[an error occurred while processing this directive] [an error occurred while processing this directive]
[an error occurred while processing this directive]蛋白液-液相分离调控植物发育及胁迫应答研究进展
收稿日期: 2023-05-29
录用日期: 2023-08-09
网络出版日期: 2023-11-13
基金资助
国家自然科学基金(32072637);国家自然科学基金(31930086);北京市自然科学基金(6212025)
Advances in the Regulation of Protein Liquid-liquid Phase Separation on Development and Stress Responses in Plants
Received date: 2023-05-29
Accepted date: 2023-08-09
Online published: 2023-11-13
黄鑫华, 刘伟, 田世平, 陈彤 . 蛋白液-液相分离调控植物发育及胁迫应答研究进展[J]. 植物学报, 2023 , 58(6) : 946 -955 . DOI: 10.11983/CBB23070
Cells are basic units of structure and function for organisms, in which membranous and membraneless organelles exert their respective functions in a given space. However, the mechanism underlying the formation and function of membraneless organelles still requires further investigation. It has been shown that liquid-liquid phase separation (LLPS) of proteins may provide a specific way for biomacromolecules within cells to aggregate and form agglomerates, then proceed to play important roles. With increasing reports on LLPS in plants, great interest has been in exploring the roles of phase separation-forming agglutinates in plant growth and development and immune processes. In this review, we mainly focus on the progress of current studies on the role of protein liquid-liquid phase separation in regulating plant growth and development as well as stress responses, which may provide references for further studies on the mechanism of LLPS in plant cells.
[1] | 李保珠, 赵孝亮, 彭雷 (2014). 植物叶绿体发育及调控研究进展. 植物学报 49, 337-345. |
[2] | 王静, 王艇 (2007). 高等植物光敏色素的分子结构、生理功能和进化特征. 植物学通报 24, 649-658. |
[3] | 张长生, 魏滔, 周玉萍, 范甜, 吕天晓, 田长恩 (2021). FLC调控植物成花的分子机制研究新进展. 植物学报 56, 651-663. |
[4] | Berry S, Rosa S, Howard M, Bühler M, Dean C (2017). Disruption of an RNA-binding hinge region abolishes LHP1- mediated epigenetic repression. Genes Dev 31, 2115-2120. |
[5] | Boisvert FM, van Koningsbruggen S, Navascués J, Lamond AI (2007). The multifunctional nucleolus. Nat Rev Mol Cell Biol 8, 574-585. |
[6] | Brangwynne CP, Eckmann CR, Courson DS, Rybarska A, Hoege C, Gharakhani J, Jülicher F, Hyman AA (2009). Germline P granules are liquid droplets that localize by controlled dissolution/condensation. Science 324, 1729-1732. |
[7] | Castel SE, Martienssen RA (2013). RNA interference in the nucleus: roles for small RNAs in transcription, epigenetics and beyond. Nat Rev Genet 14, 100-112. |
[8] | Chakrabortee S, Kayatekin C, Newby GA, Mendillo ML, Lancaster A, Lindquist S (2016). Luminidependens (LD) is an Arabidopsis protein with prion behavior. Proc Natl Acad Sci USA 113, 6065-6070. |
[9] | Chandler JW (2016). Auxin response factors. Plant Cell Environ 39, 1014-1028. |
[10] | Chen D, Lyu M, Kou XX, Li J, Yang ZX, Gao LL, Li Y, Fan LM, Shi H, Zhong SW (2022). Integration of light and temperature sensing by liquid-liquid phase separation of phytochrome B. Mol Cell 82, 3015-3029. |
[11] | Chen M, Galv?o RM, Li MN, Burger B, Bugea J, Bolado J, Chory J (2010). Arabidopsis HEMERA/pTAC12 initiates photomorphogenesis by phytochromes. Cell 141, 1230-1240. |
[12] | Dodds PN, Rathjen JP (2010). Plant immunity: towards an integrated view of plant-pathogen interactions. Nat Rev Genet 11, 539-548. |
[13] | Dorone Y, Boeynaems S, Flores E, Jin B, Hateley S, Bossi F, Lazarus E, Pennington JG, Michiels E, De Decker M, Vints K, Baatsen P, Bassel GW, Otegui MS, Holehouse AS, Exposito-Alonso M, Sukenik S, Gitler AD, Rhee SY (2021). A prion-like protein regulator of seed germination undergoes hydration-dependent phase separation. Cell 184, 4284-4298. |
[14] | Fang XF, Wang L, Ishikawa R, Li YX, Fiedler M, Liu FQ, Calder G, Rowan B, Weigel D, Li PL, Dean C (2019). Arabidopsis FLL2 promotes liquid-liquid phase separation of polyadenylation complexes. Nature 569, 265-269. |
[15] | Fu ZQ, Dong XN (2013). Systemic acquired resistance: turning local infection into global defense. Annu Rev Plant Biol 64, 839-863. |
[16] | Gall JG (2003). The centennial of the Cajal body. Nat Rev Mol Cell Biol 4, 975-980. |
[17] | Hoffmann G, López-González S, Mahboubi A, Hanson J, Hafrén A (2023). Cauliflower mosaic virus protein P6 is a multivalent node for RNA granule proteins and interferes with stress granule responses during plant infection. Plant Cell 35, 3363-3382. |
[18] | Huang H, Yoo CY, Bindbeutel R, Goldsworthy J, Tielking A, Alvarez S, Naldrett MJ, Evans BS, Chen M, Nusinow DA (2016). PCH1 integrates circadian and light-signaling pathways to control photoperiod-responsive growth in Arabidopsis. eLife 5, e13292. |
[19] | Huang S, Zhu SW, Kumar P, MacMicking JD (2021). A phase-separated nuclear GBPL circuit controls immunity in plants. Nature 594, 424-429. |
[20] | Huang XZ, Xiao N, Zou YP, Xie Y, Tang LL, Zhang YQ, Yu Y, Li YT, Xu C (2022). Heterotypic transcriptional condensates formed by prion-like paralogous proteins canalize flowering transition in tomato. Genome Biol 23, 78. |
[21] | Hyman AA, Weber CA, Jülicher F (2014). Liquid-liquid phase separation in biology. Annu Rev Cell Dev Biol 30, 39-58. |
[22] | Jiang BC, Shi YT, Peng Y, Jia YX, Yan Y, Dong XJ, Li H, Dong J, Li JG, Gong ZZ, Thomashow MF, Yang SH (2020). Cold-induced CBF-PIF3 interaction enhances freezing tolerance by stabilizing the phyB thermosensor in Arabidopsis. Mol Plant 13, 894-906. |
[23] | Jin HS, Choi SM, Kang MJ, Yun SH, Kwon DJ, Noh YS, Noh B (2018). Salicylic acid-induced transcriptional reprogramming by the HAC-NPR1-TGA histone acetyltransferase complex in Arabidopsis. Nucleic Acids Res 46, 11712-11725. |
[24] | Jones JDG, Dangl JL (2006). The plant immune system. Nature 444, 323-329. |
[25] | Jung JH, Barbosa AD, Hutin S, Kumita JR, Gao MJ, Derwort D, Silva CS, Lai XL, Pierre E, Geng F, Kim SB, Baek S, Zubieta C, Jaeger KE, Wigge PA (2020). A prion-like domain in ELF3 functions as a thermosensor in Arabidopsis. Nature 585, 256-260. |
[26] | Jung JH, Domijan M, Klose C, Biswas S, Ezer D, Gao MJ, Khattak AK, Box MS, Charoensawan V, Cortijo S, Kumar M, Grant A, Locke JCW, Sch?fer E, Jaeger KE, Wigge PA (2016). Phytochromes function as thermosensors in Arabidopsis. Science 354, 886-889. |
[27] | Kaiserli E, Páldi K, O'Donnell L, Batalov O, Pedmale UV, Nusinow DA, Kay SA, Chory J (2015). Integration of light and photoperiodic signaling in transcriptional nuclear foci. Dev Cell 35, 311-321. |
[28] | Kim EY, Wang L, Lei Z, Li H, Fan WW, Cho J (2021). Ribosome stalling and SGS3 phase separation prime the epigenetic silencing of transposons. Nat Plants 7, 303-309. |
[29] | Kim JH, Castroverde CDM, Huang S, Li C, Hilleary R, Seroka A, Sohrabi R, Medina-Yerena D, Huot B, Wang J, Nomura K, Marr SK, Wildermuth MC, Chen T, MacMicking JD, He SY (2022). Increasing the resilience of plant immunity to a warming climate. Nature 607, 339-344. |
[30] | Lippman ZB, Cohen O, Alvarez JP, Abu-Abied M, Pekker I, Paran I, Eshed Y, Zamir D (2008). The making of a compound inflorescence in tomato and related nightshades. PLoS Biol 6, e288. |
[31] | Ma XY, Cline K (2010). Multiple precursor proteins bind individual Tat receptor complexes and are collectively tran- sported. EMBO J 29, 1477-1488. |
[32] | Ma Y, Dai XY, Xu YY, Luo W, Zheng XM, Zeng DL, Pan YJ, Lin XL, Liu HH, Zhang DJ, Xiao J, Guo XY, Xu SJ, Niu YD, Jin JB, Zhang H, Xu X, Li LG, Wang W, Qian Q, Ge S, Chong K (2015). COLD1 confers chilling tolerance in rice. Cell 160, 1209-1221. |
[33] | MacAlister CA, Park SJ, Jiang K, Marcel F, Bendahmane A, Izkovich Y, Eshed Y, Lippman ZB (2012). Synchronization of the flowering transition by the tomato TERMINATING FLOWER gene. Nat Genet 44, 1393-1398. |
[34] | Mahen R, Venkitaraman AR (2012). Pattern formation in centrosome assembly. Curr Opin Cell Biol 24, 14-23. |
[35] | Martin EW, Holehouse AS, Peran I, Farag M, Incicco JJ, Bremer A, Grace CR, Soranno A, Pappu RV, Mittag T (2020). Valence and patterning of aromatic residues determine the phase behavior of prion-like domains. Science 367, 694-699. |
[36] | Misteli T (2001). Protein dynamics: implications for nuclear architecture and gene expression. Science 291, 843-847. |
[37] | Mitrea DM, Mittasch M, Gomes BF, Klein IA, Murcko MA (2022). Modulating biomolecular condensates: a novel approach to drug discovery. Nat Rev Drug Discov 21, 841-862. |
[38] | Molliex A, Temirov J, Lee J, Coughlin M, Kanagaraj AP, Kim HJ, Mittag T, Taylor JP (2015). Phase separation by low complexity domains promotes stress granule assembly and drives pathological fibrillization. Cell 163, 123-133. |
[39] | Nonogaki H (2019). Seed germination and dormancy: the classic story, new puzzles, and evolution. J Integr Plant Biol 61, 541-563. |
[40] | Nuthikattu S, McCue AD, Panda K, Fultz D, DeFraia C, Thomas EN, Slotkin RK (2013). The initiation of epigenetic silencing of active transposable elements is triggered by RDR6 and 21-22 nucleotide small interfering RNAs. Plant Physiol 162, 116-131. |
[41] | Ouyang M, Li XY, Zhang J, Feng PQ, Pu H, Kong LX, Bai ZC, Rong LW, Xu XM, Chi W, Wang Q, Chen F, Lu CM, Shen JR, Zhang LX (2020). Liquid-liquid phase transition drives intra-chloroplast cargo sorting. Cell 180, 1144-1159. |
[42] | Powers SK, Holehouse AS, Korasick DA, Schreiber KH, Clark NM, Jing HW, Emenecker R, Han S, Tycksen E, Hwang I, Sozzani R, Jez JM, Pappu RV, Strader LC (2019). Nucleo-cytoplasmic partitioning of ARF proteins controls auxin responses in Arabidopsis thaliana. Mol Cell 76, 177-190. |
[43] | Rhoads SN, Monahan ZT, Yee DS, Shewmaker FP (2018). The role of post-translational modifications on prion—like aggregation and liquid-phase separation of FUS. Int J Mol Sci 19, 886. |
[44] | Ryals JA, Neuenschwander UH, Willits MG, Molina A, Steiner HY, Hunt MD (1996). Systemic acquired resistance. Plant Cell 8, 1809-1819. |
[45] | Safi A, Smagghe W, Gon?alves A, Wang Q, Xu K, Fernandez AI, Cappe B, Riquet FB, Mylle E, Eeckhout D, De Winne N, Van De Slijke E, Persyn F, Persiau G, Van Damme D, Geelen D, De Jaeger G, Beeckman T, Van Leene J, Vanneste S (2023). Phase separation-based visualization of protein-protein interactions and kinase activities in plants. Plant Cell 35, 3280-3302. |
[46] | Slotkin RK, Martienssen R (2007). Transposable elements and the epigenetic regulation of the genome. Nat Rev Ge- net 8, 272-285. |
[47] | Song PZ, Yang JB, Wang CL, Lu Q, Shi LQ, Tayier S, Jia GF (2021). Arabidopsis N6-methyladenosine reader CPSF30-L recognizes FUE signals to control polyadenylation site choice in liquid-like nuclear bodies. Mol Plant 14, 571-587. |
[48] | Sonmez C, B?urle I, Magusin A, Dreos R, Laubinger S, Weigel D, Dean C (2011). RNA 3′ processing functions of Arabidopsis FCA and FPA limit intergenic transcription. Proc Natl Acad Sci USA 108, 8508-8513. |
[49] | Wang B, Zhang L, Dai T, Qin ZR, Lu HS, Zhang L, Zhou FF (2021). Liquid-liquid phase separation in human health and diseases. Sig Transduct Target Ther 6, 290. |
[50] | Wang WY, Wang CH, Wang YH, Ma J, Wang TY, Tao Z, Liu PP, Li S, Hu YY, Gu AJ, Wang H, Qiu CH, Li PJ (2023). The P-body component DECAPPING5 and the floral repressor SISTER OF FCA regulate FLOWERING LOCUS C transcription in Arabidopsis. Plant Cell 35, 3303-3324. |
[51] | Weber SC, Brangwynne CP (2012). Getting RNA and protein in phase. Cell 149, 1188-1191. |
[52] | Whittaker C, Dean C (2017). The FLC locus: a platform for discoveries in epigenetics and adaptation. Annu Rev Cell Dev Biol 33, 555-575. |
[53] | Wippich F, Bodenmiller B, Trajkovska MG, Wanka S, Aebersold R, Pelkmans L (2013). Dual specificity kinase DYRK3 couples stress granule condensation/dissolution to mTORC1 signaling. Cell 152, 791-805. |
[54] | Xu XM, Zheng CH, Lu DD, Song CP, Zhang LX (2021). Phase separation in plants: new insights into cellular compartmentalization. J Integr Plant Biol 63, 1835-1855. |
[55] | Yamaguchi R, Nakamura M, Mochizuki N, Kay SA, Nagatani A (1999). Light-dependent translocation of a phytochrome B-GFP fusion protein to the nucleus in transgenic Arabidopsis. J Cell Biol 145, 437-445. |
[56] | Zavaliev R, Mohan R, Chen TY, Dong XN (2020). Formation of NPR1 condensates promotes cell survival during the plant immune response. Cell 182, 1093-1108. |
[57] | Zhang H, Ji X, Li PL, Liu C, Lou JZ, Wang Z, Wen WY, Xiao Y, Zhang MJ, Zhu XL (2020a). Liquid-liquid phase separation in biology: mechanisms, physiological functions and human diseases. Sci China Life Sci 63, 953-985. |
[58] | Zhang YL, Li ZK, Chen NZ, Huang Y, Huang SJ (2020b). Phase separation of Arabidopsis EMB1579 controls transcription, mRNA splicing, and development. PLoS Biol 18, e3000782. |
[59] | Zhou H, Song Z, Zhong S, Zuo L, Qi Z, Qu LJ, Lai LH (2019). Mechanism of DNA-induced phase separation for transcriptional repressor VRN1. Angew Chem Int Ed 58, 4858-4862. |
[60] | Zhu SB, Gu JG, Yao JJ, Li YC, Zhang ZT, Xia WC, Wang Z, Gui XR, Li LT, Li D, Zhang H, Liu C (2022). Liquid- liquid phase separation of RBGD2/4 is required for heat stress resistance in Arabidopsis. Dev Cell 57, 583-597. |
/
〈 | 〉 |