Conjugation factor of Agrobacterium tumefaciens regulates Ti plasmid transfer by autoinduction

Piper, Kevin R.; Bodman, Susanne B. von; Farrand, Stephen K.

doi:10.1038/362448a0

Cited by 475 publications

(380 citation statements)

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“…1) (1). As a consequence, strains harboring this Ti plasmid express traR constitutively, produce large amounts of AAI, and transfer the plasmid at high frequency in the absence of the conjugal opine (1,23,34).…”

Section: Resultsmentioning

confidence: 99%

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Quorum Sensing but Not Autoinduction of Ti Plasmid Conjugal Transfer Requires Control by the Opine Regulon and the Antiactivator TraM

Piper¹,

Farrand

2000

J Bacteriol

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Conjugal transfer of the Ti plasmids from Agrobacterium tumefaciens is controlled by autoinduction via the transcriptional activator TraR and the acyl-homoserine lactone ligand, Agrobacterium autoinducer (AAI). This control process is itself regulated by opines, which are small carbon compounds produced by the crown gall tumors that are induced by the bacteria. Opines control autoinduction by regulating the expression of traR. Transfer of pTiC58 from donors grown with agrocinopines A and B, the conjugal opines for this Ti plasmid, was detected only after the donors had reached a population level of 10 7 cells per cm 2 . Donors incubated with the opines and AAI transferred their Ti plasmids at population levels about 10-fold lower than those incubated with opines only. Transcription of the tra regulon, as assessed by monitoring a traA::lacZ reporter, showed a similar dependence on the density of the donor population. However, even in cultures at low population densities that were induced with opines and AAI, there was a temporal lag of between 15 and 20 h in the development of conjugal competence. Moreover, even after this latent period, maximal transfer frequencies required several hours to develop. This lag period was independent of the population density of the donors but could be reduced somewhat by addition of exogenous AAI. Quorum-dependent development of conjugal competence required control by the opine regulon; donors harboring a mutant of pTiC58 deleted for the master opine responsive repressor accR transferred the Ti plasmid at maximum frequencies at very low population densities. Similarly, an otherwise wild-type derivative of pTiC58 lacking traM, which codes for an antiactivator that inhibits TraR activity, transferred at high frequency in a population-independent manner in the absence of the conjugal opines. Thus, while quorum sensing is dependent upon autoinduction, the two phenomena are not synonymous. We conclude that conjugal transfer of pTiC58 is regulated in a quorum-dependent fashion but that supercontrol of the TraR-AAI system by opines and by TraM results in a complex control process that requires not only the accumulation of AAI but also the expression of TraR and the synthesis of this protein at levels that overcome the inhibitory activity of TraM.Conjugal transfer of the Ti plasmids from Agrobacterium tumefaciens is regulated directly by the transcriptional activator TraR and its acyl-homoserine lactone (acyl-HSL) ligand, Agrobacterium autoinducer [AAI; N-(3-oxo-octanoyl)-L-homoserine lactone] (16, 34, 40; reviewed in reference 12). TraR, in its interaction with AAI, controls conjugation by autoinduction, a process by which the bacteria induce gene sets in response to signals they themselves produce. This regulatory strategy is believed to tie plasmid transfer to the population density of the donor in what has come to be called the quorumsensing effect (reviewed in reference 18). The acyl-HSL autoinducers, which are produced by the bacteria themselves, are released into the environment, w...

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Section: Resultsmentioning

confidence: 99%

“…serine lactone] (16,34,40; reviewed in reference 12). TraR, in its interaction with AAI, controls conjugation by autoinduction, a process by which the bacteria induce gene sets in response to signals they themselves produce.…”

Section: Conjugal Transfer Of the Ti Plasmids From Agrobacterium Tumementioning

confidence: 99%

Quorum Sensing but Not Autoinduction of Ti Plasmid Conjugal Transfer Requires Control by the Opine Regulon and the Antiactivator TraM

Piper¹,

Farrand

2000

J Bacteriol

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“…The intricate autoregulatory mechanism employed by luminous marine bacteria in the cell density-dependent regulation of bioluminescence is also employed by other Gram-negative bacteria to control a wide variety of different biochemical functions, including pathogenicity (1)(2)(3)(4)(5). The paradigm of this phenomenon, the luminous marine bacteria (6,7), has been studied for over three decades.…”

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Control of cell division in Escherichia coli: regulation of transcription of ftsQA involves both rpoS and SdiA-mediated autoinduction.

Sitnikov

Schineller

Baldwin

1996

Proc. Natl. Acad. Sci. U.S.A.

151

155

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The conditioning of culture medium by the production of growth-regulatory substances is a wellestablished phenomenon with eukaryotic cells. It has recently been shown that many prokaryotes are also capable of modulating growth, and in some cases sensing cell density, by production of extracellular signaling molecules, thereby allowing single celled prokaryotes to function in some respects as multicellular organisms. As Escherichia coli shifts from exponential growth to stationary growth, many changes occur, including cell division leading to formation of short minicells and expression of numerous genes not expressed in exponential phase. An understanding of the coordination between the morphological changes associated with cell division and the physiological and metabolic changes is of fundamental importance to understanding regulation of the prokaryotic cell cycle. The ftsQA genes, which encode functions required for cell division in E. coli, are regulated by promoters Pi and P2, located upstream of the ftsQ gene. The P1 promoter is rpoSstimulated and the second, P2, is regulated by a member of the LuxR subfamily of transcriptional activators, SdiA, exhibiting features characteristic of an autoinduction (quorum sensing) mechanism. The activity of SdiA is potentiated by N-acylhomoserine lactones, which are the autoinducers of luciferase synthesis in luminous marine bacteria as well as of pathogenesis functions in several pathogenic bacteria. A compound(s) produced by E. coli itself during growth in Luria Broth stimulates transcription from P2 in an SdiA-dependent process. Another substance(s) enhances transcription of rpoS and (perhaps indirectly) offtsQA via promoter P1. It appears that this bimodal control mechanism may comprise a fail-safe system, such that transcription of the ftsQA genes may be properly regulated under a variety of different environmental and physiological conditions.

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“…TraR, a member of the LuxR family of quorum-sensing transcription factors, activates expression of the transfer operons in response to the second signal, an acyl-homoserine lactone (acyl-HSL) (27,34). The cognate quormone N-(3-oxooctanoyl)-L-homoserine lactone (3-oxo-C8-HSL) is produced by the bacteria themselves via the acyl-HSL synthase TraI, also encoded by the Ti plasmid (16,24).…”

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Induction and Loss of Ti Plasmid Conjugative Competence in Response to the Acyl-Homoserine Lactone Quorum-Sensing Signal

Khan

Farrand

2008

J Bacteriol

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Conjugative transfer of the Ti plasmids ofConjugative transfer of the Ti plasmids of Agrobacterium tumefaciens is a tightly regulated process involving two signaling systems arranged in a hierarchy. Expression of the three Ti plasmid transfer operons, traAFB, traCDG, and traI-trb, requires first a small molecule signal, the conjugative opine, which is produced by the crown gall tumors induced on susceptible plants by this phytopathogen (7,8). In addition to acting as a signal, the conjugative opine also can be catabolized by the bacteria by using functions coded for by the Ti plasmid. The conjugative opines regulate transfer by controlling the expression of a Ti plasmid operon of which TraR, the direct regulator of the three transfer operons, is a member. For example, transfer of pTiC58 is induced by the sugar phosphodiester opines agrocinopine A and agrocinopine B. In this plasmid, traR is a member of the five-gene arc operon, the expression of which is regulated by the opine-responsive repressor AccR (1). In the absence of the conjugative opines, the expression of arc is repressed. When the opines are present, as when the bacteria are colonizing an agrocinopine-producing crown gall tumor, repression by AccR is relieved, and the arc operon, including traR, is expressed.TraR, a member of the LuxR family of quorum-sensing transcription factors, activates expression of the transfer operons in response to the second signal, an acyl-homoserine lactone (acyl-HSL) (27, 34). The cognate quormone N-(3-oxooctanoyl)-L-homoserine lactone (3-oxo-C8-HSL) is produced by the bacteria themselves via the acyl-HSL synthase TraI, also encoded by the Ti plasmid (16,24). This signal transits out of and back into the cells in a stochastic fashion, and its concentration in a diffusion-limited environment increases with in-

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Conjugation factor of Agrobacterium tumefaciens regulates Ti plasmid transfer by autoinduction

Cited by 475 publications

References 20 publications

Quorum Sensing but Not Autoinduction of Ti Plasmid Conjugal Transfer Requires Control by the Opine Regulon and the Antiactivator TraM

Quorum Sensing but Not Autoinduction of Ti Plasmid Conjugal Transfer Requires Control by the Opine Regulon and the Antiactivator TraM

Control of cell division in Escherichia coli: regulation of transcription of ftsQA involves both rpoS and SdiA-mediated autoinduction.

Induction and Loss of Ti Plasmid Conjugative Competence in Response to the Acyl-Homoserine Lactone Quorum-Sensing Signal

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