The Expressions of Small Ubiquitin-like Modifier (SUMO) Related Genes Under Metal (Cu, Zn and Fe) Stress in Arabidopsis thaliana

Abstract

Aim of this work was to investigate effects of Cu, Zn and Fe treatments on small ubiquitin-like modifier (SUMO) machinery of Arabidopsis thaliana. SUMO is a 100-115 amino acid post-translational modifier that can regulate stability, activity or sub-cellular localization of target proteins. A. thaliana plants were treated with 50 µM Cu, 700 µM Zn and 400 µM Fe for 7 d and then expressions of genes related to SUMOylation and deSUMOylation of target proteins were measured with qRT-PCR. Only Cu treatment was able to induce genes related to SUMOylation (SUM3, SAE2, SIZ1) of target proteins, while all of the three metal used in this study was effective in inducing a deSUMOylation related gene. Results of this study indicated that deSUMOylation of proteins might be a part of plant response to metal toxicity.

Keywords

• Arabidopsis thaliana,deSUMOylation,metal toxicity,small ubiquitin-like modifier (SUMO),SUMOylation

References

1. 1. Osakabe Y, Osakabe K, Shinozaki K, Tran LSP. 2014. Response of plants to water stress. Frontiers in Plant Science; 5: 86.
2. 2. Filichkin S, Priest HD, Megraw M, Mockler TC. 2015. Alternative splicing in plants: directing traffic at the crossroads of adaptation and environmental stress. Current Opinion in Plant Biology; 24: 125-135.
3. 3. Waszczak C, Akter S, Jacques S, Huang J, Messens J, Van Breusegem F. 2015. Oxidative post-translational modifications of cysteine residues in plant signal transduction. Journal of Experimental Botany; 66(10): 2923-2934.
4. 4. Mann M, Jensen ON. 2003. Proteomic analysis of post-translational modifications. Nature Biotechnology; 21(3): 255.
5. 5. Park HJ, Kim WY, Park HC, Lee SY, Bohnert HJ, Yun DJ 2011. SUMO and SUMOylation in plants, Molecules and Cells; 32(4):305.
6. 6. Hanania U, Furman‐Matarasso N, Ron M, Avni A. 1999. Isolation of a novel SUMO protein from tomato that suppresses EIX‐induced cell death. The Plant Journal; 19(5): 533-541.
7. 7. Castaño-Miquel L, Mas A, Teixeira I, Seguí J, Perearnau A, Thampi BN, Coca M. 2017. SUMOylation inhibition mediated by disruption of SUMO E1-E2 interactions confers plant susceptibility to necrotrophic fungal pathogens. Molecular Plant; 10(5): 709-720.
8. 8. Castro PH, Couto D, Freitas S, Verde N, Macho AP, Huguet S, Azevedo H. 2016. SUMO proteases ULP1c and ULP1d are required for development and osmotic stress responses in Arabidopsis thaliana. Plant Molecular Biology; 92(1-2): 143-159.

9. 9. Miura K, Hasegawa PM. 2010. SUMOylation and other ubiquitin-like post-translational modifications in plants. Trends in Cell Biology; 20(4): 223-232.
10. 10. Yates G, Srivastava AK, Sadanandom A. 2016. SUMO proteases: uncovering the roles of deSUMOylation in plants. Journal of Experimental Botany; 67(9): 2541-2548.
11. 11. Castro PH, Bachmair A, Bejarano ER, Coupland G, Lois L M, Sadanandom A, Azevedo H. 2018. Revised nomenclature and functional overview of the ULP gene family of plant deSUMOylating proteases. Journal of Experimental Botany; 69(19): 4505-4509.
12. 12. Vierstra, R. D. (2003). The ubiquitin/26S proteasome pathway, the complex last chapter in the life of many plant proteins. Trends in plant science, 8(3): 135-142.
13. 13. Li Y, Wang G, Xu Z, Li J, Sun M, Guo J, Ji W. 2017. Organization and regulation of soybean SUMOylation system under abiotic stress conditions. Frontiers in Plant Science; 8: 1458.
14. 14. Miura K, Jin JB, Lee J, Yoo CY, Stirm V, Miura T, Hasegawa PM. 2007. SIZ1-mediated sumoylation of ICE1 controls CBF3/DREB1A expression and freezing tolerance in Arabidopsis. The Plant Cell; 19(4): 1403-1414.
15. 15. Hasan M, Cheng Y, Kanwar MK, Chu XY, Ahammed GJ, Qi ZY. 2017. Responses of plant proteins to heavy metal stress—a review. Frontiers in Plant Science; 8: 1492.
16. 16. Jalmi SK, Bhagat PK, Verma D, Noryang S, Tayyeba S, Singh K, Sinha AK. 2018. Traversing the links between heavy metal stress and plant signaling. Frontiers in Plant Science; 9: 12.
17. 17. Nagajyoti PC, Lee KD, Sreekanth TVM. 2010. Heavy metals, occurrence and toxicity for plants: a review. Environmental Chemistry Letters; 8(3): 199-216.
18. 18. Thakur S, Singh L, Ab Wahid Z, Siddiqui MF, Atnaw SM, Din MFM. 2016. Plant-driven removal of heavy metals from soil: uptake, translocation, tolerance mechanism, challenges, and future perspectives. Environmental Monitoring and Assessment; 188(4): 206.
19. 19. Sharma SS, Dietz KJ. 2009. The relationship between metal toxicity and cellular redox imbalance. Trends in Plant Science; 14(1): 43-50.
20. 20. Gamborg OL, Murashige T, Thorpe TA, Vasil IK. 1976. Plant tissue culture media. In vitro;12(7): 473-478.
21. 21. Kumar V, Vogelsang L, Seidel T, Schmidt R, Weber M, Reichelt M, Dietz KJ. 2019. Interference between arsenic‐ induced toxicity and hypoxia. Plant, Cell & environment; 42(2): 574-590.
22. 22. Milner MJ, Seamon J, Craft E, Kochian LV. 2013. Transport properties of members of the ZIP family in plants and their role in Zn and Mn homeostasis. Journal of Experimental Botany; 64(1): 369-381.
23. 23. Sanz A, Pike S, Khan MA, Carrió-Seguí À, Mendoza-Cózatl DG, Peñarrubia L, Gassmann W. 2019. Copper uptake mechanism of Arabidopsis thaliana high-affinity COPT transporters. Protoplasma; 256(1): 161-170.
24. 24. Ozgur R, Uzilday B, Turkan I, Sekmen AH. 2017. The effects of melatonin on transcriptional profile of unfolded protein response genes under endoplasmic reticulum stress in Arabidopsis thaliana. Plant Molecular Biology Reporter; 35(2): 188-202.
25. 25. Guo Q, Zhang J, Gao Q, Xing S, Li F, Wang W. 2008. Drought tolerance through overexpression of monoubiquitin in transgenic tobacco. Journal of Plant Physiology; 165(16): 1745-1755.
26. 26. Kurepa J, Walker JM, Smalle J, Gosink MM, Davis SJ, Durham TL, Vierstra RD. 2003. The small ubiquitin-like modifier (SUMO) protein modification system in Arabidopsis accumulation of sumo1 and -2 conjugates is increased by stress. Journal of Biological Chemistry; 278(9): 6862-6872.
27. 27. Nigam N, Singh A, Sahi C, Chandramouli A, Grover A. 2008. SUMO-conjugating enzyme (Sce) and FK506-binding protein (FKBP) encoding rice (Oryza sativa L.) genes: genome-wide analysis, expression studies and evidence for their involvement in abiotic stress response. Molecular Genetics and Genomics; 279(4): 371-383.
28. 28. Lara-Ávila JP, Isordia-Jasso MI, Castillo-Collazo R, Simpson J, Alpuche-Solís ÁG. 2012. Gene expression analysis during interaction of tomato and related wild species with Clavibacter michiganensis subsp. michiganensis. Plant Molecular Biology Reporter; 30(2): 498-511.
29. 29. Ishida T, Yoshimura M, Miura K, Sugimoto K. 2012. MMS21/HPY2 and SIZ1, two Arabidopsis SUMO E3 ligases, have distinct functions in development. PloS One; 7(10).
30. 30. Chen CC, Chen YY, Tang IC, Liang HM, Lai CC, Chiou J M, Yeh KC. 2011. Arabidopsis SUMO E3 ligase SIZ1 is involved in excess copper tolerance. Plant Physiology; 156(4): 2225-2234.