Table II.7. Various stimuli documented to activate natural genetic engineering.

Signal or condition

Natural genetic engineering function

Organism(s)

Reference

Quorum pheromones

DNA release and competence for DNA uptake

Multiple bacteria

(Miller and Bassler 2001; Sturme, Kleerebezem et al. 2002; Spoering and Gilmore 2006)

Chitin

Competence for DNA uptake

Vibrio cholerae

(Meibom, Blokesch et al. 2005)

Various stress conditions

Competence for DNA uptake

Gram-positive bacteria

(Claverys, Prudhomme et al. 2006)

DNA damage

Recombination and mutator polymerases (SOS response)

Escherichia coli, Bacillus subtilis and other bacteria

(Sutton, Smith et al. 2000; Au, Kuester-Schoeck et al. 2005)

DNA damage

Prophage excision

E. coli, B. subtilis and other bacteria

(Goranov, Kuester-Schoeck et al. 2006; Rokney, Kobiler et al. 2008).

DNA damage

Horizontal transfer of integrated conjugative (ICE) elements

Multiple bacteria

(Beaber, Hochhut et al. 2004; Auchtung, Lee et al. 2005).

DNA damage

ISDra2 transposition

Deinococcus radiodurans

(Pasternak, Ton-Hoang et al. 2010)

DNA damage

Genetic exchange

Helicobacter pylori

(Dorer, Fero et al. 2010)

UV irradiation

Tn10 transposition

E. coli

(Eichenbaum and Livneh 1998)

Oxidative stress

SOS responses, prophage induction

Multiple bacteria

(Giuliodori, Gualerzi et al. 2007; Selva, Viana et al. 2009)

Chemical damage

SOS response

E. coli, Salmonella typhimurium

(Mersch-Sundermann, Mochayedi et al. 1993; Mersch-Sundermann, Rosenkranz et al. 1994; Mersch-Sundermann, Schneider et al. 1994)

Antibiotic

SOS response

E. coli

(Phillips, Culebras et al. 1987; Miller, Thomsen et al. 2004)

Antibiotic

Competence for DNA uptake

Staphylococcus aureus

(Prudhomme, Attaiech et al. 2006)

Antibiotic

Prophage excision

Staphylococcus aureus

(Goerke, Köller et al. 2006)

Antibiotic (beta lactam)

SOS response and horizontal DNA transfer

Staphylococcus aureus

(Maiques, Ubeda et al. 2006)

Antibiotic

Mutator polymerase

E. coli

(Pérez-Capilla, Baquero et al. 2005)

Tetracycline

CTnDOT excision and conjugal transfer

Bacteroides sp.

(Moon, Shoemaker et al. 2005)

Quorum pheromones, plant metabolites (opines)

Conjugal transfer

Agrobacterium tumefaciens

(Fuqua and Winans 1994)

Plant phenolics

T-DNA transfer to plant cell

A. tumefaciens

 (Gelvin 2006)

Magnetic fields

Tn5 transposition

E. coli

(Chow and Tung 2000)

Magnetic fields

Tn10 transposition

E. coli

(Del Re, Garoia et al. 2003; Del Re, Bersani et al. 2004)

Heat shock

F plasmid transfer

E. coli

(Zahrl, Wagner et al. 2007)

Growth phase

F plasmid transfer

E. coli

(Will, Lu et al. 2004)

Genome reduction

Stress-induced IS elements

E. coli

(Posfai, Plunkett et al. 2006)

Conjugation

ISPst9 transposition

P. stutzeri

(Christie-Oleza, Lanfranconi et al. 2009)

Sex pheromones

Conjugation agglutinins

Enterobacter fecaelis

(Kozlowicz, Dworkin et al. 2006; Kozlowicz, Shi et al. 2006; Clewell 2007; Dunny 2007)

Nucleic acid precursors

Reduce competence

Haemophilus influenzae

(MacFadyen, Chen et al. 2001)

Aerobic starvation

Mu prophage activation

E. coli

(Maenhaut-Michel and Shapiro 1994) (Lamrani, Ranquet et al. 1999)

Stringent response (starvation-induced ppGpp synthesis)

Activation of IS element transcription and IS3 transposition

Caulobacter crescentus

(Boutte and Crosson 2011)

Aerobic starvation

Tn4652 activation

Pseudomonas putida

(Horak, Ilves et al. 2004; Ilves, Horak et al. 2004)

Aerobic starvation

Base substitutions

E. coli

(Bjedov, Tenaillon et al. 2003)

Aerobic starvation

Tandem duplications and amplifications

Salmonella enterica

(Kugelberg, Kofoid et al. 2006)

Aerobic starvation

Plasmid transfer and replication

E. coli

(Peters and Benson 1995; Peters, Bartoszyk et al. 1996)

Elevated temperature

IS element activation

Burkholderia sp.

(Taghavi, Mergeay et al. 1997; Ohtsubo, Genka et al. 2005)

Elevated temperature and high culture density

IS4Bsu1 element

B. subtilis

(Takahashi, Sekine et al. 2007)

Adenine starvation

Ty1 retrotransposon activation

Saccharomyces cerevisiaea

(Todeschini, Morillon et al. 2005) (Servant, Pennetier et al. 2008)

DNA damage (radiation or carcinogen)

Ty1 retrotransposon activation

S. cerevisiaea

 (Bradshaw and McEntee 1989; Sacerdot, Mercier et al. 2005; Stoycheva, Massardo et al. 2007)

Telomere erosion

Ty1 retrotransposon activation

S. cerevisiaea

(Scholes, Kenny et al. 2003)

MAPK cascade activation during filamentous growth

Ty1 retrotransposon activation

S. cerevisiaea

(Conte and Curcio 2000; Morillon, Springer et al. 2000)

Oxidative conditions (H₂O₂) mediated by SREBP trancription factor

Tf2 retrotransposon activation

Schizosaccharomyces pombe

(Sehgal, Lee et al. 2007)

Mating pheromone

Ty3 retrotransposon activation

S. cerevisiaea

(Kinsey and Sandmeyer 1995)

Mating pheromone

Ty5 retrotransposon activity and transcription

S. cerevisiaea

 (Ke, Irwin et al. 1997)

Prion formation

Genome instability

S. cerevisaea

 (True and Lindquist 2000)

Improper cryopreservation

Ty1 retrotransposition

S. cerevisaea

 (Stamenova, Dimitrov et al. 2008)

Nitrogen starvation

LTR retrotransposon transcription

Diatom (P. tricornutum)

 (Maumus, Allen et al. 2009)

Aldehyde (decadienal) treatment

LTR retrotransposon transcription

Diatom (P. tricornutum)

 (Maumus, Allen et al. 2009)

DNA damage (Mitomycin C)

Transposon and retrotransposon activation

Drosophila melanogaster

(Georgiev, Korochkina et al. 1990)

DNA damage

Alu retransposition

Homo sapiens

 (Hagan, Sheffield et al. 2003)

Gamma irradiation

LINE-1 retrtransposition

Homo sapiens (human osteosarcoma cells)

(Farkash, Kao et al. 2006)

Benzpyrene

LINE-1 retrotransposition

Homo sapiens  (HeLa cells)

(Stribinskis and Ramos 2006)

Steroid hormones

Mouse mammary tumor virus (MMTV) activation

Mus musculus

(Truss, Chalepakis et al. 1992)

Plant alarm chemicals

Retrotransposon activation

Nicotiana tabacum

(Beguiristain, Grandbastien et al. 2001)

Free radical-generating agents, UVC or rose Bengal (RB)

Increased homologous recombination, systemically transmitted

Tobacco

 (Filkowski, Yeoman et al. 2004)

Hydrostatic pressure

MITE DNA transposons

rice

(Lin, Long et al. 2006)

Cutting/wounding

Retrotransposon activation

N. tabacum

(Sugimoto, Takeda et al. 2000)

Protoplasting & growth in tissue culture

Transposon and retrotransposon activation

various plants

(Hirochika 1993; Huang, Zhang et al. 2009)

Protoplasting & growth in tissue culture

Tos17 retrotransposon activation

rice

 (Hirochika, Sugimoto et al. 1996)

Growth in tissue culture

mPing transposition

rice

 (Ngezahayo, Xu et al. 2009)

Cell culture growth

1731 LTR retrotransposon

D. melanogaster

(Maisonhaute, Ogereau et al. 2007)

Cell culture growth

LINE-1 element retrotransposition

Mouse cell line

(Moran, Holmes et al. 1996)

Fungal metabolites

TnT1 retrotransposon

Nicotiana tabacum

(Melayah, Bonnivard et al. 2001)

Chlorine ions (not sodium)

DNA strand breaks and recombination

Arabidopsis thaliana

(Boyko, Hudson et al. 2006; Boyko, Golubov et al. 2010)

Nickel, Cadmium and other heavy metals

LINE-1 retrotransposition

Homo sapiens tissue culture cells

(El-Sawy, Kale et al. 2005; Kale, Moore et al. 2005; Kale, Carmichael et al. 2006)

Temperature and day length

Homologou recombination

Arabidopsis thaliana

(Boyko, Filkowski et al. 2005)

Helicobacter pylori infection

Adenocarcinoma with microsatellite instability

human gastric mucosa

 (Tahara 2004) (Li, Shi et al. 2005) (Moriichi, Watari et al. 2009)

Fungal or virus infection

(CT)n microsatellite contraction

wheat

(Schmidt and Mitter 2004) (Kovalchuk, Tryndyak et al. 2007)

Barley stripe mosaic virus (Peronospora parasitica) infection

Increased somatic recombination and transposon activation; transmissible systemic response in tobacco

Arabidopsis, maize and tobacco

 (Kovalchuk, Kovalchuk et al. 2003)

Tobacco mosaic virus and oilseed rape mosaic virus infection

Increased somatic recombination (transmissible systemic response)

Tobacco, Arabidopsis thaliana

 (Dong 2004; Boyko, Kathiria et al. 2007)

Temperature

Amplification/reduction in repetitive elements

Festuca arundinacea (Tall Fescue)

(Ceccarelli, Esposto et al. 2002)

Elevation and moisture

BARE-1 retrotransposition

Hordeum spontaneum (wild barley)

(Kalendar, Tanskanen et al. 2000)

Heat shock, toxic chemicals

SINE transcription

Bombyx morii

(Kimura, Choudary et al. 1999; Kimura, Choudary et al. 2001)

Various stress conditions

SINE transcription

H. sapiens

(Li and Schmid 2001)

Heat shock

B1 SINE transcription

M. musculus

(Li, Spearow et al. 1999)

Industrial air pollution

Microsatellite expansion

M. musculus

(Somers, Yauk et al. 2002)

Particulate air pollution

Germ-line mutations

Mouse

(Yauk, Polyzos et al. 2008)

Chemical mutagens and etoposide

Microsatellite expansion

M. musculus

(Vilarino-Guell, Smith et al. 2003)

Diet (extra folic acid, vitamin B12 choline, and betaine)

IAP retrotransposon at Agouti locus (Avy allele)

M. musculus

(Waterland and Jirtle 2003)

Lymphocyte differentiation and antigen activation

Activation of VDJ joining, somatic hypermutation and heavy chain class switching

M. musculus and H. sapiens

(Gellert 1997; Honjo, Kinoshita et al. 2002; Alt 2007)

Neuronal differentiation and exercise

LINE-1 retrotransposition

M. musculus

(Muotri, Chu et al. 2005; Muotri, Zhao et al. 2009); (Coufal, Garcia-Perez et al. 2009)

Hybrid dysgenesis

P factor transposon

D. melanogaster

 (Kidwell 1985; Kidwell, Kimura et al. 1988) (Kocur, Drier et al. 1986)

Hybrid dysgenesis

I factor non-LTR retrotransposon

D. melanogaster

(Fawcett, Lister et al. 1986; Bucheton 1990; Busseau, Chaboissier et al. 1994; Sezutsu, Nitasaka et al. 1995; de La Roche Saint Andre and Bregliano 1998; Gauthier, Tatout et al. 2000)

Hybrid dysgenesis

Hobo transposon

D. melanogaster

(Yannopoulos, Stamatis et al. 1987) (Simmons 1992) (Galindo, Ladeveze et al. 1995; Bazin, Denis et al. 1999; Bazin, Dejonghe et al. 2004)

Hybrid dysgenesis

Penelope retrotransposon and other transposable elements

D. virilis

(Scheinker, Lozovskaya et al. 1990; Zelentsova, Poluectova et al. 1999; Evgen'ev, Zelentsova et al. 2000; Lyozin, Makarova et al. 2001; Pyatkov, Shostak et al. 2002; Blumenstiel and Hartl 2005; Evgen'ev and Arkhipova 2005)

Hybrid dysgenesis

Mariner/Tc1, hAT transposons and gypsy/Ty3 LTR retrotransposons

Medfly (Ceratitis capitata)

(Torti, Gomulski et al. 1997; Gomulski, Torti et al. 2004)