Restriction-modification gene complexes as selfish gene entities: Roles of a regulatory system in their establishment, maintenance, and apoptotic mutual exclusion

被引:80
作者
Nakayama, Y [1 ]
Kobayashi, I [1 ]
机构
[1] Univ Tokyo, Inst Med Sci, Dept Biol Mol, Tokyo 1088639, Japan
关键词
programmed cell death; epigenetics; intragenomic conflicts; phage exclusion; plasmid;
D O I
10.1073/pnas.95.11.6442
中图分类号
O [数理科学和化学]; P [天文学、地球科学]; Q [生物科学]; N [自然科学总论];
学科分类号
07 ; 0710 ; 09 ;
摘要
We have reported some type II restriction-modification (RM) gene complexes on plasmids resist displacement by an incompatible plasmid through postsegregational host killing, Such selfish behavior may have contributed to the spread and maintenance of Rh?I systems. Here we analyze the role of regulatory genes (C), often found linked to RM gene complexes, in their interaction with the host and the other RM gene complexes. We identified the C gene of EcoRV as a positive regulator of restriction. A C mutation eliminated postsegregational killing by EcoRV, The C system has been proposed to allow establishment of RM systems in new hosts by delaying the appearance of restriction activity. Consistent with this proposal, bacteria pre expressing ecoRVC were transformed at a reduced efficiency by plasmids carrying the EcoRV RM gene complex Cells carrying the BamHI RM gene complex were transformed at a reduced efficiency by a plasmid carrying a PvuII RR;I gene complex, which shares the same C specificity. The reduction most likely was caused by chromosome cleavage at unmodified PvuII sites by prematurely expressed PvuII restriction enzyme. Therefore, association of the C genes of the same specificity with RM gene complexes of different sequence specificities can confer on a resident RM gene complex the capacity to abort establishment of a second, incoming RM gene complex This phenomenon, termed "apoptotic mutual exclusion," is reminiscent of suicidal defense against virus infection programmed by other selfish elements. pvuII and bamHIC genes define one incompatibility group of exclusion whereas ecoRVC gene defines another.
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页码:6442 / 6447
页数:6
相关论文
共 42 条
[1]   COMPLEX TRANSCRIPTION OF AN OPERON ENCODING THE SALI RESTRICTION MODIFICATION SYSTEM OF STREPTOMYCES-ALBUS-G [J].
ALVAREZ, MA ;
CHATER, KF ;
RODICIO, MR .
MOLECULAR MICROBIOLOGY, 1993, 8 (02) :243-252
[2]   EXPRESSION OF THE SALI RESTRICTION-MODIFICATION SYSTEM OF STREPTOMYCES-ALBUS-G IN ESCHERICHIA-COLI [J].
ALVAREZ, MA ;
GOMEZ, A ;
GOMEZ, P ;
RODICIO, MR .
GENE, 1995, 157 (1-2) :231-232
[3]   Cloning and characterization of the BglII restriction-modification system reveals a possible evolutionary footprint [J].
Anton, BP ;
Heiter, DF ;
Benner, JS ;
Hess, EJ ;
Greenough, L ;
Moran, LS ;
Slatko, BE ;
Brooks, JE .
GENE, 1997, 187 (01) :19-27
[4]   MATERNAL-EFFECT SELFISH GENES IN FLOUR BEETLES [J].
BEEMAN, RW ;
FRIESEN, KS ;
DENELL, RE .
SCIENCE, 1992, 256 (5053) :89-92
[5]   CLONING OF A RESTRICTION-MODIFICATION SYSTEM FROM PROTEUS-VULGARIS AND ITS USE IN ANALYZING A METHYLASE-SENSITIVE PHENOTYPE IN ESCHERICHIA-COLI [J].
BLUMENTHAL, RM ;
GREGORY, SA ;
COOPERIDER, JS .
JOURNAL OF BACTERIOLOGY, 1985, 164 (02) :501-509
[6]   CHARACTERIZATION OF THE GENES-CODING FOR THE ECO RV RESTRICTION AND MODIFICATION SYSTEM OF ESCHERICHIA-COLI [J].
BOUGUELERET, L ;
SCHWARZSTEIN, M ;
TSUGITA, A ;
ZABEAU, M .
NUCLEIC ACIDS RESEARCH, 1984, 12 (08) :3659-3676
[7]   A TRANSPOSON-LIKE SEQUENCE ADJACENT TO THE ACCI RESTRICTION-MODIFICATION OPERON [J].
BRASSARD, S ;
PAQUET, H ;
ROY, PH .
GENE, 1995, 157 (1-2) :69-72
[8]   COMPARATIVE MOLECULAR-BIOLOGY OF LAMBDOID PHAGES [J].
CAMPBELL, A .
ANNUAL REVIEW OF MICROBIOLOGY, 1994, 48 :193-222
[9]   INDUCTION OF ECORII METHYLTRANSFERASE - EVIDENCE FOR AUTOGENOUS CONTROL [J].
FRIEDMAN, S ;
SOM, S .
JOURNAL OF BACTERIOLOGY, 1993, 175 (19) :6293-6298
[10]  
Hanahan D., 1985, DNA CLONING, VI, P109