein PR-4	PR-4	NQYGWTAFC⁹GPAGPTGQASC²⁰GR	Beta vulgaris subsp. vulgaris	1.64	–	0.01	Cytoplasm
57	731326017	Jasmonate-induced protein homolog	JIP	LDASHDESHC¹⁰PGAAAR	Beta vulgaris subsp. vulgaris	–	1.33	0.02	Cell wall
58	731332586	Jasmonate-induced protein homolog	JIP	LENSGNC⁷SYDVDYETR	Beta vulgaris subsp. vulgaris	0.36	–	0.04	Cell wall
59	731312253	Jasmonate-induced protein homolog	JIP	C¹GPAAEFNNVNWTQVR	Beta vulgaris subsp. vulgaris	–	1.49	0.00	Cell wall
60	A0A2P4NB14	Flavonoid 3′,5′-methyltransferase	GIP	IESSLLSIGDGITLC¹⁵R	Quercus suber	–	1.33	0.02	Cytoplasm
61	731357526	lysM domain-containing GPI-anchored protein 2		STC³AYVGYNR	Beta vulgaris subsp. vulgaris	0.53	–	0.01	Plasma Membrane
Transport
62	A0A0K9RCQ9	Purple acid phosphatase	PAP	FLEEC⁵LASANR	Spinacia oleracea	0.40	–	0.03	Extracellular
63	731352863	Probable inactive purple acid phosphatase 29	PAP	QEEVIC⁶PGVNSGFFDTMR	Beta vulgaris subsp. vulgaris	0.68	0.75	0.01	Extracellular
64	731320622	Importin subunit alpha	IMP	NATWTLSNFC¹⁰R	Beta vulgaris subsp. vulgaris	1.21	–	0.03	Nucleus
65	A0A061E090	Vaculolar sorting receptor 3 isoform 1	VSR	VC²EC⁴PLVDGVQFR	Theobroma cacao	0.70	–	0.02	Golgi apparatus
66	731352092	Vacuolar-sorting receptor 4	VSR	YC²APDPEQDFSR	Beta vulgaris subsp. vulgaris	0.61	–	0.02	Golgi apparatus
67	A0A2N9HVW5	Mitochondrial import receptor subunit TOM40-1-like protein	TOM40	EEEKVDYFNLPC¹²PIPYEEIHR	Fagus sylvatica	–	1.81	0.02	Mitochondrion
Cellular structure
68	731336429	Actin-depolymerizing factor	ADP	TGTPAESYDDFLAVLPGNDC²⁰R	Beta vulgaris subsp. vulgaris	–	0.76	0.01	Extracellular
69	731320854	Actin-depolymerizing factor	ADP	TGGPAESYDDFLASLPESDC²⁰R	Beta vulgaris subsp. vulgaris	–	0.76	0.02	Extracellular
70	731375712	Basic 7S globulin	Bg7s	TIAPFNVC⁸VDPSTFPASR	Beta vulgaris subsp. vulgaris	10.20	5.10	0.04	Plasma Membrane
71	731317399	Profilin-3	Pfn	TGQALVIGLYDEPVTPGQC¹⁹NMIVER	Beta vulgaris subsp. vulgaris	1.29	–	0.03	Cytoplasm
72	A4GDT3	Profilin-1	Pfn	TGQALVFGIYEESVTPGQC¹⁹NMVVER	Olea europaea	1.53	–	0.01	Cytoplasm
73	731354018	Profilin	Pfn	TGQALVFGIYDEPVAPGQC¹⁹NMVVER	Beta vulgaris subsp. vulgaris	1.40	–	0.03	Cytoplasm
Signal transduction
74	731337809	Protein TAPETUM DETERMINANT 1	TPD	C¹LGFSTVQPVNPR	Beta vulgaris subsp. vulgaris	–	1.50	0.01	Plasma Membrane
75	731357482	Ubiquitin domain-containing protein DSK2b	DSK2b	SLVAQNC⁷DVPAEQQR	Beta vulgaris subsp. vulgaris	–	0.74	0.05	Nucleus
76	A0A287MC57	Ubiquitin-like domain-containing protein	Uds	LMNAYC⁶DR	Hordeum vulgare subsp. vulgare	–	0.80	0.00	Nucleus
77	731354496	Ribosome-inactivating protein PD-L1/PD-L2	Ubls	NQVEAPIRIC¹⁰GLPSTR	Beta vulgaris subsp. vulgaris	2.04	–	0.01	Cytoplasm
78	731345483	Auxin-binding protein ABP19a	ABP	GPEGYAC⁷RDPATLTTDDFVYTGFR	Beta vulgaris subsp. vulgaris	0.42	–	0.02	Cell wall
79	A0A2K1KH59	Protein kinase domain-containing protein	AMPK	C¹IPYLTR	Physcomitrium patens	0.76	–	0.04	Cytoplasm
80	731370564	Receptor-like serine/threonine-protein kinase SD1-8 isoform X1	RIPK	TAFVNDGLNLDQC¹³R	Beta vulgaris subsp. vulgaris	0.70	–	0.01	Plasma Membrane
81	731348205	Cell wall/vacuolar inhibitor of fructosidase 1	C/VIF1	FGEQAMVDAGNEAEGC¹⁶R	Beta vulgaris subsp. vulgaris	–	1.43	0.02	Vacuole
Transcription
82	731323512	Transcription elongation factor TFIIS	TFIIS	IC²NLTAEEMASEQR	Beta vulgaris subsp. vulgaris	0.62	–	0.02	Nucleus
83	731358684	Glycine-rich RNA-binding protein	RBP	C¹FVGGLAWATDDR	Beta vulgaris subsp. vulgaris	0.72	–	0.01	Cytoplasm
84	731363127	KH domain-containing protein	KHP	IGETVPGC⁸DER	Beta vulgaris subsp. vulgaris	0.76	–	0.03	Nucleus
85	731317968	RNA-binding KH domain-containing protein PEPPER	RBP	VSGVGDVEGSADAAAYC¹⁷SIR	Beta vulgaris subsp. vulgaris	–	1.24	0.04	Nucleus
86	A0A1D1Z0S0	U6 snRNA-associated Sm-like protein LSm7	–	SLGLIVC⁷R	Anthurium amnicola	–	1.26	0.00	Nucleus
87	A0A0C9S8X9	Transcribed RNA sequence	–	C¹GNVNFSFR	Wollemia nobilis	1.72	–	0.01	Cytoplasm
Biosynthesis
88	A0A0J8C157	Eukaryotic translation initiation factor 6	eIF6	NC²LPDSVVVQR	Beta vulgaris subsp. vulgaris	–	0.72	0.02	Nucleus
89	731369461	Eukaryotic translation initiation factor 3 subunit D	eIF3	C¹ELQSALDINNQR	Beta vulgaris subsp. vulgaris	–	1.27	0.03	Cytoplasm
90	1108926884	Elongation factor Tu, chloroplastic	EF-TU	MEVELIHPVAC¹¹EEGMR	Beta vulgaris subsp. vulgaris	–	0.80	0.03	Cytoplasm
Photosynthesis
91	731341540	Uclacyanin-3-like	–	AQNYVATAVQPC¹²C¹³QGISDAINNER	Beta vulgaris subsp. vulgaris	–	0.64	0.00	Plasma Membrane
92	731349464	Ferredoxin, root R-B1	Fd	LIGPDGQVSEFDAPDDC¹⁷YILDSAENEGVEIPYSC³⁴R	Beta vulgaris subsp. vulgaris	–	0.61	0.02	Chloroplast
Unknown
93	M1DDJ2	Uncharacterized protein	–	QSHMSLSFSILITELC¹⁶QR	Solanum tuberosum	1.63	–	0.00	Cytoplasm
94	B9T2R9	Clp R domain-containing protein	CLP	INSC⁴ISIEPSLR	Ricinus communis	–	1.24	0.01	Cytoplasm
95	M8AU58	Uncharacterized protein	–	MTPTTLAC⁸IGAAAETALPPTHPLR	Aegilops tauschii	–	1.53	0.04	Cytoplasm

^aProtein ID, gi number of NCBI
^bSequence with modification, the lower case letter are phosphorylation site in each peptide
^ciodoTMT salt200/control Ratio, a relative abundance of proteins at redox peptide level (200 mM NaCl treatment versus control), P-value < 0.05
^diodoTMT salt400/control Ratio, a relative abundance of proteins at redox peptide level (400 mM NaCl treatment versus control), P-value < 0.05
^eProtein location, refer to subcellular location prediction website (YLoc, LocTree3, ngLOC, TargetP)

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