SUMO E3 ligase SIZ1 negatively regulates arsenite resistance via depressing GSH biosynthesis in Arabidopsis
Tóm tắt
Arsenic is a metalloid toxic to plants, animals and human beings. Small ubiquitin-like modifier (SUMO) conjugation is involved in many biological processes in plants. However, the role of SUMOylation in regulating plant arsenic response is still unclear. In this study, we found that dysfunction of SUMO E3 ligase SIZ1 improves arsenite resistance in Arabidopsis. Overexpression of the dominant-negative SUMO E2 variant resembled the arsenite-resistant phenotype of siz1 mutant, indicating that SUMOylation plays a negative role in plant arsenite detoxification. The siz1 mutant accumulated more glutathione (GSH) than the wild type under arsenite stress, and the arsenite-resistant phenotype of siz1 was depressed by inhibiting GSH biosynthesis. The transcript levels of the genes in the GSH biosynthetic pathway were increased in the siz1 mutant comparing with the wild type in response to arsenite treatment. Taken together, our findings revealed a novel function of SIZ1 in modulating plant arsenite response through regulating the GSH-dependent detoxification.
Tài liệu tham khảo
Angulo-Bejarano PI, Puente-Rivera J, Cruz-Ortega R (2021) Metal and metalloid toxicity in plants: An overview on molecular aspects. Plants-Basel 10(4). https://doi.org/10.3390/plants10040635
Ashraf MA, Umetsu K, Ponomarenko O, Saito M, Aslam M, Antipova O, Dolgova N, Kiani CD, Nehzati S, Tanoi K, Minegishi K, Nagatsu K, Kamiya T, Fujiwara T, Luschnig C, Tanino K, Pickering I, George GN, Rahman A (2020) PIN FORMED 2 modulates the transport of Arsenite in Arabidopsis thaliana. Plant Commun 1(3):100009. https://doi.org/10.1016/j.xplc.2019.100009
Augustine RC, Vierstra RD (2018) SUMOylation: re-wiring the plant nucleus during stress and development. Curr Opin Plant Biol 45(Pt A):143–154. https://doi.org/10.1016/j.pbi.2018.06.006
Chao DY, Chen Y, Chen J, Shi S, Chen Z, Wang C, Danku JM, Zhao FJ, Salt DE (2014) Genome-wide association mapping identifies a new arsenate reductase enzyme critical for limiting arsenic accumulation in plants. PLoS Biol 12(12):e1002009. https://doi.org/10.1371/journal.pbio.1002009
Dong JS, Ma GJ, Sui LQ, Wei MW, Satheesh V, Zhang RY, Ge SH, Li JK, Zhang TE, Wittwer C, Jessen HJ, Zhang HM, An GY, Chao DY, Liu D, Lei MG (2019) Inositol pyrophosphate InsP (8) acts as an intracellular phosphate signal in Arabidopsis. Mol Plant 12(11):1463–1473. https://doi.org/10.1016/j.molp.2019.08.002
Hong Y, Wang Z, Liu X, Yao J, Kong X, Shi H, Zhu J-K (2020) Two chloroplast proteins negatively regulate plant drought resistance through separate pathways. Plant Physiol 182(2):1007–1021. https://doi.org/10.1104/pp.19.01106
Kong X, Hong Y, Hsu YF, Huang H, Liu X, Song Z, Zhu JK (2020) SIZ1-mediated SUMOylation of ROS1 enhances its stability and positively regulates active DNA demethylation in Arabidopsis. Mol Plant 13(12):1816–1824. https://doi.org/10.1016/j.molp.2020.09.010
LeBlanc MS, McKinney EC, Meagher RB, Smith AP (2013) Hijacking membrane transporters for arsenic phytoextraction. J Biotechnol 163(1):1–9. https://doi.org/10.1016/j.jbiotec.2012.10.013
Lee BR, Koprivova A, Kopriva S (2011) The key enzyme of sulfate assimilation, adenosine 5 '-phosphosulfate reductase, is regulated by HY5 in Arabidopsis. Plant J 67(6):1042–1054. https://doi.org/10.1111/j.1365-313X.2011.04656.x
Lin XL, Niu D, Hu ZL, Kim DH, Jin YH, Cai B, Liu P, Miura K, Yun DJ, Kim WY, Lin RC, Jin JB (2016) An Arabidopsis SUMO E3 Ligase, SIZ1. Negatively Regulates Photomorphogenesis by Promoting COP1 Activity Plos Genetics 12(4). https://doi.org/10.1371/journal.pgen.1006016
Miura K, Lee J, Miura T, Hasegawa PM (2010) SIZ1 controls cell growth and plant development in Arabidopsis through salicylic acid. Plant Cell Physiol 51(1):103–113. https://doi.org/10.1093/pcp/pcp171
Miura K, Rus A, Sharkhuu A, Yokoi S, Karthikeyan AS, Raghothama KG, Baek D, Koo YD, Jin JB, Bressan RA, Yun DJ, Hasegawa PM (2005) The Arabidopsis SUMO E3 ligase SIZ1 controls phosphate deficiency responses. Proc Natl Acad Sci U S A 102(21):7760–7765. https://doi.org/10.1073/pnas.0500778102
Morrell R, Sadanandom A (2019) Dealing with stress: a review of plant SUMO proteases. Front Plant Sci 10. https://doi.org/10.3389/fpls.2019.01122
Navarro C, Mateo-Elizalde C, Mohan TC, Sanchez-Bermejo E, Urrutia O, Fernandez-Muniz MN, Garcia-Mina JM, Munoz R, Paz-Ares J, Castrillo G, Leyva A (2021) Arsenite provides a selective signal that coordinates arsenate uptake and detoxification through the regulation of PHR1 stability in Arabidopsis. Mol Plant 14(9):1489–1507. https://doi.org/10.1016/j.molp.2021.05.020
Schnaubelt D, Queval G, Dong YP, Diaz-Vivancos P, Makgopa ME, Howell G, De Simone A, Bai J, Hannah MA, Foyer CH (2015) Low glutathione regulates gene expression and the redox potentials of the nucleus and cytosol in Arabidopsis thaliana. Plant Cell and Environment 38(2):266–279. https://doi.org/10.1111/pce.12252
Tomanov K, Hardtke C, Budhiraja R, Hermkes R, Coupland G, Bachmair A (2013) Small ubiquitin-like modifier conjugating enzyme with active site mutation acts as dominant negative inhibitor of SUMO conjugation in arabidopsis(F). J Integr Plant Biol 55(1):75–82. https://doi.org/10.1111/jipb.12016
Tripathi RD, Srivastava S, Mishra S, Singh N, Tuli R, Gupta DK, Maathuis FJM (2007) Arsenic hazards: strategies for tolerance and remediation by plants. Trends Biotechnol 25(4):158–165. https://doi.org/10.1016/j.tibtech.2007.02.003
Wang Z, Hong Y, Zhu G, Li Y, Niu Q, Yao J, Hua K, Bai J, Zhu Y, Shi H, Huang S, Zhu JK (2020) Loss of salt tolerance during tomato domestication conferred by variation in a Na(+) /K(+) transporter. EMBO J: e103256
Yadav SK (2010) Heavy metals toxicity in plants: An overview on the role of glutathione and phytochelatins in heavy metal stress tolerance of plants. S Afr J Bot 76(2):167–179. https://doi.org/10.1016/j.sajb.2009.10.007
Zhao FJ, McGrath SP, Meharg AA (2010) Arsenic as a food chain contaminant: mechanisms of plant uptake and metabolism and mitigation strategies. Annu Rev Plant Biol 61(61):535–559. https://doi.org/10.1146/annurev-arplant-042809-112152