Presence of the deleted hobo element Th in Eurasian populations of Drosophila melanogaster

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Presence of the deleted hobo element Th in Eurasian

populations of Drosophila melanogaster

Georges Périquet, M.H. Hamelin, Y. Bigot, Kai Hu

To cite this version:

Original

article

Presence

of

the deleted

hobo element Th in

Eurasian

populations

of

_{Drosophila melanogaster}

G.

_Periquet

M.H.

Hamelin

Y.

_Bigot

Kai Hu

1 _{Institut de}

Biocdnotique Expérimentale

des Agrosystdmes, Faculté des Sciences, Parc Grand-mont, 37200 Tours, France,

2

_{Biology Department, University}

_{of Hainan, Hainandao,}

_{Peoples’ Republic}

_{of China}

(received 3-1-1988, accepted 6-7-1988)

Summary —

Molecular analysis has revealed _{the presence of} a

_specific

deletion-derivative hobo element, the Th _element, in all current strains of

_{Drosophila melanogaster}

examined

_throughout

the Eurasian continent. The Th element is characterized by an internal deletion of 1.5 kb as _compared to the _{complete hobo element. The presence of this element in natural} populations raises the ques-tion of its

_possible

role in the

_regulation

of the hobo _system.

Drosophila- transposable

elements - hobo-

_populations

Résumé — Présence de l’élément hobo délété Th dans les

_populations

eurasiennes de

Dro-sophila melanogaster.

Un élément hobo défectif

_{(élément Th), présentant}

une délétion interne de 1,5 kb a été mis en évidence par analyse moléculaire. Cet élément est présent dans toutes les souches actuelles de _{Drosophila melanogaster} examinées sur le continent eurasien. Sa

_présence

dans les populations naturelles pose la question de son rôle éventuel dans le mécanisme de

régu-lation du _système hobo.

Drosophila -

éléments

_{transposables -}

hobo -

_populations

Introduction

In

_{Drosophila melanogaster,}

_{the progeny} of certain out-crosses is characterized

_by

a

number of

_germline

abnormalities,

including

chromosome

_{breakage, high}

mutation rates,

sterility,

and male recombination. This

syndrome

has been termed

_{hybrid dysgenesis}

(Kidwell

et al.,

1977).

Three

_independent

_systems

of

_transposable

elements

_(i,

P,

hobo)

can

_produce

these anomalies

_through

the interaction of

chromosomal,

cytoplasmic,

and environmental factors

_(see

reviews

_by

Blackman and

Gelbart,

1988;

Engels,

1988; Louis

In the hobo

_system,

molecular

_analysis

has determined 2 classes of strains defined

by

their hobo elements. H strains contain 3.0-kb full-sized elements and numerous smaller

derivatives,

whereas E strains lack all such elements.

In most strains

examined,

the number of 3.0-kb elements is low, about 2-10

_copies

per genome, while smaller elements appear to be more numerous, from 30 to 75. These elements

_usually

form

_only

a few size classes, with each member of a class

_having

the

same internal deletion

_(Streck

et aL,

1986; Blackman

et al.,

1987).

However,

different H

strains,

tested from different

_laboratory

stocks,

harbor different classes of defective ele-ments. The

_homogeneity

of defective elements within a

_given

strain contrasts with the

heterogeneity

of the size classes among different strains. The presence of identical defective elements

_throughout

these strains has

_suggested

the

_predominance

of

prefe-rence for the

_{amplification}

of defective elements rather than

_complete

elements

(Black-man and

Gelbart,

1988).

In this _paper, we _report the

_analysis

of current strains collected from natural

popula-tions over the Eurasian continent and show _{the presence of 2}

_major

classes of hobo

ele-ments, a 3.0-kb element class and one

_particular

deletion-derivative class of elements which have accumulated in all

_{naturally occurring}

strains

_throughout

the continent.

Materials and Methods

Southern blot analyses were performed on DNA extracted from 31 strains of D. melanogaster, esta-blised by mass _culture, from natural

_populations

collected from France to China in 1986-87 ₍₁₁

strains), and in 1981-84 (20

strains).

Standard

_techniques

were used for DNA extraction,

gel

electrophoresis,

blotting,

hybridization,

Results

The results of Southern blot

_analyses

are shown in

_Fig.

2a for natural strains collected in

1986-87, and in

_Fig.

2b for the 1981-84

_sampling.

About 4 gg of each

_drosophila

geno-mic DNA was

_digested

with Xhol and

_probed

with

_pRG

2.6 X. _{The presence} of full-sized

3.0-kb hobo elements

_gives

rise to a 2.6-kb Xhol

_fragment

with this

probe. Any

other bands are due to the _{presence of} hobo deletion-derivatives which either have a deletion

between the Xhol sites or have lost a Xhol site.

All strains _{contain sequences}

_homologous

to the

_{probe. However,}

in the Paris strain the 2.6-kb band was not detected, and in the other strains

_strong

differences in the

inten-sity

of this band were

_observed,

_reflecting

variations in the number of full-sized elements

present

in each strain. More

_strikingly,

all 31 of the Eurasian strains tested show a

mar-ked band of

_{hybridization}

at

1.1

kb. This band _appears to be derived from several

_copies

of a

_particular

class of deleted hobo

_element,

in turn derived from a 3.0-kb element

_by

an

internal deletion of about 1.5 kb located between the 2 Xhol sites

_(Fig.

₁

_{). We}

refer to this element as the Th element as it was first detected from the French Tours

₍₈₂₎

strain. The

presence of this element

was

also detected in current

_populations

of the United States and

_Mexico,

but not in the

_early

collected strains:

_Oregon-R

_S

_{(USA, 1920-30)}

Paris

(1945),

and Marseillan

_{(France, 1965).}

Discussion

Our _survey of natural

_populations

shows that the 3.0-kb hobo element and its

deletion-derivative Th element are

_present

in all Eurasian

_populations

examined. No other

deriva-tive hobo elements have been accumulated to such a

_great

extent, in terms _{of either}

geo-graphic

distribution or

_copy-number.

Hobo elements have been

_implicated

as determinants of

_{genetic instability,}

but their contribution to

_{hybrid dysgenesis}

remains to be determined

_(Blackman

and

_Gelbart,

1988;

Louis and

_{Yannopoulos, 1988).}

The hobo

_system

has

_{genetic analogies}

with the P-M

_system,

_although

the molecular sequences of the elements are different. In the P-M

system,

genetic instability

is

_{clearly promoted by complete}

2.9-kb P elements which

encode for a

_{transposase (Rio et aL,}

1986;

Engels,

1988).

Other smaller and defective P

elements are also

_present

in the

_Drosophila

_genome,

either associated with

_complete

P

element or alone.

The distributions of the P and hobo elements in the Eurasian

_population

show

_striking

similarities. In the

_P-Msystem,

molecular and

_genetic

_analysis

has revealed a

_specific

P

deletion-derivative, the

KR

element, present

in all

_{naturally occurring}

strains in

Europe-USSR (Black

et

al.,

1987)

and China

_{(Anxolabehere}

et

_al.,

_{unpublished data).}

The KP element appears to be

_implicated

in the

_regulatory

mechanisms of P-induced

hybrid dysgenesis (Black

et

_{al., 1987).}

These authors

_suggested

that the accumulation of KP elements in natural

_populations

is due to the selection of individuals with the

_highest

numbers of KP

_elements,

in which P

_{hybrid dysgenesis}

is

_suppressed.

In

the hobo

_system,

all 3.0-kb elements found in nature are not

_necessarily

_functional,

labora-tory

strains

_(Blackman

and

_{Gelbart, 1988). However,}

the induction of

_genetic

instabilities

by

strains isolated from a natural Greek

_population

_suggests

that intact hobo elements

are

_present

in the wild and may express their

dysgenic properties (Yannopoulos

et

al.,

1987). According

to this

_hypothesis,

_{the presence of the Th element may be}

_interpreted

as a contribution to the

_regulatory

mechanisms of the hobo

_{system. Moreover,}

their

absence in some old

_laboratory

strains raises the

_question

of their

_putative

recent

_origin

and

_expansion.

References

Black D.M., Jackson M.S., Kidwell M.G. & Dover G.A. (1987) KP elements _repress P induced

dys-genesis

in

_Drosophila

_{melanogaster.} EMBO J. 6, 4125-4135

Blackman R.K. & Gelbart W.M.

₍₁₉₈₈₎

The

_transposable

element hobo of

_{Drosophila melanogaster.}

In: Mobile DNA _{(D.E Berg} and M.M. Howe, eds.), American

_Society

for

_Microbiology

Publications _(in

press)

Blackman R.K., Grimaila R., Koehler M.M.D. & Gelbart W.M. ₍₁₉₈₇₎ Mobilization of hobo elements

residing within the

_{decapentaplegic}

gene complex: suggestion of a new hybrid

dysgeneisi

system in

Drosophila melanogaster.

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eds.),

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_Microbiology

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₍₁₉₈₆₎

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_transposable

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