生物技术通报 ›› 2023, Vol. 39 ›› Issue (3): 26-34.doi: 10.13560/j.cnki.biotech.bull.1985.2022-0775
收稿日期:
2022-06-25
出版日期:
2023-03-26
发布日期:
2023-04-10
通讯作者:
曲桂芹,女,博士,副教授,研究方向:果蔬采后生理与分子生物学;E-mail: qugq@cau.edu.cn作者简介:
刘铖霞,女,硕士研究生,研究方向:果蔬采后生理与分子生物学;E-mail: 18817515889@163.com
基金资助:
LIU Cheng-xia(), SUN Zong-yan, LUO Yun-bo, ZHU Hong-liang, QU Gui-qin()
Received:
2022-06-25
Published:
2023-03-26
Online:
2023-04-10
摘要:
bHLH转录因子是植物体内第二大类转录因子,在植物生长发育和胁迫反应的转录调控网络中扮演着非常重要的角色。磷酸化作为蛋白质翻译后重要的调控方式,影响转录因子的转录活性、定位、蛋白间互作、稳定性。为深入了解磷酸化对bHLH转录因子的影响,本文对近年来bHLH家族成员的磷酸化研究进展进行综述,包括bHLH转录因子的结构、分类、功能以及磷酸化位点上的突变对其生理及生化功能的改变,为从磷酸化调控角度提升农作物的营养利用效率、品质和抗逆性等农艺性状提供理论依据。
刘铖霞, 孙宗艳, 罗云波, 朱鸿亮, 曲桂芹. bHLH转录因子的磷酸化调控植物生理功能的研究进展[J]. 生物技术通报, 2023, 39(3): 26-34.
LIU Cheng-xia, SUN Zong-yan, LUO Yun-bo, ZHU Hong-liang, QU Gui-qin. Multifaceted Roles of bHLH Phosphorylation in Regulation of Plant Physiological Functions[J]. Biotechnology Bulletin, 2023, 39(3): 26-34.
[1] |
Lv PT, Yu S, Zhu N, et al. Genome encode analyses reveal the basis of convergent evolution of fleshy fruit ripening[J]. Nat Plants, 2018, 4(10): 784-791.
doi: 10.1038/s41477-018-0249-z pmid: 30250279 |
[2] | Ji XY, Nie XG, Liu YJ, et al. A bHLH gene from Tamarix hispida improves abiotic stress tolerance by enhancing osmotic potential and decreasing reactive oxygen species accumulation[J]. Tree Physiol, 2016, 36(2): 193-207. |
[3] |
Verma D, Jalmi SK, Bhagat PK, et al. A bHLH transcription factor, MYC2, imparts salt intolerance by regulating proline biosynthesis in Arabidopsis[J]. FEBS J, 2020, 287(12): 2560-2576.
doi: 10.1111/febs.v287.12 URL |
[4] |
Wang PC, Zhao Y, Li ZP, et al. Reciprocal regulation of the TOR kinase and ABA receptor balances plant growth and stress response[J]. Mol Cell, 2018, 69(1): 100-112.e6.
doi: S1097-2765(17)30930-9 pmid: 29290610 |
[5] |
Yin XJ, Wang X, Komatsu S. Phosphoproteomics: protein phosphorylation in regulation of seed germination and plant growth[J]. Curr Protein Pept Sci, 2018, 19(4): 401-412.
doi: 10.2174/1389203718666170209151048 URL |
[6] |
Zhang X, Cui YN, Yu M, et al. Phosphorylation-mediated dynamics of nitrate transceptor NRT1.1 regulate auxin flux and nitrate signaling in lateral root growth[J]. Plant Physiol, 2019, 181(2): 480-498.
doi: 10.1104/pp.19.00346 pmid: 31431511 |
[7] |
van Wijk KJ, Friso G, Walther D, et al. Meta-analysis of Arabidopsis thaliana phospho-proteomics data reveals compartmentalization of phosphorylation motifs[J]. Plant Cell, 2014, 26(6): 2367-2389.
doi: 10.1105/tpc.114.125815 URL |
[8] |
Bethke G, Unthan T, Uhrig JF, et al. Flg22 regulates the release of an ethylene response factor substrate from MAP kinase 6 in Arabidopsis thaliana via ethylene signaling[J]. Proc Natl Acad Sci USA, 2009, 106(19): 8067-8072.
doi: 10.1073/pnas.0810206106 pmid: 19416906 |
[9] |
Tsuda K, Somssich IE. Transcriptional networks in plant immunity[J]. New Phytol, 2015, 206(3): 932-947.
doi: 10.1111/nph.13286 pmid: 25623163 |
[10] |
Guo JR, Sun BX, He HR, et al. Current understanding of bHLH transcription factors in plant abiotic stress tolerance[J]. Int J Mol Sci, 2021, 22(9): 4921.
doi: 10.3390/ijms22094921 URL |
[11] |
Wang HL, Guo SY, Qiao X, et al. BZU2/ZmMUTE controls symmetrical division of guard mother cell and specifies neighbor cell fate in maize[J]. PLoS Genet, 2019, 15(8): e1008377.
doi: 10.1371/journal.pgen.1008377 URL |
[12] |
Buti S, Hayes S, Pierik R. The bHLH network underlying plant shade-avoidance[J]. Physiol Plant, 2020, 169(3): 312-324.
doi: 10.1111/ppl.13074 pmid: 32053251 |
[13] |
Li PH, Chen BB, Zhang GY, et al. Regulation of anthocyanin and proanthocyanidin biosynthesis by Medicago truncatula bHLH transcription factor MtTT8[J]. New Phytol, 2016, 210(3): 905-921.
doi: 10.1111/nph.2016.210.issue-3 URL |
[14] |
Qian YC, Zhang TY, Yu Y, et al. Regulatory mechanisms of bHLH transcription factors in plant adaptive responses to various abiotic stresses[J]. Front Plant Sci, 2021, 12: 677611.
doi: 10.3389/fpls.2021.677611 URL |
[15] |
Jones S. An overview of the basic helix-loop-helix proteins[J]. Genome Biol, 2004, 5(6): 226.
doi: 10.1186/gb-2004-5-6-226 pmid: 15186484 |
[16] |
Atchley WR, Terhalle W, Dress A. Positional dependence, cliques, and predictive motifs in the bHLH protein domain[J]. J Mol Evol, 1999, 48(5): 501-516.
doi: 10.1007/pl00006494 pmid: 10198117 |
[17] |
Nesi N, Debeaujon I, Jond C, et al. The TT8 gene encodes a basic helix-loop-helix domain protein required for expression of DFR and BAN genes in Arabidopsis siliques[J]. Plant Cell, 2000, 12(10): 1863-1878.
doi: 10.1105/tpc.12.10.1863 pmid: 11041882 |
[18] |
Feller A, Machemer K, Braun EL, et al. Evolutionary and comparative analysis of MYB and bHLH plant transcription factors[J]. Plant J, 2011, 66(1): 94-116.
doi: 10.1111/tpj.2011.66.issue-1 URL |
[19] |
Hao YQ, Zong XM, Ren P, et al. Basic helix-loop-helix(bHLH)transcription factors regulate a wide range of functions in Arabidopsis[J]. Int J Mol Sci, 2021, 22(13): 7152.
doi: 10.3390/ijms22137152 URL |
[20] |
Groszmann M, Bylstra Y, Lampugnani ER, et al. Regulation of tissue-specific expression of SPATULA, a bHLH gene involved in carpel development, seedling germination, and lateral organ growth in Arabidopsis[J]. J Exp Bot, 2010, 61(5): 1495-1508.
doi: 10.1093/jxb/erq015 pmid: 20176890 |
[21] |
Carretero-Paulet L, Galstyan A, Roig-Villanova I, et al. Genome-wide classification and evolutionary analysis of the bHLH family of transcription factors in Arabidopsis, poplar, rice, moss, and algae[J]. Plant Physiol, 2010, 153(3): 1398-1412.
doi: 10.1104/pp.110.153593 pmid: 20472752 |
[22] |
Song XM, Huang ZN, Duan WK, et al. Genome-wide analysis of the bHLH transcription factor family in Chinese cabbage(Brassica rapa ssp. pekinensis)[J]. Mol Genet Genom, 2014, 289(1): 77-91.
doi: 10.1007/s00438-013-0791-3 URL |
[23] |
Sun H, Fan HJ, Ling HQ. Genome-wide identification and characterization of the bHLH gene family in tomato[J]. BMC Genom, 2015, 16: 9.
doi: 10.1186/s12864-014-1209-2 URL |
[24] |
Waseem M, Li N, Su DD, et al. Overexpression of a basic helix-loop-helix transcription factor gene, SlbHLH22, promotes early flowering and accelerates fruit ripening in tomato(Solanum lycopersicum L.)[J]. Planta, 2019, 250(1): 173-185.
doi: 10.1007/s00425-019-03157-8 |
[25] |
Du J, Huang ZA, Wang B, et al. SlbHLH068 interacts with FER to regulate the iron-deficiency response in tomato[J]. Ann Bot, 2015, 116(1): 23-34.
doi: 10.1093/aob/mcv058 URL |
[26] |
Lau OS, Bergmann DC. Stomatal development: a plant's perspective on cell polarity, cell fate transitions and intercellular communication[J]. Development, 2012, 139(20): 3683-3692.
pmid: 22991435 |
[27] |
Lopez-Anido CB, Vatén A, Smoot NK, et al. Single-cell resolution of lineage trajectories in the Arabidopsis stomatal lineage and developing leaf[J]. Dev Cell, 2021, 56(7): 1043-1055.e4.
doi: 10.1016/j.devcel.2021.03.014 pmid: 33823130 |
[28] |
Lampard GR, MacAlister CA, Bergmann DC. Arabidopsis stomatal initiation is controlled by MAPK-mediated regulation of the bHLH SPEECHLESS[J]. Science, 2008, 322(5904): 1113-1116.
doi: 10.1126/science.1162263 URL |
[29] |
Yang KZ, Jiang M, Wang M, et al. Phosphorylation of serine 186 of bHLH transcription factor SPEECHLESS promotes stomatal development in Arabidopsis[J]. Mol Plant, 2015, 8(5): 783-795.
doi: 10.1016/j.molp.2014.12.014 URL |
[30] | 周晓今, 陈茹梅, 范云六. 植物对铁元素吸收、运输和储存的分子机制[J]. 作物研究, 2012, 26(5): 605-610. |
Zhou XJ, Chen RM, Fan YL. Molecular mechanism of iron uptake, translocation and storage in plants[J]. Crop Res, 2012, 26(5): 605-610. | |
[31] |
Connorton JM, Balk J, Rodríguez-Celma J. Iron homeostasis in plants - a brief overview[J]. Metallomics, 2017, 9(7): 813-823.
doi: 10.1039/c7mt00136c pmid: 28686269 |
[32] |
Mai HJ, Pateyron S, Bauer P. Iron homeostasis in Arabidopsis thaliana: transcriptomic analyses reveal novel FIT-regulated genes, iron deficiency marker genes and functional gene networks[J]. BMC Plant Biol, 2016, 16(1): 211.
doi: 10.1186/s12870-016-0899-9 URL |
[33] |
Gratz R, Manishankar P, Ivanov R, et al. CIPK11-dependent phosphorylation modulates FIT activity to promote Arabidopsis iron acquisition in response to calcium signaling[J]. Dev Cell, 2019, 48(5): 726-740.e10.
doi: 10.1016/j.devcel.2019.01.006 URL |
[34] |
Gratz R, Brumbarova T, Ivanov R, et al. Phospho-mutant activity assays provide evidence for alternative phospho-regulation pathways of the transcription factor Fer-like iron deficiency-induced transcription factor[J]. New Phytol, 2020, 225(1): 250-267.
doi: 10.1111/nph.v225.1 URL |
[35] |
Naranjo-Arcos MA, Maurer F, Meiser J, et al. Dissection of iron signaling and iron accumulation by overexpression of subgroup Ib bHLH039 protein[J]. Sci Rep, 2017, 7(1): 10911.
doi: 10.1038/s41598-017-11171-7 pmid: 28883478 |
[36] |
Legris M, Ince YÇ, Fankhauser C. Molecular mechanisms underlying phytochrome-controlled morphogenesis in plants[J]. Nat Commun, 2019, 10(1): 5219.
doi: 10.1038/s41467-019-13045-0 pmid: 31745087 |
[37] |
Chen M, Chory J. Phytochrome signaling mechanisms and the control of plant development[J]. Trends Cell Biol, 2011, 21(11): 664-671.
doi: 10.1016/j.tcb.2011.07.002 pmid: 21852137 |
[38] |
Leivar P, Monte E. PIFs: systems integrators in plant development[J]. Plant Cell, 2014, 26(1): 56-78.
doi: 10.1105/tpc.113.120857 URL |
[39] |
Lee N, Park J, Kim K, et al. The transcriptional coregulator LEUNIG_HOMOLOG inhibits light-dependent seed germination in Arabidopsis[J]. Plant Cell, 2015, 27(8): 2301-2313.
doi: 10.1105/tpc.15.00444 URL |
[40] |
Shi H, Zhong SW, Mo XR, et al. HFR1 sequesters PIF1 to govern the transcriptional network underlying light-initiated seed germination in Arabidopsis[J]. Plant Cell, 2013, 25(10): 3770-3784.
doi: 10.1105/tpc.113.117424 URL |
[41] |
Pham VN, Kathare PK, Huq E. Phytochromes and phytochrome interacting factors[J]. Plant Physiol, 2018, 176(2): 1025-1038.
doi: 10.1104/pp.17.01384 pmid: 29138351 |
[42] |
Xu XS, Paik I, Zhu L, et al. Illuminating progress in phytochrome-mediated light signaling pathways[J]. Trends Plant Sci, 2015, 20(10): 641-650.
doi: S1360-1385(15)00174-0 pmid: 26440433 |
[43] |
Paik I, Chen FL, Ngoc Pham V, et al. A phyB-PIF1-SPA1 kinase regulatory complex promotes photomorphogenesis in Arabidopsis[J]. Nat Commun, 2019, 10(1): 4216.
doi: 10.1038/s41467-019-12110-y |
[44] |
Ni WM, Xu SL, Chalkley RJ, et al. Multisite light-induced phosphorylation of the transcription factor PIF3 is necessary for both its rapid degradation and concomitant negative feedback modulation of photoreceptor phyB levels in Arabidopsis[J]. Plant Cell, 2013, 25(7): 2679-2698.
doi: 10.1105/tpc.113.112342 URL |
[45] |
Li L, Ljung K, Breton G, et al. Linking photoreceptor excitation to changes in plant architecture[J]. Genes Dev, 2012, 26(8): 785-790.
doi: 10.1101/gad.187849.112 URL |
[46] |
Holtkotte X, Dieterle S, Kokkelink L, et al. Mutations in the N-terminal kinase-like domain of the repressor of photomorphogenesis SPA1 severely impair SPA1 function but not light responsiveness in Arabidopsis[J]. Plant J, 2016, 88(2): 205-218.
doi: 10.1111/tpj.2016.88.issue-2 URL |
[47] |
Zhu JK. Abiotic stress signaling and responses in plants[J]. Cell, 2016, 167(2): 313-324.
doi: 10.1016/j.cell.2016.08.029 URL |
[48] |
Bailey PC, Martin C, Toledo-Ortiz G, et al. Update on the basic helix-loop-helix transcription factor gene family in Arabidopsis thaliana[J]. Plant Cell, 2003, 15(11): 2497-2502.
pmid: 14600211 |
[49] |
Li H, Ding YL, Shi YT, et al. MPK3- and MPK6-mediated ICE1 phosphorylation negatively regulates ICE1 stability and freezing tolerance in Arabidopsis[J]. Dev Cell, 2017, 43(5): 630-642.e4.
doi: 10.1016/j.devcel.2017.09.025 URL |
[50] |
Zhao CZ, Wang PC, Si T, et al. MAP kinase cascades regulate the cold response by modulating ICE1 protein stability[J]. Dev Cell, 2017, 43(5): 618-629.e5.
doi: S1534-5807(17)30783-9 pmid: 29056551 |
[51] |
Zhang ZY, Li JH, Li F, et al. OsMAPK3 phosphorylates OsbHLH002/OsICE1 and inhibits its ubiquitination to activate OsTPP1 and enhances rice chilling tolerance[J]. Dev Cell, 2017, 43(6): 731-743.e5.
doi: S1534-5807(17)30951-6 pmid: 29257952 |
[52] |
Ding YL, Li H, Zhang XY, et al. OST1 kinase modulates freezing tolerance by enhancing ICE1 stability in Arabidopsis[J]. Dev Cell, 2015, 32(3): 278-289.
doi: 10.1016/j.devcel.2014.12.023 URL |
[53] |
Goossens J, Mertens J, Goossens A. Role and functioning of bHLH transcription factors in jasmonate signalling[J]. J Exp Bot, 2017, 68(6): 1333-1347.
doi: 10.1093/jxb/erw440 pmid: 27927998 |
[54] |
Chen Q, Sun JQ, Zhai QZ, et al. The basic helix-loop-helix transcription factor MYC2 directly represses PLETHORA expression during jasmonate-mediated modulation of the root stem cell niche in Arabidopsis[J]. Plant Cell, 2011, 23(9): 3335-3352.
doi: 10.1105/tpc.111.089870 URL |
[55] |
Sheard LB, Tan X, Mao HB, et al. Jasmonate perception by inositol-phosphate-potentiated COI1-JAZ co-receptor[J]. Nature, 2010, 468(7322): 400-405.
doi: 10.1038/nature09430 |
[56] | An CP, Li L, Zhai QZ, et al. Mediator subunit MED25 links the jasmonate receptor to transcriptionally active chromatin[J]. Proc Natl Acad Sci USA, 2017, 114(42): E8930-E8939. |
[57] |
Wang H, Li SY, Li YA, et al. MED25 connects enhancer-promoter looping and MYC2-dependent activation of jasmonate signalling[J]. Nat Plants, 2019, 5(6): 616-625.
doi: 10.1038/s41477-019-0441-9 pmid: 31182849 |
[58] |
Zander M, Lewsey MG, Clark NM, et al. Integrated multi-omics framework of the plant response to jasmonic acid[J]. Nat Plants, 2020, 6(3): 290-302.
doi: 10.1038/s41477-020-0605-7 pmid: 32170290 |
[59] |
Liu YY, Du MM, Deng L, et al. MYC2 regulates the termination of jasmonate signaling via an autoregulatory negative feedback loop[J]. Plant Cell, 2019, 31(1): 106-127.
doi: 10.1105/tpc.18.00405 URL |
[60] |
Song C, Cao YP, Dai J, et al. The multifaceted roles of MYC2 in plants: toward transcriptional reprogramming and stress tolerance by jasmonate signaling[J]. Front Plant Sci, 2022, 13: 868874.
doi: 10.3389/fpls.2022.868874 URL |
[61] |
Shin J, Heidrich K, Sanchez-Villarreal A, et al. TIME FOR COFFEE represses accumulation of the MYC2 transcription factor to provide time-of-day regulation of jasmonate signaling in Arabidopsis[J]. Plant Cell, 2012, 24(6): 2470-2482.
doi: 10.1105/tpc.111.095430 URL |
[62] |
Chico JM, Fernández-Barbero G, Chini A, et al. Repression of jasmonate-dependent defenses by shade involves differential regulation of protein stability of MYC transcription factors and their JAZ repressors in Arabidopsis[J]. Plant Cell, 2014, 26(5): 1967-1980.
doi: 10.1105/tpc.114.125047 URL |
[63] |
Zhai QZ, Yan LH, Tan D, et al. Phosphorylation-coupled proteolysis of the transcription factor MYC2 is important for jasmonate-signaled plant immunity[J]. PLoS Genet, 2013, 9(4): e1003422.
doi: 10.1371/journal.pgen.1003422 URL |
[64] |
Guo HQ, Nolan TM, Song GY, et al. FERONIA receptor kinase contributes to plant immunity by suppressing jasmonic acid signaling in Arabidopsis thaliana[J]. Curr Biol, 2018, 28(20): 3316-3324.e6.
doi: 10.1016/j.cub.2018.07.078 URL |
[65] |
Wang MM, Tian YC, Han C, et al. Phospho-mutant activity assays provide evidence for the negative regulation of transcriptional regulator PRE1 by phosphorylation[J]. Int J Mol Sci, 2020, 21(23): 9183.
doi: 10.3390/ijms21239183 URL |
[66] |
Zhu L, Bu QY, Xu XS, et al. CUL4 forms an E3 ligase with COP1 and SPA to promote light-induced degradation of PIF1[J]. Nat Commun, 2015, 6: 7245.
doi: 10.1038/ncomms8245 pmid: 26037329 |
[67] |
Jeong JS, Jung C, Seo JS, et al. The deubiquitinating enzymes UBP12 and UBP13 positively regulate MYC2 levels in jasmonate responses[J]. Plant Cell, 2017, 29(6): 1406-1424.
doi: 10.1105/tpc.17.00216 URL |
[68] |
An JP, Zhang XW, Bi SQ, et al. MdbHLH93, an apple activator regulating leaf senescence, is regulated by ABA and MdBT2 in antagonistic ways[J]. New Phytol, 2019, 222(2): 735-751.
doi: 10.1111/nph.2019.222.issue-2 URL |
[1] | 熊淑琪. 胆汁酸生理功能及其与肠道微生物互作研究进展[J]. 生物技术通报, 2023, 39(4): 187-200. |
[2] | 梁星星, 王佳, 许文涛. 抗病毒核苷酸类似物磷酸化修饰研究进展[J]. 生物技术通报, 2022, 38(2): 218-226. |
[3] | 段绪果, 张玉华, 黄婷婷, 丁乾, 栾舒越, 朱秋雨. 化学分子伴侣及诱导条件协同强化Thermotoga maritima α-葡聚糖磷酸化酶可溶性表达[J]. 生物技术通报, 2021, 37(8): 233-242. |
[4] | 赵阿慧, 王宪国, 董剑, 侯佐, 赵万春, 高翔, 杨明明. 植物磷脂酶C在应答胁迫反应中的研究进展[J]. 生物技术通报, 2021, 37(5): 154-164. |
[5] | 刘静, 李亚超, 周梦岩, 吴鹏飞, 马祥庆, 李明. 植物蛋白质翻译后修饰组学研究进展[J]. 生物技术通报, 2021, 37(1): 67-76. |
[6] | 侯成林, 杨艳坤, 陈嘉荔, 白仲虎. Mxr1磷酸化水平受Ptp调控机理的初步研究[J]. 生物技术通报, 2019, 35(7): 108-113. |
[7] | 李露露, 曲长凤, 郑洲, 王以斌, 缪锦来, 张莉. 藻类水通道蛋白的研究进展[J]. 生物技术通报, 2017, 33(8): 1-6. |
[8] | 袁敏,齐玉荣,王瑞菊,. 蛋白激酶BIN2的纯化及活性分析[J]. 生物技术通报, 2017, 33(7): 145-149. |
[9] | 华晓雨, 陶爽, 孙盛楠, 郭娜, 阎秀峰, 蔺吉祥. 植物次生代谢产物-酚类化合物的研究进展[J]. 生物技术通报, 2017, 33(12): 22-29. |
[10] | 程庆灵, 王敬强,. 同源异型框蛋白Msx1的两个新的磷酸化位点的鉴定[J]. 生物技术通报, 2016, 32(6): 211-218. |
[11] | 刘妍, 孟志刚, 孙国清, 王远, 周焘, 郭三堆, 张锐. 陆地棉GhPYR1基因的克隆和功能分析[J]. 生物技术通报, 2016, 32(2): 90-99. |
[12] | 王洁, 余磊, 杨东, 李婕, 王洪钟. 基于酵母表面展示技术的胸苷磷酸化酶全细胞催化剂的构建[J]. 生物技术通报, 2016, 32(1): 201-206. |
[13] | 白桦,崔雪琼,白少星,姚新灵. 马铃薯AGPase活力反馈调控光合速率定量分析[J]. 生物技术通报, 2014, 0(11): 125-129. |
[14] | 吴睿睿,朱福兴. 金黄色葡萄球菌SarA家族蛋白及其翻译后修饰[J]. 生物技术通报, 2013, 0(10): 40-45. |
[15] | 李茹;陈鹏;. 细菌趋化性的信号传导及调节机制研究进展[J]. , 2011, 0(11): 54-57. |
阅读次数 | ||||||
全文 |
|
|||||
摘要 |
|
|||||