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Current Proteomics

Editor-in-Chief

ISSN (Print): 1570-1646
ISSN (Online): 1875-6247

Research Article

Quantitative Proteomics Reveals SOS2-Related Proteins in Arabidopsis Under Salt Stress

Author(s): Xiang Yu, Xiaoyun Zhao, Yongqing Yang and Zhen Li*

Volume 19, Issue 2, 2022

Published on: 13 April, 2021

Page: [142 - 152] Pages: 11

DOI: 10.2174/1570164618666210413105907

Price: $65

Abstract

Background: Soil salinity is a major issue that seriously affects plant growth and cultivated land utilization. Salt tolerance is one of the most fundamental biological processes that ensures plant’s survival. SOS2 is one of the most important components of the Salt Overly Sensitive (SOS) signaling pathway, which maintains plant ion homeostasis under salt stress. The SOS2-related signaling pathways remain incompletely exploited especially at the proteomics level.

Objective: In this paper, proteins potentially interacting with and regulated by SOS2 in Arabidopsis were identified.

Methods: The proteomes of Arabidopsis Wild Type (WT) and SOS2-deficient mutant (sos2-2) exposed to 100 mM NaCl for 6 h were compared, proteins were identified using data-independent acquisition- based quantitative proteomics strategy.

Results: A total of 7470 proteins were identified and quantified, 372 Differentially Expressed Proteins (DEP) were detected between WT and sos2-2 mutant under normal condition and 179 DEPs were identified under salt treatment. Functional analysis showed that the DEPs were mainly involved in protein binding and catalytic activity. Among the DEPs under salt stress, the protein expressions of AVP1, Photosystem II reaction center protein A, B, C, and stress-responsive protein (KIN2) were significantly up-regulated. LHCA1, LHCA2, LHCA4, ATPD and ATPE were significantly down-regulated. These proteins were involved in biological processes including: stress response, photosynthesis, transport and heat shock.

Conclusion: These results revealed complexity of the functions of SOS2 in maintaining intracellular homeostasis, in addition to its function in sodium homeostasis. Plant salt resistance is not independent but closely related to metabolic processes including photosystem, ATP synthase, transport and other stress resistances.

Keywords: Quantitative proteomics, salt tolerance, SOS2, homeostasis, photosynthesis, heat shock.

Graphical Abstract
[1]
Mir, M.A.; John, R.; Alyemeni, M.N.; Alam, P.; Ahmad, P. Jasmonic acid ameliorates alkaline stress by improving growth performance, ascorbate glutathione cycle and glyoxylase system in maize seedlings. Sci. Rep., 2018, 8(1), 2831-2831.
[http://dx.doi.org/10.1038/s41598-018-21097-3] [PMID: 29434207]
[2]
Yang, Y.; Zhang, C.; Tang, R.J.; Xu, H.X.; Lan, W.Z.; Zhao, F.; Luan, S. Calcineurin B-Like Proteins CBL4 and CBL10 Mediate Two Independent Salt Tolerance Pathways in Arabidopsis. Int. J. Mol. Sci., 2019, 20(10), E2421.
[http://dx.doi.org/10.3390/ijms20102421] [PMID: 31100786]
[3]
Gong, X.; Shi, S.; Dou, F.; Song, Y.; Ma, F. Exogenous Melatonin Alleviates Alkaline Stress in Malus hupehensis Rehd. by Regulating the Biosynthesis of Polyamines. Molecules, 2017, 22(9), 1542.
[http://dx.doi.org/10.3390/molecules22091542] [PMID: 28902159]
[4]
Yi, C.; Yao, K.; Cai, S.; Li, H.; Zhou, J.; Xia, X.; Shi, K.; Yu, J.; Foyer, C.H.; Zhou, Y. High atmospheric carbon dioxide-dependent alleviation of salt stress is linked to respiratory burst oxidase 1 (RBOH1)-dependent H2O2 production in tomato (Solanum lycopersicum). J. Exp. Bot., 2015, 66(22), 7391-7404.
[http://dx.doi.org/10.1093/jxb/erv435] [PMID: 26417022]
[5]
Yang, Y.; Guo, Y. Unraveling salt stress signaling in plants. J. Integr. Plant Biol., 2018, 60(9), 796-804.
[http://dx.doi.org/10.1111/jipb.12689] [PMID: 29905393]
[6]
Ishikawa, S.; Hayashi, S.; Abe, T.; Igura, M.; Kuramata, M.; Tanikawa, H.; Iino, M.; Saito, T.; Ono, Y.; Ishikawa, T.; Fujimura, S.; Goto, A.; Takagi, H. Low-cesium rice: mutation in OsSOS2 reduces radiocesium in rice grains. Sci. Rep., 2017, 7(1), 2432.
[http://dx.doi.org/10.1038/s41598-017-02243-9] [PMID: 28546542]
[7]
Yang, Z.; Wang, C.; Xue, Y.; Liu, X.; Chen, S.; Song, C.; Yang, Y.; Guo, Y. Calcium-activated 14-3-3 proteins as a molecular switch in salt stress tolerance. Nat. Commun., 2019, 10(1), 1199.
[http://dx.doi.org/10.1038/s41467-019-09181-2] [PMID: 30867421]
[8]
Nutan, K.K.; Kumar, G.; Singla-Pareek, S.L.; Pareek, A. A Salt Overly Sensitive Pathway Member from Brassica juncea BjSOS3 Can Functionally Complement ΔAtSOS3 in Arabidopsis. Curr. Genomics, 2018, 19(1), 60-69.
[PMID: 29491733]
[9]
Ma, L.; Ye, J.; Yang, Y.; Lin, H.; Yue, L.; Luo, J.; Long, Y.; Fu, H.; Liu, X.; Zhang, Y. J. D. C. The SOS2-SCaBP8 Complex Generates and Fine-Tunes an AtANN4-Dependent Calcium Signature under Salt Stress., 2019, 48(5), 697-709.e5.
[http://dx.doi.org/10.1016/j.devcel.2019.02.010]
[10]
Verslues, P.E.; Batelli, G.; Grillo, S.; Agius, F.; Kim, Y-S.; Zhu, J.; Agarwal, M.; Katiyar-Agarwal, S.; Zhu, J-K. Interaction of SOS2 with Nucleoside Diphosphate Kinase 2 and Catalases Reveals a Point of Connection between Salt Stress and H<sub>2</sub>O<sub>2</sub> Signaling in <em>Arabidopsis thaliana</em&gt. Mol. Cell. Biol., 2007, 27(22), 7771.
[http://dx.doi.org/10.1128/MCB.00429-07] [PMID: 17785451]
[11]
Ji, H.; Pardo, J.M.; Batelli, G.; Van Oosten, M.J.; Bressan, R.A.; Li, X. The Salt Overly Sensitive (SOS) pathway: established and emerging roles. Mol. Plant, 2013, 6(2), 275-286.
[http://dx.doi.org/10.1093/mp/sst017] [PMID: 23355543]
[12]
Jia, T.; Wang, J.; Chang, W.; Fan, X.; Sui, X.; Song, F. J. I. J. M. Proteomics Analysis of E. angustifolia Seedlings Inoculated with Arbuscular Mycorrhizal Fungi under Salt Stress. 2019, 20(3)
[13]
Singh, R.P.; Runthala, A.; Khan, S.; Jha, P.N. Quantitative proteomics analysis reveals the tolerance of wheat to salt stress in response to Enterobacter cloacae SBP-8. PLoS One, 2017, 12(9), e0183513.
[http://dx.doi.org/10.1371/journal.pone.0183513] [PMID: 28877183]
[14]
Yu, B.; Li, J.; Koh, J.; Dufresne, C.; Yang, N.; Qi, S.; Zhang, Y.; Ma, C.; Duong, B.V.; Chen, S.; Li, H. Quantitative proteomics and phosphoproteomics of sugar beet monosomic addition line M14 in response to salt stress. J. Proteomics, 2016, 143, 286-297.
[http://dx.doi.org/10.1016/j.jprot.2016.04.011] [PMID: 27233743]
[15]
Harris, Y. J. B. Y. N. S.; Botany, M. K. D. J. J. o. E Comparative proteomic analysis of NaCl stress-responsive proteins in Arabidopsis roots. 2007, 8(13), 3591-3607.
[16]
Du, C.-X.; Fan, H.-F.; Guo, S.-R.; Tezuka, T.; Li, J. Proteomic analysis of cucumber seedling roots subjected to salt stress. phytochemistry, 2010, 71(13), 1450-1459.
[17]
Koopmans, F.; Ho, J.T.C.; Smit, A.B.; Li, K.W. Comparative Analyses of Data Independent Acquisition Mass Spectrometric Approaches: DIA, WiSIM-DIA, and Untargeted DIA. Proteomics, 2018, 18(1), 1700304.
[http://dx.doi.org/10.1002/pmic.201700304] [PMID: 29134766]
[18]
Poulos, R.C.; Hains, P.G.; Shah, R.; Lucas, N.; Xavier, D.; Manda, S.S.; Anees, A.; Koh, J.M.S.; Mahboob, S.; Wittman, M.; Williams, S.G.; Sykes, E.K.; Hecker, M.; Dausmann, M.; Wouters, M.A.; Ashman, K.; Yang, J.; Wild, P.J.; deFazio, A.; Balleine, R.L.; Tully, B.; Aebersold, R.; Speed, T.P.; Liu, Y.; Reddel, R.R.; Robinson, P.J.; Zhong, Q. Strategies to enable large-scale proteomics for reproducible research. Nat. Commun., 2020, 11(1), 3793.
[http://dx.doi.org/10.1038/s41467-020-17641-3] [PMID: 32732981]
[19]
Bekker-Jensen, D. B.; Bernhardt, O. M.; Hogrebe, A.; Martinez- Val, A.; Olsen, J. V. J. N. C. Rapid and site-specific deep phosphoproteome profiling by data-independent acquisition without the need for spectral libraries. Nat. Commun., 2020, 11(1), 1-12.
[http://dx.doi.org/10.1038/s41467-020-14609-1]
[20]
Distler, U.; Kuharev, J. R.; Navarro, P.; Tenzer, S. J. N. P. Label-free quantification in ion mobility–enhanced data-independent acquisition proteomics. Nat. Protoc., 2016, 11(4), 795-812.
[http://dx.doi.org/10.1038/nprot.2016.042]
[21]
Tsugawa, H.; Cajka, T.; Kind, T.; Ma, Y.; Higgins, B.; Ikeda, K.; Kanazawa, M.; VanderGheynst, J.; Fiehn, O.; Arita, M. MS- DIAL: data-independent MS/MS deconvolution for comprehensive metabolome analysis. Nat. Methods, 2015, 12(6), 523-526.
[http://dx.doi.org/10.1038/nmeth.3393] [PMID: 25938372]
[22]
Bekker-Jensen, D.B.; Bernhardt, O.M.; Hogrebe, A.; Martinez- Val, A.; Verbeke, L.; Gandhi, T.; Kelstrup, C.D.; Reiter, L.; Olsen, J.V. Rapid and site-specific deep phosphoproteome profiling by data-independent acquisition without the need for spectral libraries. Nat. Commun., 2020, 11(1), 787.
[http://dx.doi.org/10.1038/s41467-020-14609-1] [PMID: 32034161]
[23]
Jiping, Liu.; Ishitani, America, M. J. P. o. t. N. A. o. S. o. t. U. S. o. The Arabidopsis thaliana SOS2 gene encodes a protein kinase that is required for salt tolerance. 2000.
[24]
Yastreb, T. O.; Kolupaev, Y. E.; Karpets, Y. V.; Dmitriev, A. P. J. R. J. o. P. P. Effect of nitric oxide donor on salt resistance of Arabidopsis jin1 mutants and wild-type plants. Russian J. Plant Physiol., 2017, 64, 207-214.
[http://dx.doi.org/10.1134/S1021443717010186]
[25]
Xiaoyun, Zhao.; Xue, Bai.; Caifu, Jiang.; Zhen, Sciences, L. J. I. J. o. M. Phosphoproteomic Analysis of Two Contrasting Maize Inbred Lines Provides Insights into the Mechanism of Salt-Stress Tolerance 2019.
[26]
Wiśniewski, J.R.; Zougman, A.; Nagaraj, N.; Mann, M. Universal sample preparation method for proteome analysis. Nat. Methods, 2009, 6(5), 359-362.
[http://dx.doi.org/10.1038/nmeth.1322] [PMID: 19377485]
[27]
Qi, J.; Zhao, X.; Li, Z. J. I. J. o. M. E. iTRAQ-based quantitative proteomic analysis of the arabidopsis mutant opr3-1 in response to exogenous MeJA. 2020, 21(2), 571.
[28]
Bressan, M.; Bassi, R.; Dall'Osto, L. J. P. R. Loss of LHCI system affects LHCII re-distribution between thylakoid domains upon state transitions., 2018, 135(1), 251-261.
[http://dx.doi.org/10.1007/s11120-017-0444-1]
[29]
Ihalainen, J.A.; Klimmek, F.; Ganeteg, U.; van Stokkum, I.H.M.; van Grondelle, R.; Jansson, S.; Dekker, J.P. Excitation energy trapping in photosystem I complexes depleted in Lhca1 and Lhca4. FEBS Lett., 2005, 579(21), 4787-4791.
[http://dx.doi.org/10.1016/j.febslet.2005.06.091] [PMID: 16098971]
[30]
Hey, D.; Grimm, B. ONE-HELIX PROTEIN1 and 2 Form Heterodimers to Bind Chlorophyll in Photosystem II Biogenesis. Plant Physiol., 2020, 183(1), 179-193.
[http://dx.doi.org/10.1104/pp.19.01304] [PMID: 32071152]
[31]
Li, Y.; Liu, B.; Zhang, J.; Kong, F.; Zhang, L.; Meng, H.; Li, W.; Rochaix, J.D.; Li, D.; Peng, L. OHP1, OHP2, and HCF244 Form a Transient Functional Complex with the Photosystem II Reaction Center. Plant Physiol., 2019, 179(1), 195-208.
[http://dx.doi.org/10.1104/pp.18.01231] [PMID: 30397023]
[32]
Hey, D.; Grimm, B. ONE-HELIX PROTEIN2 (OHP2) Is Required for the Stability of OHP1 and Assembly Factor HCF244 and Is Functionally Linked to PSII Biogenesis. Plant Physiol., 2018, 177(4), 1453-1472.
[http://dx.doi.org/10.1104/pp.18.00540] [PMID: 29930106]
[33]
Tang, R.J.; Liu, H.; Bao, Y.; Lv, Q.D.; Yang, L.; Zhang, H.X. The woody plant poplar has a functionally conserved salt overly sensitive pathway in response to salinity stress. Plant Mol. Biol., 2010, 74(4-5), 367-380.
[http://dx.doi.org/10.1007/s11103-010-9680-x] [PMID: 20803312]
[34]
Cheng, C.; Zhong, Y.; Wang, Q.; Cai, Z.; Wang, D.; Li, C. Genome-wide identification and gene expression analysis of SOS family genes in tuber mustard (Brassica juncea var. tumida). PLoS One, 2019, 14(11), e0224672.
[http://dx.doi.org/10.1371/journal.pone.0224672] [PMID: 31710609]
[35]
Oh, D.H.; Dassanayake, M.; Haas, J.S.; Kropornika, A.; Wright, C.; d’Urzo, M.P.; Hong, H.; Ali, S.; Hernandez, A.; Lambert, G.M.; Inan, G.; Galbraith, D.W.; Bressan, R.A.; Yun, D.J.; Zhu, J.K.; Cheeseman, J.M.; Bohnert, H.J. Genome structures and halophyte-specific gene expression of the extremophile Thellungiella parvula in comparison with Thellungiella salsuginea (Thellungiella halophila) and Arabidopsis. Plant Physiol., 2010, 154(3), 1040-1052.
[http://dx.doi.org/10.1104/pp.110.163923] [PMID: 20833729]
[36]
Yang, Y.; Tang, R.J.; Jiang, C.M.; Li, B.; Kang, T.; Liu, H.; Zhao, N.; Ma, X.J.; Yang, L.; Chen, S.L.; Zhang, H.X. Overexpression of the PtSOS2 gene improves tolerance to salt stress in transgenic poplar plants. Plant Biotechnol. J., 2015, 13(7), 962-973.
[http://dx.doi.org/10.1111/pbi.12335] [PMID: 25641517]
[37]
Sui, N.; Yang, Z.; Liu, M.; Wang, B. Identification and transcriptomic profiling of genes involved in increasing sugar content during salt stress in sweet sorghum leaves. BMC Genomics, 2015, 16, 534.
[http://dx.doi.org/10.1186/s12864-015-1760-5] [PMID: 26186930]
[38]
Pei, L.; Peng, L.; Wan, X.; Xiong, J.; Liu, Z.; Li, X.; Yang, Y.; Wang, J. J. I. j. o. m. e. Expression Pattern and Function Analysis of AtPPRT1, a Novel Negative Regulator in ABA and Drought Stress Responses in Arabidopsis., 2019, 20(2)
[http://dx.doi.org/10.3390/ijms20020394]
[39]
Mingxue, C.; Jiaojiao, L.; Jingyu, Z.; Sufen, S.; Cuina, L.; Yingjie, G.; Suqiao, Z. AtCaM4 interacts with a Sec14-like protein, PATL1, to regulate freezing tolerance in Arabidopsis in a CBF-independent manner. J. Experimental Botany, 2018, 69(21), 5241–5253.
[40]
Peng, P.H.; Lin, C.H.; Tsai, H.W.; Lin, T.Y. Cold response in Phalaenopsis aphrodite and characterization of PaCBF1 and PaICE1. Plant Cell Physiol., 2014, 55(9), 1623-1635.
[http://dx.doi.org/10.1093/pcp/pcu093] [PMID: 24974386]
[41]
Zhang, J.; Jia, W.; Yang, J.; Ismail, A.M.J.F.C.R. Role of ABA in integrating plant responses to drought and salt stresses. Field Crops Res., 2006, 97(1), 111-119.
[http://dx.doi.org/10.1016/j.fcr.2005.08.018]
[42]
Jun, LIU; Ming-Yi, JIANG; Yi-Feng, ZHOU; Ismail, A.M.J.F.C.R. Production of polyamines is enhanced by endogenous abscisic acid in maize seedlings subjected to salt stress. 2005.
[43]
Christian, Zörb; Christoph-Martin, Geilfus; Karl, H; Mühling, Jutta L.-M. The influence of salt stress on ABA and auxin concentrations in two maize cultivars differing in salt resistance. J. Plant Physiol., 2013, 170(2), 220-224.
[44]
Luo, Ming; Yu-Yuan, Wang; Xuncheng, Liu; Songguang, Yang; Qing, Lu; Yuhai, Cui; Botany, K. W. J. J. o. E HD2C interacts with HDA6 and is involved in ABA and salt stress response in Arabidopsis. 2012, 63(8), 3297-3306.
[45]
Schilling, R.K.; Tester, M.; Marschner, P.; Plett, D.C.; Roy, S.J. AVP1: One Protein, Many Roles. Trends Plant Sci., 2017, 22(2), 154-162.
[http://dx.doi.org/10.1016/j.tplants.2016.11.012] [PMID: 27989652]
[46]
Wang, Q.; Guan, C.; Wang, P.; Ma, Q.; Bao, A-K.; Zhang, J-L.; Wang, S-M. The Effect of AtHKT1;1 or AtSOS1 Mutation on the Expressions of Na⁺ or K⁺ Transporter Genes and Ion Homeostasis in Arabidopsis thaliana under Salt Stress. Int. J. Mol. Sci., 2019, 20(5), 1085.
[http://dx.doi.org/10.3390/ijms20051085] [PMID: 30832374]
[47]
Beere, H.M.; Wolf, B.B.; Cain, K.; Mosser, D.D.; Mahboubi, A.; Kuwana, T.; Tailor, P.; Morimoto, R.I.; Cohen, G.M.; Green, D.R. Heat-shock protein 70 inhibits apoptosis by preventing recruitment of procaspase-9 to the Apaf-1 apoptosome. Nat. Cell Biol., 2000, 2(8), 469-475.
[http://dx.doi.org/10.1038/35019501] [PMID: 10934466]
[48]
Sun, W.; Van Montagu, M.; Verbruggen, N. Small heat shock proteins and stress tolerance in plants. Biochimica et Biophysica Acta (BBA) -. Gene Structure and Expression, 2002, 1577(1), 1-9.
[http://dx.doi.org/10.1016/S0167-4781(02)00417-7]
[49]
Al-Whaibi, M. H. Plant heat-shock proteins: A mini review. Journal of King Saud University - Science, 2011, 23(2), 139-150.
[50]
Iwata, Y.; Iida, T.; Matsunami, T.; Yamada, Y.; Mishiba, K.I.; Ogawa, T.; Kurata, T.; Koizumi, N. Constitutive BiP protein accumulation in Arabidopsis mutants defective in a gene encoding chloroplast-resident stearoyl-acyl carrier protein desaturase. Genes Cells, 2018, 23(6), 456-465.
[http://dx.doi.org/10.1111/gtc.12585] [PMID: 29688606]
[51]
Zhang, R.; Chen, H.; Duan, M.; Zhu, F.; Wen, J.; Dong, J.; Wang, T. Medicago falcata MfSTMIR, an E3 ligase of endoplasmic reticulum-associated degradation, is involved in salt stress response. Plant J., 2019, 98(4), 680-696.
[http://dx.doi.org/10.1111/tpj.14265] [PMID: 30712282]
[52]
Sato, R.; Maeshima, M. The ER-localized aquaporin SIP2;1 is involved in pollen germination and pollen tube elongation in Arabidopsis thaliana. Plant Mol. Biol., 2019, 100(3), 335-349.
[http://dx.doi.org/10.1007/s11103-019-00865-3] [PMID: 30963359]
[53]
Liu, J.X.; Howell, S.H. Endoplasmic reticulum protein quality control and its relationship to environmental stress responses in plants. Plant Cell, 2010, 22(9), 2930-2942.
[http://dx.doi.org/10.1105/tpc.110.078154] [PMID: 20876830]
[54]
Ron, D.; Walter, P. Signal integration in the endoplasmic reticulum unfolded protein response. Nat. Rev. Mol. Cell Biol., 2007, 8(7), 519-529.
[http://dx.doi.org/10.1038/nrm2199] [PMID: 17565364]

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