细菌转录终止的分子机制研究进展

doi:10.16288/j.yczz.24-244

[an error occurred while processing this directive]

Hereditas(Beijing) ›› 2024, Vol. 46 ›› Issue (12): 982-994.doi: 10.16288/j.yczz.24-244

• Special Section: Excellent Doctoral Thesis • Previous Articles Next Articles

Progress on molecular mechanisms of bacterial transcription termination

Linlin You¹^,²^,³(), Yu Zhang¹()

1. Key Laboratory of Synthetic Biology, CAS Center for Excellence in Molecular Plant Sciences, Shanghai 200032, China
2. University of Chinese Academy of Sciences, Beijing 100049, China
3. Waksman Institute of Microbiology, Rutgers University, Piscataway, NJ 08854, USA

Received:2024-08-21 Revised:2024-10-12 Online:2024-12-20 Published:2024-10-25
Contact: Yu Zhang E-mail:youlinlin2016@gmail.com;yzhang@cemps.ac.cn
Supported by:
Supported by the Basic Research Zone Program of Shanghai(JCYJ-SHFY-2022-012);National Key Research and Development Program of China(2018YFA0903701);Strategic Priority Research Program of the CAS(CAS XDB29020000)

Abstract

Abstract:

Transcription is the process by which genetic information is copied from DNA to RNA, and it can be divided into three stages: transcription initiation, elongation, and termination. Transcription termination is the last step of gene transcription and is crucial for accurate gene expression. Two prevailing modes of transcription termination exist in bacteria: Rho-dependent termination and intrinsic termination (Rho-independent termination). Transcription termination is positively and negatively regulated by bacterial or bacteriophage proteins. In this review, we summarize the research progress of bacterial transcription and its regulation, with the aim of providing a theoretical foundation for further studies and understanding of transcription termination process.

Key words: transcription, RNA polymerase, transcription termination, transcription regulation

Linlin You, Yu Zhang. Progress on molecular mechanisms of bacterial transcription termination[J]. Hereditas(Beijing), 2024, 46(12): 982-994.

Figures/Tables 4

References 75

[1]	Crick F. Central dogma of molecular biology. Nature, 1970, 227(5258): 561-563.
[2]	Chen J, Chiu C, Gopalkrishnan S, Chen AY, Olinares PDB, Saecker RM, Winkelman JT, Maloney MF, Chait BT, Ross W, Gourse RL, Campbell EA, Darst SA. Stepwise promoter melting by bacterial RNA polymerase. Mol Cell, 2020, 78(2): 275-288.e6. doi: S1097-2765(20)30110-6 pmid: 32160514
[3]	Feklistov A, Darst SA. Structural basis for promoter-10 element recognition by the bacterial RNA polymerase σ subunit. Cell, 2011, 147(6): 1257-1269. doi: 10.1016/j.cell.2011.10.041 pmid: 22136875
[4]	Campbell EA, Muzzin O, Chlenov M, Sun JL, Olson CA, Weinman O, Trester-Zedlitz ML, Darst SA. Structure of the bacterial RNA polymerase promoter specificity sigma subunit. Mol Cell, 2002, 9(3): 527-539. pmid: 11931761
[5]	Ross W, Gosink KK, Salomon J, Igarashi K, Zou C, Ishihama A, Severinov K, Gourse RL. A third recognition element in bacterial promoters: DNA binding by the alpha subunit of RNA polymerase. Science, 1993, 262(5138): 1407-1413. doi: 10.1126/science.8248780 pmid: 8248780
[6]	Boyaci H, Chen J, Jansen R, Darst SA, Campbell EA. Structures of an RNA polymerase promoter melting intermediate elucidate DNA unwinding. Nature, 2019, 565(7739): 382-385.
[7]	Chen J, Boyaci H, Campbell EA. Diverse and unified mechanisms of transcription initiation in bacteria. Nat Rev Microbiol, 2021, 19(2): 95-109. doi: 10.1038/s41579-020-00450-2 pmid: 33122819
[8]	Revyakin A, Liu CY, Ebright RH, Strick TR. Abortive initiation and productive initiation by RNA polymerase involve DNA scrunching. Science, 2006, 314(5802): 1139-1143. doi: 10.1126/science.1131398 pmid: 17110577
[9]	Li LT, Molodtsov V, Lin W, Ebright RH, Zhang Y. RNA extension drives a stepwise displacement of an initiation-factor structural module in initial transcription. Proc Natl Acad Sci USA, 2020, 117(11): 5801-5809. doi: 10.1073/pnas.1920747117 pmid: 32127479
[10]	Vassylyev DG, Vassylyeva MN, Perederina A, Tahirov TH, Artsimovitch I. Structural basis for transcription elongation by bacterial RNA polymerase. Nature, 2007, 448(7150): 157-162.
[11]	Landick R. The regulatory roles and mechanism of transcriptional pausing. Biochem Soc Trans, 2006, 34(6): 1062-1066.
[12]	Farnham PJ, Greenblatt J, Platt T. Effects of NusA protein on transcription termination in the tryptophan operon of Escherichia coli. Cell, 1982, 29(3): 945-951. pmid: 6758952
[13]	Schmidt MC, Chamberlin MJ. Nusa protein of Escherichia coli is an efficient transcription termination factor for certain terminator sites. J Mol Biol, 1987, 195(4): 809-818. pmid: 2821282
[14]	Yakhnin AV, Babitzke P. NusA-stimulated RNA polymerase pausing and termination participates in the Bacillus subtilis trp operon attenuation mechanism invitro. Proc Natl Acad Sci USA, 2002, 99(17): 11067-11072. doi: 10.1073/pnas.162373299 pmid: 12161562
[15]	Guo XY, Myasnikov AG, Chen J, Crucifix C, Papai G, Takacs M, Schultz P, Weixlbaumer A. Structural basis for NusA stabilized transcriptional pausing. Mol Cell, 2018, 69(5): 816-827.e4. doi: S1097-2765(18)30106-0 pmid: 29499136
[16]	You LL, Shi J, Shen LQ, Li LT, Fang CL, Yu CZ, Cheng WB, Feng Y, Zhang Y. Structural basis for transcription antitermination at bacterial intrinsic terminator. Nat Commun, 2019, 10(1): 3048. doi: 10.1038/s41467-019-10955-x pmid: 31296855
[17]	Krupp F, Said N, Huang YH, Loll B, Bürger J, Mielke T, Spahn CMT, Wahl MC. Structural basis for the action of an all-purpose transcription anti-termination factor. Mol Cell, 2019, 74(1): 143-157.e5. doi: S1097-2765(19)30036-X pmid: 30795892
[18]	Shi J, Gao X, Tian TG, Yu ZY, Gao B, Wen AJ, You LL, Chang SH, Zhang X, Zhang Y, Feng Y. Structural basis of Q-dependent transcription antitermination. Nat Commun, 2019, 10(1): 2925. doi: 10.1038/s41467-019-10958-8 pmid: 31266960
[19]	Yin Z, Kaelber JT, Ebright RH. Structural basis of Q-dependent antitermination. Proc Natl Acad Sci USA, 2019, 116(37): 18384-18390. doi: 10.1073/pnas.1909801116 pmid: 31455742
[20]	Ray-Soni A, Bellecourt MJ, Landick R. Mechanisms of bacterial transcription termination: all good things must end. Annu Rev Biochem, 2016, 85: 319-347. doi: 10.1146/annurev-biochem-060815-014844 pmid: 27023849
[21]	Santangelo TJ, Artsimovitch I. Termination and antitermination: RNA polymerase runs a stop sign. Nat Rev Microbiol, 2011, 9(5): 319-329. doi: 10.1038/nrmicro2560 pmid: 21478900
[22]	Roberts JW. Mechanisms of bacterial transcription termination. J Mol Biol, 2019, 431(20): 4030-4039. doi: S0022-2836(19)30185-8 pmid: 30978344
[23]	Kang JY, Llewellyn E, Chen J, Olinares PDB, Brewer J, Chait BT, Campbell EA, Darst SA. Structural basis for transcription complex disruption by the Mfd translocase. eLife, 2021, 10: e62117.
[24]	Selby CP, Sancar A. Molecular mechanism of transcription- repair coupling. Science, 1993, 260(5104): 53-58. doi: 10.1126/science.8465200 pmid: 8465200
[25]	Shi J, Wen AJ, Zhao MX, Jin S, You LL, Shi Y, Dong SL, Hua XT, Zhang Y, Feng Y. Structural basis of Mfd-dependent transcription termination. Nucleic Acids Res, 2020, 48(20): 11762-11772. doi: 10.1093/nar/gkaa904 pmid: 33068413
[26]	Wang L, Watters JW, Ju XW, Lu GZ, Liu SX. Head-on and co-directional RNA polymerase collisions orchestrate bidirectional transcription termination. Mol Cell, 2023, 83(7): 1153-1164.e4. doi: 10.1016/j.molcel.2023.02.017 pmid: 36917983
[27]	Roberts JW. Termination factor for RNA synthesis. Nature, 1969, 224(5225): 1168-1174.
[28]	De Crombrugghe B, Adhya S, Gottesman M, Pastan I. Effect of Rho on transcription of bacterial operons. Nat New Biol, 1973, 241(113): 260-264.
[29]	Opperman T, Richardson JP. Phylogenetic analysis of sequences from diverse bacteria with homology to the Escherichia coli rho gene. J Bacteriol, 1994, 176(16): 5033-5043. pmid: 8051015
[30]	Grylak-Mielnicka A, Bidnenko V, Bardowski J, Bidnenko E. Transcription termination factor Rho: a hub linking diverse physiological processes in bacteria. Microbiology (Reading), 2016, 162(3): 433-447. doi: 10.1099/mic.0.000244 pmid: 26796109
[31]	Riaz-Bradley A. Transcription in cyanobacteria: a distinctive machinery and putative mechanisms. Biochem Soc Trans, 2019, 47(2): 679-689.
[32]	Peters JM, Mooney RA, Grass JA, Jessen ED, Tran F, Landick R. Rho and NusG suppress pervasive antisense transcription in Escherichia coli. Genes Dev, 2012, 26(23): 2621-2633.
[33]	Richardson JP, Grimley C, Lowery C. Transcription termination factor rho activity is altered in Escherichia coli with suA gene mutations. Proc Natl Acad Sci USA, 1975, 72(5): 1725-1728. pmid: 1098042
[34]	Cardinale CJ, Washburn RS, Tadigotla VR, Brown LM, Gottesman ME, Nudler E. Termination factor Rho and its cofactors NusA and NusG silence foreign DNA in E. coli. Science, 2008, 320(5878): 935-938.
[35]	Peters JM, Mooney RA, Kuan PF, Rowland JL, Keles S, Landick R. Rho directs widespread termination of intragenic and stable RNA transcription. Proc Natl Acad Sci USA, 2009, 106(36): 15406-15411. doi: 10.1073/pnas.0903846106 pmid: 19706412
[36]	Dutta D, Shatalin K, Epshtein V, Gottesman ME, Nudler E. Linking RNA polymerase backtracking to genome instability in E. coli. Cell, 2011, 146(4): 533-543.
[37]	Leela JK, Syeda AH, Anupama K, Gowrishankar J. Rho-dependent transcription termination is essential to prevent excessive genome-wide R-loops in Escherichia coli. Proc Natl Acad Sci USA, 2013, 110(1): 258-263.
[38]	Mitra P, Ghosh G, Hafeezunnisa M, Sen RJ. Rho protein: roles and mechanisms. Annu Rev Microbiol, 2017, 71: 687-709. doi: 10.1146/annurev-micro-030117-020432 pmid: 28731845
[39]	Geiselmann J, Seifried SE, Yager TD, Liang C, von Hippel PH. Physical properties of the Escherichia coli transcription termination factor rho. 2. Quaternary structure of the rho hexamer. Biochemistry, 1992, 31(1): 121-132. pmid: 1370624
[40]	Geiselmann J, Yager TD, Gill SC, Calmettes P, von Hippel PH. Physical properties of the Escherichia coli transcription termination factor rho. 1. Association states and geometry of the rho hexamer. Biochemistry, 1992, 31(1): 111-121. pmid: 1370623
[41]	Kang JY, Mooney RA, Nedialkov Y, Saba J, Mishanina TV, Artsimovitch I, Landick R, Darst SA. Structural basis for transcript elongation control by NusG family universal regulators. Cell, 2018, 173(7): 1650-1662.e14. doi: S0092-8674(18)30594-4 pmid: 29887376
[42]	Sullivan SL, Gottesman ME. Requirement for E. coli NusG protein in factor-dependent transcription termination. Cell, 1992, 68(5): 989-994. pmid: 1547498
[43]	Martinez-Rucobo FW, Sainsbury S, Cheung ACM, Cramer P. Architecture of the RNA polymerase-Spt4/5 complex and basis of universal transcription processivity. EMBO J, 2011, 30(7): 1302-1310. doi: 10.1038/emboj.2011.64 pmid: 21386817
[44]	Lawson MR, Ma W, Bellecourt MJ, Artsimovitch I, Martin A, Landick R, Schulten K, Berger JM. Mechanism for the regulated control of bacterial transcription termination by a universal adaptor protein. Mol Cell, 2018, 71(6): 911-922.e4. doi: S1097-2765(18)30583-5 pmid: 30122535
[45]	Skordalakes E, Berger JM. Structure of the Rho transcription terminator: mechanism of mRNA recognition and helicase loading. Cell, 2003, 114(1): 135-146. pmid: 12859904
[46]	Thomsen ND, Berger JM. Running in reverse: the structural basis for translocation polarity in hexameric helicases. Cell, 2009, 139(3): 523-534. doi: 10.1016/j.cell.2009.08.043 pmid: 19879839
[47]	Molodtsov V, Wang CY, Firlar E, Kaelber JT, Ebright RH. Structural basis of Rho-dependent transcription termination. Nature, 2023, 614(7947): 367-374.
[48]	Park JS, Roberts JW. Role of DNA bubble rewinding in enzymatic transcription termination. Proc Natl Acad Sci USA, 2006, 103(13): 4870-4875.
[49]	Richardson JP. Rho-dependent termination and ATPases in transcript termination. Biochim Biophys Acta, 2002, 1577(2): 251-260. pmid: 12213656
[50]	Mooney RA, Davis SE, Peters JM, Rowland JL, Ansari AZ, Landick R. Regulator trafficking on bacterial transcription units in vivo. Mol Cell, 2009, 33(1): 97-108.
[51]	Said N, Hilal T, Sunday ND, Khatri A, Burger J, Mielke T, Belogurov GA, Loll B, Sen R, Artsimovitch I, Wahl MC. Steps toward translocation-independent RNA polymerase inactivation by terminator ATPase ρ. Science, 2021, 371(6524): eabd1673.
[52]	Hao ZT, Epshtein V, Kim KH, Proshkin S, Svetlov V, Kamarthapu V, Bharati B, Mironov A, Walz T, Nudler E. Pre-termination transcription complex: structure and function. Mol Cell, 2021, 81(2): 281-292.e8. doi: 10.1016/j.molcel.2020.11.013 pmid: 33296676
[53]	Gusarov I, Nudler E. The mechanism of intrinsic transcription termination. Mol Cell, 1999, 3(4): 495-504. pmid: 10230402
[54]	Yarnell WS, Roberts JW. Mechanism of intrinsic transcription termination and antitermination. Science, 1999, 284(5414): 611-615. pmid: 10213678
[55]	You LL, Omollo EO, Yu CZ, Mooney RA, Shi J, Shen LQ, Wu XX, Wen AJ, He DW, Zeng Y, Feng Y, Landick R, Zhang Y. Structural basis for intrinsic transcription termination. Nature, 2023, 613(7945): 783-789.
[56]	Kang JY, Mishanina TV, Bellecourt MJ, Mooney RA, Darst SA, Landick R. RNA polymerase accommodates a pause RNA hairpin by global conformational rearrangements that prolong pausing. Mol Cell, 2018, 69(5): 802-815.e5. doi: S1097-2765(18)30047-9 pmid: 29499135
[57]	Santangelo TJ, Roberts JW. Forward translocation is the natural pathway of RNA release at an intrinsic terminator. Mol Cell, 2004, 14(1): 117-126. pmid: 15068808
[58]	Larson MH, Greenleaf WJ, Landick R, Block SM. Applied force reveals mechanistic and energetic details of transcription termination. Cell, 2008, 132(6): 971-982. doi: 10.1016/j.cell.2008.01.027 pmid: 18358810
[59]	Komissarova N, Becker J, Solter S, Kireeva M, Kashlev M. Shortening of RNA:DNA hybrid in the elongation complex of RNA polymerase is a prerequisite for transcription termination. Mol Cell, 2002, 10(5): 1151-1162. pmid: 12453422
[60]	Epshtein V, Cardinale CJ, Ruckenstein AE, Borukhov S, Nudler E. An allosteric path to transcription termination. Mol Cell, 2007, 28(6): 991-1001. pmid: 18158897
[61]	Peters JM, Vangeloff AD, Landick R. Bacterial transcription terminators: the RNA 3'-end chronicles. J Mol Biol, 2011, 412(5): 793-813. doi: 10.1016/j.jmb.2011.03.036 pmid: 21439297
[62]	Kang W, Ha KS, Uhm H, Park K, Lee JY, Hohng S, Kang C. Transcription reinitiation by recycling RNA polymerase that diffuses on DNA after releasing terminated RNA. Nat Commun, 2020, 11(1): 450. doi: 10.1038/s41467-019-14200-3 pmid: 31974350
[63]	Harden TT, Herlambang KS, Chamberlain M, Lalanne JB, Wells CD, Li GW, Landick R, Hochschild A, Kondev J, Gelles J. Alternative transcription cycle for bacterial RNA polymerase. Nat Commun, 2020, 11(1): 448. doi: 10.1038/s41467-019-14208-9 pmid: 31974358
[64]	Kouba T, Koval' T, Sudzinová P, Pospíšil J, Brezovská B, Hnilicová J, Šanderová H, Janoušková M, Šiková M, Halada P, Sýkora M, Barvík I, Nováček J, Trundová M, Dušková J, Skálová T, Chon U, Murakami KS, Dohnálek J, Krásný L. Mycobacterial HelD is a nucleic acids-clearing factor for RNA polymerase. Nat Commun, 2020, 11(1): 6419. doi: 10.1038/s41467-020-20158-4 pmid: 33339823
[65]	Inlow K, Tenenbaum D, Friedman LJ, Kondev J, Gelles J. Recycling of bacterial RNA polymerase by the Swi2/Snf2 ATPase RapA. Proc Natl Acad Sci USA, 2023, 120(28): e2303849120.
[66]	Deaconescu AM, Chambers AL, Smith AJ, Nickels BE, Hochschild A, Savery NJ, Darst SA. Structural basis for bacterial transcription-coupled DNA repair. Cell, 2006, 124(3): 507-520. doi: 10.1016/j.cell.2005.11.045 pmid: 16469698
[67]	Adebali O, Chiou YY, Hu JC, Sancar A, Selby CP. Genome-wide transcription-coupled repair in Escherichia coli is mediated by the Mfd translocase. Proc Natl Acad Sci USA, 2017, 114(11): E2116-E2125.
[68]	Ju XW, Li DY, Liu SX. Full-length RNA profiling reveals pervasive bidirectional transcription terminators in bacteria. Nat Microbiol, 2019, 4(11): 1907-1918. doi: 10.1038/s41564-019-0500-z pmid: 31308523
[69]	Gutierrez P, Kozlov G, Gabrielli L, Elias D, Osborne MJ, Gallouzi IE, Gehring K. Solution structure of YaeO, a Rho-specific inhibitor of transcription termination. J Biol Chem, 2007, 282(32): 23348-23353. doi: 10.1074/jbc.M702010200 pmid: 17565995
[70]	Said N, Finazzo M, Hilal T, Wang B, Selinger TL, Gjorgjevikj D, Artsimovitch I, Wahl MC. Sm-like protein Rof inhibits transcription termination factor ρ by binding site obstruction and conformational insulation. Nat Commun, 2024, 15(1): 3186. doi: 10.1038/s41467-024-47439-6 pmid: 38622114
[71]	Zhang J, Zhang S, Zhou W, Zhang X, Li GJ, Li RX, Lin XY, Chen ZY, Liu F, Shen P, Zhou XG, Gao Y, Chen ZG, Chao YJ, Wang CY. A widely conserved protein Rof inhibits transcription termination factor Rho and promotes Salmonella virulence program. Nat Commun, 2024, 15(1): 3187. doi: 10.1038/s41467-024-47438-7 pmid: 38622116
[72]	Sauer B, Ow D, Ling L, Calendar R. Mutants of satellite bacteriophage P4 that are defective in the suppression of transcriptional polarity. J Mol Biol, 1981, 145(1): 29-46. pmid: 7021852
[73]	Magyar A, Zhang X, Abdi F, Kohn H, Widger WR. Identifying the bicyclomycin binding domain through biochemical analysis of antibiotic-resistant Rho proteins. J Biol Chem, 1999, 274(11): 7316-7324. doi: 10.1074/jbc.274.11.7316 pmid: 10066795
[74]	Skordalakes E, Brogan AP, Park BS, Kohn H, Berger JM. Structural mechanism of inhibition of the Rho transcription termination factor by the antibiotic bicyclomycin. Structure, 2005, 13(1): 99-109. pmid: 15642265
[75]	Lawson MR, Dyer K, Berger JM. Ligand-induced and small-molecule control of substrate loading in a hexameric helicase. Proc Natl Acad Sci USA, 2016, 113(48): 13714-13719. pmid: 27821776

Metrics

Comments

www.chinagene.cn
备案号：京ICP备09063187号

Progress on molecular mechanisms of bacterial transcription termination

RichHTML

PDF (PC)

Knowledge

Abstract

Cite this article

share this article

Figures/Tables 4

References 75

Related Articles 15

Recommended Articles

Metrics

Comments

[1]	Jilong Wang, Qing Li, Tingzheng Zhan. Principle and application of self-transcribing active regulatory region sequencing in enhancer discovery research [J]. Hereditas(Beijing), 2024, 46(8): 589-602.
[2]	Zhaoran Sun, Xudong Wu. The roles and mechanisms of histone variant H2A.Z in transcriptional regulation [J]. Hereditas(Beijing), 2024, 46(4): 279-289.
[3]	Jiaxin Hong, Song’en Xu, Wenqing Zhang, Wei Liu. The interaction of Pu.1 and cMyb in zebrafish neutrophil development [J]. Hereditas(Beijing), 2024, 46(4): 319-332.
[4]	Qi Li, Zhicheng Dong, Min Liu. The carboxy-terminal domain of RNA polymerase II large subunit: simple repeats are not simple [J]. Hereditas(Beijing), 2024, 46(12): 1028-1041.
[5]	Meng Yuan, Hui Li, Shouzhi Wang. Massively parallel reporter assay: a novel technique for analyzing the regulation of gene expression [J]. Hereditas(Beijing), 2023, 45(10): 859-873.
[6]	Dandan Wu, Mingkun Zhu, Zhongyan Fang, Wei Ma. Progress on molecular composition and genetic mechanism of plant B chromosomes [J]. Hereditas(Beijing), 2022, 44(9): 772-782.
[7]	Fengyu Sun, Qianghua Xu. Research progress of microRNAs involved in hematopoiesis [J]. Hereditas(Beijing), 2022, 44(9): 756-771.
[8]	Rongrong Mu, Qingqing Niu, Yuqiang Sun, Jun Mei, Meng Miao. Cloning and characterization of the MYB transcription factor gene GhTT2 in Gossypium hirsutum [J]. Hereditas(Beijing), 2022, 44(8): 720-728.
[9]	Yuan Zhang, Yuting Zhao, Lenan Zhuang, Jin He. Transcriptional regulation of transcriptional Mediator complexes in cardiovascular development and disease [J]. Hereditas(Beijing), 2022, 44(5): 383-397.
[10]	Haoliang Cui, Peihua Shi, Jinchun Gao, Xinbo Zhang, Shunran Zhao, Chenyu Tao. Progress on the study of nucleosome reorganization during cellular reprogramming [J]. Hereditas(Beijing), 2022, 44(3): 208-215.
[11]	Guofang Liu, Peidong Ren, Wenxin Ye, Guangtao Lu. Analysis of transcriptional regulators HpaR1 and Clp regulating the expression of glycoside hydrolase-encoding gene in the Xanthomonas campestris pv. campestris [J]. Hereditas(Beijing), 2021, 43(9): 910-920.
[12]	Tianyi Wang, Yingxiang Wang, Chenjiang You. Structural and functional characteristics of plant PHD domain-containing proteins [J]. Hereditas(Beijing), 2021, 43(4): 323-339.
[13]	Menggang Lv, Aijia Liu, Qingwei Li, Peng Su. Progress on the origin, function and evolutionary mechanism of RHR transcription factor family [J]. Hereditas(Beijing), 2021, 43(3): 215-225.
[14]	Yuanyuan Hao, Xiangqian Zhao, Fudeng Huang, Chunshou Li. The role of PPR proteins in posttranscriptional regulation of organelle components in plants [J]. Hereditas(Beijing), 2021, 43(11): 1050-1065.
[15]	Guofang Liu, Xinxin Wang, Huizhao Su, Guangtao Lu. Progress on the GntR family transcription regulators in bacteria [J]. Hereditas(Beijing), 2021, 43(1): 66-73.