Small ubiquitin-like modifiers E3 ligases in plant stress
Shantwana Ghimire
A , Md Mahadi Hasan A and Xiang-Wen Fang A *
A
Abstract
Plants regularly encounter various environmental stresses such as salt, drought, cold, heat, heavy metals and pathogens, leading to changes in their proteome. Of these, a post-translational modification, SUMOylation is particularly significant for its extensive involvement in regulating various plant molecular processes to counteract these external stressors. Small ubiquitin-like modifiers (SUMO) protein modification significantly contributes to various plant functions, encompassing growth, development and response to environmental stresses. The SUMO system has a limited number of ligases even in fully sequenced plant genomes but SUMO E3 ligases are pivotal in recognising substrates during the process of SUMOylation. E3 ligases play pivotal roles in numerous biological and developmental processes in plants, including DNA repair, photomorphogenesis, phytohormone signalling and responses to abiotic and biotic stress. A considerable number of targets for E3 ligases are proteins implicated in reactions to abiotic and biotic stressors. This review sheds light on how plants respond to environmental stresses by focusing on recent findings on the role of SUMO E3 ligases, contributing to a better understanding of how plants react at a molecular level to such stressors.
Keywords: abiotic stress, biotic stress, hormonal signalling, plant response, small ubiquitin-like modifiers, SUMO E3 ligase, SUMO targets, SUMOylation.
References
Andrews EA, Palecek J, Sergeant J, Taylor E, Lehmann AR, Watts FZ (2005) Nse2, a component of the Smc5-6 complex, is a SUMO ligase required for the response to DNA damage. Molecular and Cellular Biology 25, 185-196.
| Crossref | Google Scholar | PubMed |
Augustine RC, Vierstra RD (2018) SUMOylation: re-wiring the plant nucleus during stress and development. Current Opinion in Plant Biology 45, 143-154.
| Crossref | Google Scholar | PubMed |
Bari R, Pant BD, Stitt M, Scheible W-R (2006) PHO2, microRNA399, and PHR1 define a phosphate-signaling pathway in plants. Plant Physiology 141, 988-999.
| Crossref | Google Scholar | PubMed |
Cai B, Kong X, Zhong C, Sun S, Zhou XF, Jin YH, Wang Y, Li X, Zhu Z, Jin JB (2017) SUMO E3 Ligases GmSIZ1a and GmSIZ1b regulate vegetative growth in soybean. Journal of Integrative Plant Biology 59, 2-14.
| Crossref | Google Scholar | PubMed |
Cappadocia L, Lima CD (2018) Ubiquitin-like protein conjugation: structures, chemistry, and mechanism. Chemical Reviews 118, 889-918.
| Crossref | Google Scholar | PubMed |
Castro PH, Tavares RM, Bejarano ER, Azevedo H (2012) SUMO, a heavyweight player in plant abiotic stress responses. Cellular and Molecular Life Sciences 69, 3269-3283.
| Crossref | Google Scholar | PubMed |
Castro PH, Verde N, Tavares RM, Bejarano ER, Azevedo H (2018) Sugar signaling regulation by Arabidopsis SIZ1-driven sumoylation is independent of salicylic acid. Plant Signaling & Behavior 13, e1179417.
| Crossref | Google Scholar | PubMed |
Catala R, Ouyang J, Abreu IA, Hu Y, Seo H, Zhang X, Chua N-H (2007) The Arabidopsis E3 SUMO ligase SIZ1 regulates plant growth and drought responses. The Plant Cell 19, 2952-2966.
| Crossref | Google Scholar | PubMed |
Celen AB, Sahin U (2020) Sumoylation on its 25th anniversary: mechanisms, pathology, and emerging concepts. The FEBS Journal 287, 3110-3140.
| Crossref | Google Scholar | PubMed |
Chen XL, Silver HR, Xiong L, Belichenko I, Adegite C, Johnson ES (2007) Topoisomerase I-dependent viability loss in Saccharomyces cerevisiae mutants defective in both SUMO conjugation and DNA repair. Genetics 177, 17-30.
| Crossref | Google Scholar | PubMed |
Cheong MS, Park HC, Hong MJ, Lee J, Choi W, Jin JB, Bohnert HJ, Lee SY, Bressan RA, Yun D-J (2009) Specific domain structures control abscisic acid-, salicylic acid-, and stress-mediated SIZ1 phenotypes. Plant Physiology 151, 1930-1942.
| Crossref | Google Scholar | PubMed |
Cheong MS, Park HC, Bohnert HJ, Bressan RA, Yun D-J (2010) Structural and functional studies of SIZ1, a PIAS-type SUMO E3 ligase from Arabidopsis. Plant Signaling & Behavior 5, 567-569.
| Crossref | Google Scholar | PubMed |
Coleman D, Kawamura A, Ikeuchi M, Favero DS, Lambolez A, Rymen B, Iwase A, Suzuki T, Sugimoto K (2020) The SUMO E3 ligase SIZ1 negatively regulates shoot regeneration. Plant Physiology 184, 330-344.
| Crossref | Google Scholar | PubMed |
Duan K, Yi K, Dang L, Huang H, Wu W, Wu P (2008) Characterization of a sub-family of Arabidopsis genes with the SPX domain reveals their diverse functions in plant tolerance to phosphorus starvation. The Plant Journal 54, 965-975.
| Crossref | Google Scholar | PubMed |
Elrouby N (2017) Regulation of plant cellular and organismal development by SUMO. Advances in Experimental Medicine and Biology 963, 227-247.
| Crossref | Google Scholar | PubMed |
Esmaeili N, Yang X, Cai Y, Sun L, Zhu X, Shen G, Payton P, Fang W, Zhang H (2019) Co-overexpression of AVP1 and OsSIZ1 in Arabidopsis substantially enhances plant tolerance to drought, salt, and heat stresses. Scientific Reports 9, 7642.
| Crossref | Google Scholar | PubMed |
Fang Q, Zhang J, Yang D-L, Huang C-F (2021) The SUMO E3 ligase SIZ1 partially regulates STOP1 SUMOylation and stability in Arabidopsis thaliana. Plant Signaling & Behavior 16, 1899487.
| Crossref | Google Scholar | PubMed |
FAO (2023) FAO report: agrifood sector faces growing threat from climate change-induced loss and damage. Food and Agriculture Organization. Available at https://www.fao.org/newsroom/detail/fao-report-agrifood-sector-faces-growing-threat-from-climate-change-induced-loss-and-damage/en
Garcia-Dominguez M, March-Diaz R, Reyes JC (2008) The PHD domain of plant PIAS proteins mediates sumoylation of bromodomain GTE proteins. Journal of Biological Chemistry 283, 21469-21477.
| Crossref | Google Scholar | PubMed |
Geoffroy M-C, Hay RT (2009) An additional role for SUMO in ubiquitin-mediated proteolysis. Nature Reviews: Molecular Cell Biology 10, 564-568.
| Crossref | Google Scholar | PubMed |
Ghimire S, Tang X, Zhang N, Liu W, Si H (2020) SUMO and SUMOylation in plant abiotic stress. Plant Growth Regulation 91, 317-325.
| Crossref | Google Scholar |
Ghimire S, Tang X, Liu W, Fu X, Zhang H, Zhang N, Si H (2021) SUMO conjugating enzyme: a vital player of SUMO pathway in plants. Physiology and Molecular Biology of Plants 27, 2421-2431.
| Crossref | Google Scholar | PubMed |
Guo J, Xu W, Yu X, Shen H, Li H, Cheng D, Liu A, Liu J, Liu C, Zhao S, Song J (2016) Cuticular wax accumulation is associated with drought tolerance in wheat near-isogenic lines. Frontiers in Plant Science 7, 1809.
| Crossref | Google Scholar | PubMed |
Hammoudi V, Fokkens L, Beerens B, Vlachakis G, Chatterjee S, Arroyo-Mateos M, Wackers PFK, Jonker MJ, van den Burg HA (2018) The Arabidopsis SUMO E3 ligase SIZ1 mediates the temperature dependent trade-off between plant immunity and growth. PLoS Genetics 14, e1007157.
| Crossref | Google Scholar | PubMed |
Han J, Mu Y, Huang J (2023) Preserving genome integrity: the vital role of SUMO-targeted ubiquitin ligases. Cell Insight 2, 100128.
| Crossref | Google Scholar | PubMed |
Hong Y, Chen Y, Shi H, Kong X, Yao J, Lei M, Zhu J-K, Wang Z (2022) SUMO E3 ligase SIZ1 negatively regulates arsenite resistance via depressing GSH biosynthesis in Arabidopsis. Stress Biology 2, 9.
| Crossref | Google Scholar | PubMed |
Huang L, Yang S, Zhang S, Liu M, Lai J, Qi Y, Shi S, Wang J, Wang Y, Xie Q, Yang C (2009) The Arabidopsis SUMO E3 ligase AtMMS21, a homologue of NSE2/MMS21, regulates cell proliferation in the root. The Plant Journal 60, 666-678.
| Crossref | Google Scholar | PubMed |
Ishida T, Fujiwara S, Miura K, Stacey N, Yoshimura M, Schneider K, Adachi S, Minamisawa K, Umeda M, Sugimoto K (2009) SUMO E3 ligase HIGH PLOIDY2 regulates endocycle onset and meristem maintenance in Arabidopsis. The Plant Cell 21, 2284-2297.
| Crossref | Google Scholar | PubMed |
Jiang J, Xie Y, Du J, Yang C, Lai J (2021) A SUMO ligase OsMMS21 regulates rice development and auxin response. Journal of Plant Physiology 263, 153447.
| Crossref | Google Scholar | PubMed |
Jiang H, Zhou L-J, Gao H-N, Wang X-F, Li Z-W, Li Y-Y (2022) The transcription factor MdMYB2 influences cold tolerance and anthocyanin accumulation by activating SUMO E3 ligase MdSIZ1 in apple. Plant Physiology 189, 2044-2060.
| Crossref | Google Scholar | PubMed |
Jin JB, Hasegawa PM (2008) Flowering time regulation by the SUMO E3 ligase SIZ1. Plant Signaling & Behavior 3, 891-892.
| Crossref | Google Scholar | PubMed |
Jin JB, Jin YH, Lee J, et al. (2008) The SUMO E3 ligase, AtSIZ1, regulates flowering by controlling a salicylic acid-mediated floral promotion pathway and through affects on FLC chromatin structure. The Plant Journal 53, 530-540.
| Crossref | Google Scholar | PubMed |
Jing Y, Yang Z, Yang R, Zhang Y, Qiao W, Zhou Y, Sun J (2023) PKL is stabilized by MMS21 to negatively regulate Arabidopsis drought tolerance through directly repressing AFL1 transcription. New Phytologist 239, 920-935.
| Crossref | Google Scholar | PubMed |
Johnson ES (2004) Protein Modification by SUMO. Annual Review of Biochemistry 73, 355-382.
| Crossref | Google Scholar | PubMed |
Joo H, Lim CW, Lee SC (2022) Pepper SUMO E3 ligase CaDSIZ1 enhances drought tolerance by stabilizing the transcription factor CaDRHB1. New Phytologist 235, 2313-2330.
| Crossref | Google Scholar | PubMed |
Kim DY, Han YJ, Kim S-I, Song JT, Seo HS (2015a) Arabidopsis CMT3 activity is positively regulated by AtSIZ1-mediated sumoylation. Plant Science 239, 209-215.
| Crossref | Google Scholar | PubMed |
Kim S-I, Park BS, Kim DY, Yeu SY, Song SI, Song JT, Seo HS (2015b) E3 SUMO ligase AtSIZ1 positively regulates SLY1-mediated GA signalling and plant development. Biochemical Journal 469, 299-314.
| Crossref | Google Scholar | PubMed |
Kim S-I, Kwak JS, Song JT, Seo HS (2016) The E3 SUMO ligase AtSIZ1 functions in seed germination in Arabidopsis. Physiologia Plantarum 158, 256-271.
| Crossref | Google Scholar | PubMed |
Kim JY, Song JT, Seo HS (2017) Post-translational modifications of Arabidopsis E3 SUMO ligase AtSIZ1 are controlled by environmental conditions. FEBS Open Bio 7, 1622-1634.
| Crossref | Google Scholar | PubMed |
Kwak JS, Kim S-I, Park SW, Song JT, Seo HS (2019) E3 SUMO ligase AtSIZ1 regulates the cruciferin content of Arabidopsis seeds. Biochemical and Biophysical Research Communications 519, 761-766.
| Crossref | Google Scholar | PubMed |
Lai R, Jiang J, Wang J, Du J, Lai J, Yang C (2022) Functional characterization of three maize SIZ/PIAS-type SUMO E3 ligases. Journal of Plant Physiology 268, 153588.
| Crossref | Google Scholar | PubMed |
Lascorz J, Codina-Fabra J, Reverter D, Torres-Rosell J (2022) SUMO-SIM interactions: from structure to biological functions. Seminars in Cell & Developmental Biology 132, 193-202.
| Crossref | Google Scholar | PubMed |
Lee J, Nam J, Park HC, et al. (2007) Salicylic acid-mediated innate immunity in Arabidopsis is regulated by SIZ1 SUMO E3 ligase. The Plant Journal 49, 79-90.
| Crossref | Google Scholar | PubMed |
Lei S, Wang Q, Chen Y, Song Y, Zheng M, Hsu Y-F (2022) Capsicum SIZ1 contributes to ABA-induced SUMOylation in pepper. Plant Science 314, 111099.
| Crossref | Google Scholar | PubMed |
Li Z, Hu Q, Zhou M, Vandenbrink J, Li D, Menchyk N, Reighard S, Norris A, Liu H, Sun D, Luo H (2013) Heterologous expression of OsSIZ1, a rice SUMO E3 ligase, enhances broad abiotic stress tolerance in transgenic creeping bentgrass. Plant Biotechnology Journal 11, 432-445.
| Crossref | Google Scholar | PubMed |
Li R, Ma J, Liu H, Wang X, Li J, Li Z, Li M, Sui S, Liu D (2021) Overexpression of CpSIZ1, a SIZ/PIAS-type SUMO E3 ligase from wintersweet (Chimonanthus praecox), delays flowering, accelerates leaf senescence and enhances cold tolerance in Arabidopsis. Plant Molecular Biology Reporter 39, 301-316.
| Crossref | Google Scholar |
Liao X, Sun J, Li Q, Ding W, Zhao B, Wang B, Zhou S, Wang H (2023) ZmSIZ1a and ZmSIZ1b play an indispensable role in resistance against fusarium ear rot in maize. Molecular Plant Pathology 24, 711-724.
| Crossref | Google Scholar | PubMed |
Lin F-M, Kumar S, Ren J, Karami S, Bahnassy S, Li Y, Zheng X, Wang J, Bawa-Khalfe T (2016) SUMOylation of HP1α supports association with ncRNA to define responsiveness of breast cancer cells to chemotherapy. Oncotarget 7, 30336-30349.
| Crossref | Google Scholar | PubMed |
Ling Y, Zhang C, Chen T, Hao H, Liu P, Bressan RA, Hasegawa PM, Jin JB, Lin J (2012) Mutation in SUMO E3 ligase, SIZ1, disrupts the mature female gametophyte in Arabidopsis. PLoS ONE 7, e29470.
| Crossref | Google Scholar | PubMed |
Liu M, Shi S, Zhang S, Xu P, Lai J, Liu Y, Yuan D, Wang Y, Du J, Yang C (2014) SUMO E3 ligase AtMMS21 is required for normal meiosis and gametophyte development in Arabidopsis. BMC Plant Biology 14, 153.
| Crossref | Google Scholar | PubMed |
Liu F, Wang X, Su M, Yu M, Zhang S, Lai J, Yang C, Wang Y (2015) Functional characterization of DnSIZ1, a SIZ/PIAS-type SUMO E3 ligase from Dendrobium. BMC Plant Biology 15, 225.
| Crossref | Google Scholar | PubMed |
Mercier C, Roux B, Have M, et al. (2021) Root responses to aluminium and iron stresses require the SIZ1 SUMO ligase to modulate the STOP1 transcription factor. The Plant Journal 108, 1507-1521.
| Crossref | Google Scholar | PubMed |
Minty A, Dumont X, Kaghad M, Caput D (2000) Covalent modification of p73α by SUMO-1: two-hybrid screening with p73 identifies novel SUMO-1-interacting proteins and a SUMO-1 interaction motif. Journal of Biological Chemistry 275, 36316-36323.
| Crossref | Google Scholar | PubMed |
Mishra N, Sun L, Zhu X, et al. (2017) Overexpression of the rice SUMO E3 ligase gene OsSIZ1 in cotton enhances drought and heat tolerance, and substantially improves fiber yields in the field under reduced irrigation and rainfed conditions. Plant and Cell Physiology 58, 735-746.
| Crossref | Google Scholar | PubMed |
Mishra N, Srivastava AP, Esmaeili N, Hu W, Shen G (2018) Overexpression of the rice gene OsSIZ1 in Arabidopsis improves drought-, heat-, and salt-tolerance simultaneously. PLoS ONE 13, e0201716.
| Crossref | Google Scholar | PubMed |
Miura K, Hasegawa PM (2009) Sumoylation and abscisic acid signaling. Plant Signaling & Behavior 4, 1176-1178.
| Crossref | Google Scholar | PubMed |
Miura K, Rus A, Sharkhuu A, Yokoi S, Karthikeyan AS, Raghothama KG, Baek D, Koo YD, Jin JB, Bressan RA, Yun D-J, Hasegawa PM (2005) The Arabidopsis SUMO E3 ligase SIZ1 controls phosphate deficiency responses. Proceedings of the National Academy of Sciences United States of America 102, 7760-7765.
| Crossref | Google Scholar |
Miura K, Jin JB, Lee J, Yoo CY, Stirm V, Miura T, Ashworth EN, Bressan RA, Yun D-J, Hasegawa P (2007) SIZ1-mediated sumoylation of ICE1 controls CBF3/DREB1A expression and freezing tolerance in Arabidopsis. The Plant Cell 19, 1403-1414.
| Crossref | Google Scholar | PubMed |
Miura K, Lee J, Jin JB, Yoo CY, Miura T, Hasegawa PM (2009) Sumoylation of ABI5 by the Arabidopsis SUMO E3 ligase SIZ1 negatively regulates abscisic acid signaling. Proceedings of the National Academy of Sciences United States of America 106, 5418-5423.
| Crossref | Google Scholar |
Miura K, Lee J, Miura T, Hasegawa PM (2010) SIZ1 controls cell growth and plant development in Arabidopsis through salicylic acid. Plant and Cell Physiology 51, 103-113.
| Crossref | Google Scholar | PubMed |
Miura K, Lee J, Gong Q, Ma S, Jin JB, Yoo CY, Miura T, Sato A, Bohnert HJ, Hasegawa PM (2011) SIZ1 regulation of phosphate starvation-induced root architecture remodeling involves the control of auxin accumulation. Plant Physiology 155, 1000-1012.
| Crossref | Google Scholar | PubMed |
Miura K, Okamoto H, Okuma E, Shiba H, Kamada H, Hasegawa PM, Murata Y (2013) SIZ1 deficiency causes reduced stomatal aperture and enhanced drought tolerance via controlling salicylic acid-induced accumulation of reactive oxygen species in Arabidopsis. The Plant Journal 73, 91-104.
| Crossref | Google Scholar | PubMed |
Muhammad W, Mehtab MA, Sunil KS (2024) Understanding the mechanistic basis of plant adaptation to salinity and drought. Functional Plant Biology 51, FP23216,.
| Crossref | Google Scholar |
Okushima Y, Shimizu K, Ishida T, Sugimoto K, Umeda M (2014) Differential regulation of B2-type CDK accumulation in Arabidopsis roots. Plant Cell Reports 33, 1033-1040.
| Crossref | Google Scholar | PubMed |
Park HJ, Yun D-J (2013) New insights into the role of the small ubiquitin-like modifier (SUMO) in plants. International Review of Cell and Molecular Biology 300, 161-209.
| Crossref | Google Scholar | PubMed |
Park HC, Kim H, Koo SC, et al. (2010) Functional characterization of the SIZ/PIAS-type SUMO E3 ligases, OsSIZ1 and OsSIZ2 in rice. Plant, Cell & Environment 33, 1923-1934.
| Crossref | Google Scholar | PubMed |
Park HJ, Kim W-Y, Park HC, Lee SY, Bohnert HJ, Yun D-J (2011a) SUMO and SUMOylation in plants. Molecules and Cells 32, 305-316.
| Crossref | Google Scholar | PubMed |
Park BS, Song JT, Seo HS (2011b) Arabidopsis nitrate reductase activity is stimulated by the E3 SUMO ligase AtSIZ1. Nature Communications 2, 400.
| Crossref | Google Scholar | PubMed |
Pei W, Jain A, Sun Y, Zhang Z, Ai H, Liu X, Wang H, Feng B, Sun R, Zhou H, Xu G, Sun S (2017) OsSIZ2 exerts regulatory influences on the developmental responses and phosphate homeostasis in rice. Scientific Reports 7, 12280.
| Crossref | Google Scholar | PubMed |
Pei W, Jain A, Ai H, Liu X, Feng B, Wang X, Sun Y, Xu G, Sun S (2019) OsSIZ2 regulates nitrogen homeostasis and some of the reproductive traits in rice. Journal of Plant Physiology 232, 51-60.
| Crossref | Google Scholar | PubMed |
Perez-Torres C-A, Lopez-Bucio J, Cruz-Ramı’rez A, Ibarra-Laclette E, Dharmasiri S, Estelle M, Herrera-Estrella L (2008) Phosphate availability alters lateral root development in Arabidopsis by modulating auxin sensitivity via a mechanism involving the TIR1 auxin receptor. The Plant Cell 20, 3258-3272.
| Crossref | Google Scholar |
Pichler A, Gast A, Seeler JS, Dejean A, Melchior F (2002) The nucleoporin RanBP2 has SUMO1 E3 ligase activity. Cell 108, 109-120.
| Crossref | Google Scholar | PubMed |
Potts PR, Yu H (2005) Human MMS21/NSE2 is a SUMO ligase required for DNA repair. Molecular and Cellular Biology 25, 7021-7032.
| Crossref | Google Scholar |
Psakhye I, Jentsch S (2012) Protein group modification and synergy in the SUMO pathway as exemplified in DNA repair. Cell 151, 807-820.
| Crossref | Google Scholar | PubMed |
Rubio V, Linhares F, Solano R, Martín AC, Iglesias J, Leyva A, Paz-Ares J (2001) A conserved MYB transcription factor involved in phosphate starvation signaling both in vascular plants and in unicellular algae. Genes & Development 15, 2122-2133.
| Crossref | Google Scholar | PubMed |
Rytz TC, Miller MJ, McLoughlin F, Augustine RC, Marshall RS, Juan Y-T, Charng Y-Y, Scalf M, Smith LM, Vierstra RD (2018) SUMOylome profiling reveals a diverse array of nuclear targets modified by the SUMO ligase SIZ1 during heat stress. The Plant Cell 30, 1077-1099.
| Crossref | Google Scholar | PubMed |
Sarangi P, Zhao X (2015) SUMO-mediated regulation of DNA damage repair and responses. Trends in Biochemical Sciences 40, 233-242.
| Crossref | Google Scholar | PubMed |
Son GH, Park BS, Song JT, Seo HS (2014) FLC-mediated flowering repression is positively regulated by sumoylation. Journal of Experimental Botany 65, 339-351.
| Crossref | Google Scholar | PubMed |
Thangasamy S, Guo C-L, Chuang M-H, Lai M-H, Chen J, Jauh G-Y (2011) Rice SIZ1, a SUMO E3 ligase, controls spikelet fertility through regulation of anther dehiscence. New Phytologist 189, 869-882.
| Crossref | Google Scholar | PubMed |
Tomanov K, Zeschmann A, Hermkes R, Eifler K, Ziba I, Grieco M, Novatchkova M, Hofmann K, Hesse H, Bachmair A (2014) Arabidopsis PIAL1 and 2 promote SUMO chain formation as E4-type SUMO ligases and are involved in stress responses and sulfur metabolism. The Plant Cell 26, 4547-4560.
| Crossref | Google Scholar | PubMed |
Tsuge M, Kaneoka H, Masuda Y, Ito H, Miyake K, Iijima S (2015) Implication of SUMO E3 ligases in nucleotide excision repair. Cytotechnology 67, 681-687.
| Crossref | Google Scholar | PubMed |
Varejão N, Lascorz J, Li Y, Reverter D (2020) Molecular mechanisms in SUMO conjugation. Biochemical Society Transactions 48, 123-135.
| Crossref | Google Scholar | PubMed |
Varejão N, Lascorz J, Codina-Fabra J, Bellí G, Borràs-Gas H, Torres-Rosell J, Reverter D (2021) Structural basis for the E3 ligase activity enhancement of yeast Nse2 by SUMO-interacting motifs. Nature Communications 12, 7013.
| Crossref | Google Scholar | PubMed |
Vertegaal ACO (2022) Signalling mechanisms and cellular functions of SUMO. Nature Reviews Molecular Cell Biology 23, 715-731.
| Crossref | Google Scholar | PubMed |
Wang X, Du G, Wang X, Meng Y, Li Y, Wu P, Yi K (2010) The function of LPR1 is controlled by an element in the promoter and is independent of SUMO E3 ligase SIZ1 in response to low Pi stress in Arabidopsis thaliana. Plant and Cell Physiology 51, 380-394.
| Crossref | Google Scholar | PubMed |
Wang H, Makeen K, Yan Y, Cao Y, Sun S, Xu G (2011) OsSIZ1 regulates the vegetative growth and reproductive development in rice. Plant Molecular Biology Reporter 29, 411-417.
| Crossref | Google Scholar |
Wang G-L, Zhang C-L, Huo H-Q, Sun X-S, Zhang Y-L, Hao Y-J, You C-X (2022) The SUMO E3 ligase MdSIZ1 sumoylates a cell number regulator MdCNR8 to control organ size. Frontiers in Plant Science 13, 836935.
| Crossref | Google Scholar | PubMed |
Wilkinson KA, Henley JM (2010) Mechanisms, regulation and consequences of protein SUMOylation. Biochemical Journal 428, 133-145.
| Crossref | Google Scholar | PubMed |
Xiong J, Yang F, Wei F, Yang F, Lin H, Zhang D (2023) Inhibition of SIZ1-mediated SUMOylation of HOOKLESS1 promotes light-induced apical hook opening in Arabidopsis. The Plant Cell 35, 2027-2043.
| Crossref | Google Scholar | PubMed |
Xu P, Yuan D, Liu M, Li C, Liu Y, Zhang S, Yao N, Yang C (2013) AtMMS21, an SMC5/6 complex subunit, is involved in stem cell niche maintenance and DNA damage responses in Arabidopsis roots. Plant Physiology 161, 1755-1768.
| Crossref | Google Scholar | PubMed |
Xu J, Zhu J, Liu J, Wang J, Ding Z, Tian H (2021) SIZ1 negatively regulates aluminum resistance by mediating the STOP1-ALMT1 pathway in Arabidopsis. Journal of Integrative Plant Biology 63, 1147-1160.
| Crossref | Google Scholar | PubMed |
Xun Q, Song Y, Mei M, Ding Y, Ding C (2023) The SMC5/6 complex subunit MMS21 regulates stem cell proliferation in rice. Plant Cell Reports 42, 1279-1290.
| Crossref | Google Scholar | PubMed |
Yoo CY, Miura K, Jin JB, Lee J, Park HC, Salt DE, Yun D-J, Bressan RA, Hasegawa PM (2006) SIZ1 small ubiquitin-like modifier E3 ligase facilitates basal thermotolerance in Arabidopsis independent of salicylic acid. Plant Physiology 142, 1548-1558.
| Crossref | Google Scholar | PubMed |
Yuan H, Liu D (2008) Signaling components involved in plant responses to phosphate starvation. Journal of Integrative Plant Biology 50, 849-859.
| Crossref | Google Scholar | PubMed |
Zhang S, Qi Y, Yang C (2010) Arabidopsis SUMO E3 ligase AtMMS21 regulates root meristem development. Plant Signaling & Behavior 5, 53-55.
| Crossref | Google Scholar | PubMed |
Zhang S, Qi Y, Liu M, Yang C (2013) SUMO E3 ligase AtMMS21 regulates drought tolerance in Arabidopsis thaliana. Journal of Integrative Plant Biology 55, 83-95.
| Crossref | Google Scholar | PubMed |
Zhang R-F, Guo Y, Li Y-Y, Zhou L-J, Hao Y-J, You C-X (2016) Functional identification of MdSIZ1 as a SUMO E3 ligase in apple. Journal of Plant Physiology 198, 69-80.
| Crossref | Google Scholar | PubMed |
Zhang S, Zhuang K, Wang S, Lv J, Ma N, Meng Q (2017) A novel tomato SUMO E3 ligase, SlSIZ1, confers drought tolerance in transgenic tobacco. Journal of Integrative Plant Biology 59, 102-117.
| Crossref | Google Scholar | PubMed |
Zhang S, Wang S, Lv J, Liu Z, Wang Y, Ma N, Meng Q (2018) SUMO E3 ligase SlSIZ1 facilitates heat tolerance in tomato. Plant and Cell Physiology 59, 58-71.
| Crossref | Google Scholar | PubMed |
Zhang R-F, Zhou L-J, Li Y-Y, You C-X, Sha G-L, Hao Y-J (2019) Apple SUMO E3 ligase MdSIZ1 is involved in the response to phosphate deficiency. Journal of Plant Physiology 232, 216-225.
| Crossref | Google Scholar | PubMed |
Zhang L, Han Q, Xiong J, Zheng T, Han J, Zhou H, Lin H, Yin Y, Zhang D (2019b) Sumoylation of BRI1-EMS-SUPPRESSOR 1 (BES1) by the SUMO E3 ligase SIZ1 negatively regulates brassinosteroids signaling in Arabidopsis thaliana. Plant and Cell Physiology 60, 2282-2292.
| Crossref | Google Scholar |
Zhang X, Huai J, Liu S, Jin JB, Lin R (2020) SIZ1-mediated SUMO modification of SEUSS regulates photomorphogenesis in Arabidopsis. Plant Communications 1, 100080.
| Crossref | Google Scholar | PubMed |
Zhang C-L, Wang G-L, Zhang Y-L, Hu X, Zhou L-J, You C-X, Li Y-Y, Hao Y-J (2021) Apple SUMO E3 ligase MdSIZ1 facilitates SUMOylation of MdARF8 to regulate lateral root formation. New Phytologist 229, 2206-2222.
| Crossref | Google Scholar | PubMed |
Zhang H, Zhu J, Gong Z, Zhu J-K (2022) Abiotic stress responses in plants. Nature Reviews Genetics 23, 104-119.
| Crossref | Google Scholar | PubMed |
Zhang Y, Xu J, Li R, Ge Y, Li Y, Li R (2023a) Plants’ response to abiotic stress: mechanisms and strategies. International Journal of Molecular Sciences 24, 10915.
| Crossref | Google Scholar | PubMed |
Zhang C, Yang Y, Yu Z, Wang J, Huang R, Zhan Q, Li S, Lai J, Zhang S, Yang C (2023b) SUMO E3 ligase AtMMS21-dependent SUMOylation of AUXIN/INDOLE-3-ACETIC ACID 17 regulates auxin signaling. Plant Physiology 191, 1871-1883.
| Crossref | Google Scholar | PubMed |
Zhang Y, Lyu S, Hu Z, Yang X, Zhu H, Deng S (2023c) Identification and functional characterization of the SUMO system in sweet potato under salt and drought stress. Plant Science 330, 111645.
| Crossref | Google Scholar | PubMed |
Zhang Y-L, Tian Y, Man Y-Y, Zhang C-L, Wang Y, You C-X, Li Y-Y (2023d) Apple SUMO E3 ligase MdSIZ1 regulates cuticular wax biosynthesis by SUMOylating transcription factor MdMYB30. Plant Physiology 191, 1771-1788.
| Crossref | Google Scholar | PubMed |
Zheng Y, Schumaker KS, Guo Y (2012) Sumoylation of transcription factor MYB30 by the small ubiquitin-like modifier E3 ligase SIZ1 mediates abscisic acid response in Arabidopsis thaliana. Proceedings of the National Academy of Sciences, USA 109, 12822-12827.
| Crossref | Google Scholar |
Zheng T, Wu G, Tao X, He B (2022) Arabidopsis SUMO E3 ligase SIZ1 enhances cadmium tolerance via the glutathione-dependent phytochelatin synthesis pathway. Plant Science 322, 111357.
| Crossref | Google Scholar | PubMed |
Zhou X, Du J, Liu Y, Yang C, Lai J (2019a) Functional characterization of DiMMS21, a SUMO ligase from Desmodium intortum. Plant Physiology and Biochemistry 141, 206-214.
| Crossref | Google Scholar | PubMed |
Zhou L-J, Zhang C-L, Zhang R-F, Wang G-L, Li Y-Y, Hao Y-J (2019b) The SUMO E3 ligase MdSIZ1 targets MdbHLH104 to regulate plasma membrane H+-ATPase activity and iron homeostasis. Plant Physiology 179, 88-106.
| Crossref | Google Scholar | PubMed |
