植物碱基错配修复系统中Muts蛋白家族研究进展

doi:10.3969/j.issn.1006-8082.2017.05.002

摘要/Abstract

摘要： DNA错配修复（mismatch repair， MMR）是DNA损伤修复的一个重要途径，主要用于细胞中DNA合成和遗传重组时发生损伤过程中出现的单个或少数碱基的缺失、插入以及错配的修复，它对维持基因组稳定性和DNA复制保真度至关重要。原核生物和真核生物中都有非常保守的MMR系统。在人体DNA修复系统的研究中，发现癌症的发生与Muts蛋白家族功能缺陷密切相关。类似的在拟南芥和水稻中功能缺陷的Muts蛋白家族（同源蛋白Muts homolog，MSH）会产生增变基因表型，这将为植物的基因功能分析和育种利用奠定基础。基于此，本文综述了近年来有关植物DNA错配修复及相关基因功能的研究进展，特别是植物MMR功能缺陷导致基因突变和微卫星不稳定造成的性状畸形进行了描述，对Muts蛋白家族各个亚基功能做了分类说明，并对植物中如何利用MSH产生的增变基因突变和如何利用突变育种研究进行了展望。

关键词: 水稻, DNA错配修复, Muts蛋白家族, 同源重组, 突变, 稳定

Abstract: DNA mismatch repair （mismatch repair, MMR） is an important way of DNA damage repair, and it is mainly used to repair the lack of a single or a few bases, insert and mismatch in the process of DNA damage occurred when DNA synthesis and genetic recombination in the cell, which is very important to maintain genomic stability and DNA replication fidelity. MMR systems are very conservative in both prokaryotes and eukaryotes. It was found that the occurrence of cancer is closely associated with functional defect of the Muts-protein family in the study of human DNA repair system. Similarly, it has been found that functional defect of the Muts-protein family will appear gene mutant or phenotypes in the Arabidopsis and rice, which will lay the foundation for the further study of plant functional gene analysis and breeding. In this paper, the author reviewed recent advances in the research of mismatch repair of plant DNA and the function of related genes, especially the mutations caused by plant MMR functional defects and microsatellite instability. It is suggested that MMR mutants can be used as a reference for further breeding of MMR-deficient mutants.

Key words: rice, DNA mismatch repair, Muts-protein family, homologous recombination, mutation, stability

中图分类号:

S511

丰安徽1，3,王伍梅2,李桂娇4,郭龙彪1,张效忠2*, 崔永涛1*. 植物碱基错配修复系统中Muts蛋白家族研究进展[J]. 中国稻米, DOI: 10.3969/j.issn.1006-8082.2017.05.002 .

参考文献

[1] Manova V, Gruszka D. DNA damage and repair in plants-from models to crops[J]. Front Plant Sci, 2015, 6: 885. [2] Bray C M, West C E. DNA repair mechanisms in plants: crucial sensors and effectors for the maintenance of genome integrity[J]. New Phytol, 2005, 168（3）: 511-528. [3] Horwath M, Kramer W, Kunze R. Structure and expression of the Zea mays mutS-homologs Mus1 and Mus2 [J]. Theor Appl Genet, 2002, 105（2-3）: 423-430. [4] Rastogi R P, Richa, Kumar A, et al. Molecular mechanisms of ultraviolet radiation-induced DNA damage and repair [J]. J Nucleic Acids, 2010, 6551: 592 980. [5] Lario L D, Ramirez-Parra E, Gutierrez C, et al. Regulation of plant MSH2 and MSH6 genes in the UV-B-induced DNA damage response [J]. J Exp Bot, 2011, 62（8）: 2 925-2 937. [6] Culligan K M, Hays J B. Arabidopsis MutS homologs-AtMSH2, AtMSH3, AtMSH6, and a novel AtMSH7-form three distinct protein heterodimers with different specificities for mismatched DNA [J]. Plant Cell, 2000, 12（6）: 991-1 002. [7] Puchta H, Hohn B. From centiMorgans to base pairs: homologous recombination in plants[J]. Trends Plant Sci, 1996, 1（10）: 340-348. [8] Waterworth W M, Drury G E, Bray C M, et al. Repairing breaks in the plant genome: the importance of keeping it together [J]. New Phytol, 2011, 192（4）: 805-822. [9] Spampinato C P, Gomez R L, Galles C, et al. From bacteria to plants: A compendium of mismatch repair assays [J]. MutatRes, 2009, 682（2-3）: 110-128. [10] Iyer R R, Pluciennik A, Burdett V, et al. DNA mismatch repair: functions and mechanisms[J]. Chem Rev, 2006, 106（2）: 302-323. [11] Kunkel T A, Erie D A. DNA Mismatch Repair [J]. Annu Rev Biochem, 2005, 74: 681-710. [12] Modrich P. Mechanisms in eukaryotic mismatch repair [J]. J Biol Chem, 2006, 281（41）: 30 305-30 309. [13] Marti T M, Kunz C, Fleck O. DNA mismatch repair and mutation avoidance pathways[J]. J Cell Physiol, 2002, 191（1）: 28-41. [14] Golubov A, Yao Y, Maheshwari P, etal. Microsatellite instability in Arabidopsis increases with plant development[J]. Plant Physiol, 2010, 154（3）: 1 415-1 427. [15] Lafleuriel J, Degroote F, Depeiges A, et al. Impact of the loss of AtMSH2 on double-strand break-induced recombination between highly diverged homeologous sequences in Arabidopsis thaliana germinal tissues [J]. Plant Mol Biol, 2007, 63（6）: 833-846. [16] Dzantiev L, Constantin N, Genschel J, et al. A defined human system that supports bidirectional mismatch-provoked excision[J]. Mol Cell, 2004, 15（1）: 31-41. [17] Prolla T A, Christie D M, Liskay R M. Dual requirement in yeast DNA mismatch repair for MLH1 and PMS1, two homologs of the bacterial mutL gene[J]. Mol Cell Bio, 1994, 14（1）: 407-415. [18] Hall M C, Shcherbakova P V, Fortune J M, et al. DNA binding by yeast Mlh1 and Pms1: implications for DNA mismatch repair[J]. Nucleic Acids Res, 2003, 31（8）: 2 025-2 034. [19] Culligan K M, Hays J B. DNA mismatch repair in plants （an Arabidopsis thaliana gene that predicts a protein belonging to the MSH2 subfamily of eukaryotic MutS homologs）[J]. Plant Physiol, 1997, 115（2）: 833-839. [20] Ade J, Belzile F, Philippe H, et al. Four mismatch repair paralogues coexist in Arabidopsis thaliana: AtMSH2, AtMSH3, AtMSH6-1 and AtMSH6-2[J]. Mol Gen Genet, 1999, 262（2）: 239-249. [21] Doerks T, Copley R R, Schultz J, et al. Systematic identification of novel protein domain families associated with nuclear functions[J]. Genome Res, 2002, 12（1）: 47-56. [22] Lu X, Liu X, An L, et al. The Arabidopsis MutS homolog AtMSH5 is required for normal meiosis[J]. Cell Res, 2008, 18（5）: 589-599. [23] Higgins JD, Vignard J, Mercier R, et al. AtMSH5 partners AtMSH4 in the class I meiotic crossover pathway in Arabidopsis thaliana, but is not required for synapsis[J]. Plant J, 2008, 55（1）: 28-39. [24] Dong C, Whitford R, Langridge P. A DNA mismatch repair gene links to the Ph2 locus in wheat[J]. Genome, 2002, 45（1）: 116-124. [25] Virdi K S, Wamboldt Y, Kundariya H, et al. MSH1 is a plant organellar DNA Binding and Thylakoid Protein under precise spatial regulation to alter development[J]. Mol Plant, 2016, 9（2）: 245-260. [26] Lloyd A H, Milligan A S, Langridge P, et al. TaMSH7: a cereal mismatch repair gene that affects fertility in transgenic barley （Hordeum vulgare L.）[J]. BMC Plant Biol, 2007, 7: 67. [27] Xu Y Z, Arrieta-Montiel M P, Virdi K S, et al. MutS HOMOLOG1 is a nucleoid protein that alters mitochondrial and plastid properties and plant response to high light[J]. Plant Cell, 2011, 23（9）: 3 428-3 441. [28] Abdelnoor R V, Yule R, Elo A, et al. Substoichiometric shifting in the plant mitochondrial genome is influenced by a gene homologous to MutS[J]. Proc Natl Acad Sci USA, 2003, 100（10）: 5 968-5 973. [29] Abdelnoor R V, Christensen A C, Mohammed S, et al. Mitochondrial genome dynamics in plants and animals: convergent gene fusions of a MutS homologue [J]. J Mol Evol, 2006, 63（2）: 165-173. [30] Davila J I, Arrieta-Montiel M P, Wamboldt Y, et al. Double-strand break repair processes drive evolution of the mitochondrial genome in Arabidopsis[J]. BMC Biol, 2011, 9（1）: 64. [31] Xu Y Z, Santamaria Rde L, Virdi K S, et al. The chloroplast triggers developmental reprogramming when mutS HOMOLOG1 is suppressed in plants[J]. Plant Physiol, 2012, 159（2）: 710-720. [32] Shedge V, Davila J, Arrieta-Montiel M P, et al. Extensive rearrangement of the Arabidopsis mitochondrial genome elicits cellular conditions for thermotolerance[J]. Plant Physiol, 2010, 152（4）: 1960-1970. [33] Xu Y Z, Arrieta-Montiel M P, Virdi K S, et al. MutS HOMOLOG1 is a nucleoid protein that alters mitochondrial and plastid properties and plant response to high light[J]. Plant Cell, 2011, 23（9）: 3 428 -3 441. [34] Sandhu A P, Abdelnoor R V, Mackenzie S A. Transgenic induction of mitochondrial rearrangements for cytoplasmic male sterility in crop plants[J]. Proc Natl Acad Sci U S A, 2007, 104（6）: 1 766-1 770. [35] Virdi K S, Laurie J D, Xu Y Z, et al. Arabidopsis MSH1 mutation alters the epigenome and produces heritable changes in plant growth[J]. Nat Commun, 2015, 6: 6386. [36] Zhao N, Xu X, Wamboldt Y,et al. MutS HOMOLOG1 silencing mediates ORF220 substoichiometric shifting and causes male sterility in Brassica juncea [J]. J Exp Bot, 2016, 67（1）: 435-444. [37] Yang X, Kundariya H, Xu Y Z, et al. MutS HOMOLOG1-derived epigenetic breeding potential in tomato[J]. Plant Physiol, 2015, 168（1）: 222-232. [38] Culligan K M, Hays J B. Arabidopsis MutS homologs-AtMSH2, AtMSH3, AtMSH6, and a novel AtMSH7-form three distinct protein heterodimers with different specificities for mismatched DNA[J]. Plant Cell, 2000, 12（6）: 991-1002. [39] Gomez R L, Galles C, Spampinato C P. High-level production of MSH2 from Arabidopsis thaliana: a DNA mismatch repair system key subunit[J]. Mol Biotechnol, 2011, 47: 120-129. [40] Modrich P, Lahue R. Mismatch repair in replication fidelity, genetic recombination, and cancer biology[J]. Annu Rev Biochem, 1996, 65（1）: 101-133. [41] Lee S D, Surtees J A, Alani E. Saccharomyces cerevisiae MSH2-MSH3 and MSH2-MSH6 complexes display distinct requirements for DNA binding domain I in mismatch recognition[J]. J Mol Biol, 2007, 366（1）: 53-66. [42] Culligan K M, Meyer-Gauen G, Lyons-Weiler J, et al. Evolutionary origin, diversification and specialization of eukaryotic MutS homolog mismatch repair proteins[J]. Nucleic Acids Res, 2000, 28（2）: 463-471. [43] Malkov V A, Biswas I, Camerini-Otero R D, et al. Photocross-linking of the NH2-terminal region of Taq MutS protein to the major groove of a heteroduplex DNA[J]. J Biol Chem, 1997, 272（38）: 23811-23 817. [44] Otterlei M, Warbrick E, Nagelhus T A, et al. Post-replicative base excision repair in replication foci[J]. EMBO J, 1999, 18（13）: 3 834-3 844. [45] Johnson R E, Kovvali G K, Guzder S N, et al. Evidence for involvement of yeast proliferating cell nuclear antigen in DNA mismatch repair[J]. J Biological Chem, 1996, 271（45）: 27 987-27 990. [46] Umar A, Buermeyer A B, Simon J A, et al. Requirement for PCNA in DNA mismatch repair at a step preceding DNA resynthesis[J]. Cell, 1996, 87（1）: 65-73.. [47] Chen C, Merrill B J, Lau P J, et al. Saccharomyces cerevisiae pol30（proliferating cell nuclear antigen）mutations impair replication fidelity and mismatch repair[J]. Mol Cell Biol, 1999, 19（11）: 7 801 -7 815. [48] Chen W, Jinks-Robertson S. The role of the mismatch repair machinery in regulating mitotic and meiotic recombination between diverged sequences in yeast[J]. Genetics, 1999, 151（4）: 1 299-1 313. [49] Opperman R, Emmanuel E, Levy A A. The effect of sequence divergence on recombination between direct repeats in Arabidopsis[J]. Genetics, 2004, 168（4）: 2 207-2 215. [50] Li L, Santerre-Ayotte S, Boivin E B, et al. A novel reporter for intrachromosomal homoeologous recombination in Arabidopsis thaliana[J]. Plant J, 2004, 40（6）: 1 007-1 015. [51] Li L, Jean M, Belzile F. The impact of sequence divergence and DNA mismatch repair on homeologous recombination in Arabidopsis[J]. Plant J, 2006, 45（6）: 908-916. [52] Rayssiguier C, Thaler D S, Radman M. The barrier to recombination between Escherichia coli and Salmonella typhimurium is disrupted in mismatch-repair mutants[J]. Nature, 1989, 342（6248）: 396-401. [53] Datta A, Adjiri A, New L, et al. Mitotic crossovers between diverged sequences are regulated by mismatch repair proteins in Saccaromyces cerevisiae[J]. Mol Cell Biol, 1996, 16（3）: 1 085-1 093. [54] Nicholson A, Hendrix M, Jinks-Robertson S, et al. Regulation of mitotic homeologous recombination in yeast: functions of mismatch repair and nucleotide excision repair genes[J]. Genetics, 2000, 154（1）: 133-146. [55] Elliott B, Jasin M. Repair of double-strand breaks by homologous recombination in mismatch repair-defective mammalian cells[J]. Mol Cell Biol, 2001, 21（8）: 2 671-2 682. [56] Emmanuel E, Yehuda E, Melamed-Bessudo C, et al. The role of AtMSH2 in homologous recombination in Arabidopsis thaliana[J]. EMBO Rep, 2006, 7（1）: 100-105. [57] Leonard J M. Reduction of stability of Arabidopsis genomic and transgenic DNA-repeat sequences （Microsatellites） by inactivation of AtMSH2 Mismatch-Repair function[J]. Plant Physiol, 2003, 133（1）: 328-338. [58] Meira L B, Cheo D L, Reis A M, et al. Mice defective in the mismatch repair gene Msh2 show increased predisposition to UVB radiation-induced skin cancer[J]. DNA Repair（Amst）, 2002, 1（11）: 929-934. [59] Young L C, Thulien K J, Campbell M R, et al. DNA mismatch repair proteins promote apoptosis and suppress tumorigenesis in response to UVB irradiation: an in vivo study [J]. Carcinogenesis, 2004, 25（10）: 1 821-1 827. [60] Peters A. Mammalian DNA mismatch repair protects cells from UVB-induced DNA damage by facilitating apoptosis and p53 activation[J]. DNA Repair（Amst）, 2003, 2（4）: 427-435. [61] Narine K A D, Felton K E A, Parker A A M, et al. Non-tumor cells from an MSH2-null individual show altered cell cycle effects post-UVB[J]. Oncol Rep, 2007, 18（6）: 1 403-1 412. [62] Casati P, Stapleton A E, Blum J E, et al. Genome-wide analysis of high-altitude maize and gene knockdown stocks implicates chromatin remodeling proteins in response to UVB[J]. Plant J, 2006, 46（4）: 613-627. [63] 袁兵，崔海瑞，富昊伟，等. 水稻 Os09g24220 基因插入突变体的分子鉴定与农艺性状分析[J]. 浙江大学学报: 农业与生命科学版，2014，40（4）：456-462. [64] Hollingsworth N M, Ponte L, Halsey C. MSH5, a novel MutS homolog, facilitates meiotic reciprocal recombination between homologs in Saccharomyces cerevisiae but not mismatch repair[J]. Genes Dev, 1995, 9（14）: 1 728-1 739. [65] Kolas N K, Cohen P E. Novel and diverse functions of the DNA mismatch repair family in mammalian meiosis and recombination[J]. Cytogenet Genome Res, 2004, 107（3-4）: 216-231. [66] Tam S M, Samipak S, Britt A, et al. Characterization and comparative sequence analysis of the DNA mismatch repair MSH2 and MSH7 genes from tomato[J]. Genetica, 2009, 137（3）: 341-354. [67] Snowden T, Acharya S, Butz C, et al. hMSH4-hMSH5 recognizes Holliday Junctions and forms a meiosis-specific sliding clamp that embraces homologous chromosomes[J]. Mol Cell, 2004, 15（3）: 437-451. [68] Higgins J D, Armstrong S J, Franklin F C H, et al. The Arabidopsis MutS homolog AtMSH4 functions at an early step in recombination: evidence for two classes of recombination in Arabidopsis[J]. Genes Dev, 2004, 18（20）: 2 557-2 570. [69] Biswas I, Obmolova G, Takahashi M, et al. Disruption of the helix-u-turn-helix motif of MutS protein: loss of subunit dimerization, mismatch binding and ATP hydrolysis[J]. J Mol Biol, 2001, 305（4）: 805-816. [70] Luo Q, Tang D, Wang M, et al. The role of OsMSH5 in crossover formation during rice meiosis [J]. Mol Plant, 2013, 6（3）: 729-742. [71] Culligan K M, Hays J B. DNA mismatch repair in plants. An Arabidopsis thaliana gene that predicts a protein belonging to the MSH2 subfamily of eukaryotic MutS homologs [J]. PlantPhysiol, 1997, 115（2）: 833-839. [72] Jean M, Pelletier J, Hilpert M, et al. Isolationand characterization of AtMLH1, a MutL homologue from Arabidopsis thaliana [J]. Mol Gen Genet, 262（4-5）: 633-642. [73] Leonard J M, Bollmann S R, Hays J B. Reduction of stability of Arabidopsis genomic and transgenic DNA-repeat sequences（microsatellites） by inactivation of AtMSH2 mismatch-repair function [J]. Plant Physiol, 2003, 133（1）: 328-338. [74] Hoffman P D, Leonard J M, Lindberg G E, et al. Rapid accumulation of mutations during seed-to-seed propagation Arabidopsis of mismatch-repair-defective [J]. Genes Dev, 2004, 18（21）: 2676-2685. [75] Xu J, Li M R, Chen L, et al. Rapid generation of rice mutants via the dominant negative suppression of the mismatch repair protein OsPMS1[J]. Theor Appl Genet, 2012, 125（5）: 975-986.