A
framework
for
species
selection: sequencing
of
insects
to
explore
the
evolution
and
maintenance
of
symbiotic
associations
Prepared
by: Nicole
Gerardo,
Emory
University
(nicole.gerardo@emory.edu)
Alex
Wilson,
University
of
Miami
(acwilson@bio.miami.edu) Overview Organisms
across
many
kingdoms
of
life
are
associated
with
microbial
partners
that
shape
their
hosts'
diet
breadth
and
ability
to
combat
disease.
Some
of
the
best
insights
into
the
establishment,
evolution
and
maint enance
of
these
associations
have
come
from
the
study
of
insects
associated
with
obligate
microbial
symbionts.
Recently,
the
availability
of
paired
insect
and
symbiont
genomes
has
greatly
advanced
our
understanding
of
host- symbiont
interactions
(Gerardo,
Wilson,
2011).
Here,
we
suggest
sequencing
a
suite
of
phylogenetically
diverse
insects
with
intimate
associations
with
microbial
partners.
Symbiosis
is
critical
to
defining
the
ecology
and
evolution
of
many
arthropods
(Moran,
2006).
Many
insect
symbionts
are
nutritional
partners, synthesizing
nutrients
that
their
hosts
do
not
get
from
their
diet.
Thus,
symbionts
shape
the
host
plant
range
of
insects;
many
of
these
plants
are agricultural
crops.
Other
symbionts
provide
a
role
in
defense
against
environmental
stressors,
parasites
and
pathogens.
Studies
of
insect
symbioses
can
therefore
provide
insight
into
multiple
aspects
of
arthropod
ecology
and
evolution.
For
example,
metabo lic
complementary
is
predicted
for
hosts
and
their
associated
microbes.
Pathways
for
amino
acid
synthesis
are
shared
between
pea
aphids
(Acythrosiphon
pisum )
and
their
obligate
symbiont
Buchnera
aphidicola (Wilson et
al. ,
2010).
Similar interchange
is
predicted
between
the
glassy winged
sharpshooter
(Homalodisca
coagulata)
and
its
two
obligate
bacterial
symbionts,
Sulcia
muelleri
and
Baumannia
cicadellinicola
(Wu et
al.,
2006). Study of
insect- symbiont
associations
can
also
provide
insight
into
how
animals
and
symbionts
establish
associations
in
the
presence
of
immune
systems
meant
to
clear
microbes
and
how
hosts
regulate
symbiont
populations.
This
list
is
meant
to
highlight
how
the
I5K
initiative
can
provide
insight
into
one
important
aspect
of insect
ecology
and
evolution,
and
will
hopefully
inform
species
selection
as
the
project
proceeds.
While
many
insects
have
associations
with
microbial
partners,
we
focus
this
list
on
species
with
obligate
symbiotic
associations.
Many
of
the
symbiotic
part ners
of
these
insects
have
already
been
sequenced,
allowing
for
immediate
assessment
of
the
complementarity
of host
and
symbiont
genomes.
In
addition
to
these
core
species
that are
obligate
and
frequently
intracellular,
w e
also
suggest
a
handful
of species
with
looser
symbiotic
associations
that
can
serve
as
a
basis
for
beginning
to
explore
the
adaptations
specific
to
the
obligate
symbiotic
lifestyle.
Many
of
these
species
have
been
nominated
by
other
researchers
for
their
agricultural
or
phylogenetic
importance,
highlighting
the
role
that
one
species
can
play
in
shaping
knowledge
in
many
disciplines.
1
List
of
Suggested
Focal
Insects
with
Brief
Description
of
Symbiotic
Association s
Aphi ds Cinara
cedri ,
cedar
aphid
Tuberaphis
styraci ,
gall -forming
social
aphid Cerataphis
brasiliensis,
the
palm
aphid Ceratovacuna
nekoashi
Adelges
tsugae, the
hemlock
w ooly
a delgid Daktulosphaira
vitifoliae ,
grape
phylloxera Aphids
are
globally
distributed,
economically
important
insects
that
include
the
first
symbiotic
consortia
for
which
all
members
had
fully
sequenced
genomes
(IAGC,
2010;
Shigenobu
et
al. ,
2000).
Currently,
the
genome
of
Acyrthosiphon
pisum (pea aphid)
has
been
sequenced, and
the
genomes
of
Myzus
persicae (green
peach
aphid)
and
Aphis
gossypii (cotton
aphid)
are
being
sequenced.
We
propose
to
sequence
a
phylogenetically
nested
group
of
aphid
taxa
that
differ
in
their
symbiotic
consortia.
These
include
(1)
taxa
that
depend
solely
on
the
primary
obligate
intracellular
gammaproteobacteria
Buchnera
aphidicola (A.
pisum ,
M.
persicae ,
A. gossypii
and
Ceratovacuna
nekoashi );
(2)
taxa
dependent
on
a
bacterial
consortium
(Cinara cedri,
which
needs
both Buchnera
aphidicola
and Serratia
symbiotica);
(3)
taxa
that
have
secondarily
developed
novel
microbial
consortia
(Tuberaphis
styraci ,
a
gall
forming
aphid in
which
Buchnera has
been
replaced
by
an
extracellular
fungal
symbiont
(Hongoh,
Ishikawa,
2000)
and Cerataphis
brasiliensis , which
also
has
a
fungal
rather
than
bacte
rial
symbiont) ;
and
(4)
outgroups
that
include
an
a delgid
(Adelges
tsugae)
that
possesses
a
Buchnera - like
symbiont
and
Daktulosphaira
vitifoliae ,
grape
phylloxera,
an
aphid- like
insect
that
does
not
contain
Buchnera . Many
of
these
species
can
be
reared
in
the
laboratory,
and
many
have associations
with
facultative
symbionts
as
well.
Mealybugs Planococcus
citri ,
citrus
mealybug The
citrus
mealybug,
Planococcus citri ,
is
globally
distributed
and
feeds
on
phloem
sap. Among
other
plants,
it
is
a
pest
of
citrus
and
ornamental
plants. P.
citri represents
the
scale
insects,
the
sister
taxon
of
aphids,
phylloxerids
and
adelgids
(Von
Dohlen,
Moran,
1995);
thus
it
is
an
outgroup
for
studies
on
symbioses
of
aphids
and
their
kin.
Like
aphids
and
other
phloem
feeders,
P.
citri relies
on
intracellular
bacterial
symbionts
to
provision
them
with
essential
amino
acids
deficient
in
their
phloem
sap
diet.
Unlike
aphids
and
other
phloem
feeders,
P.
citri uniquely
harbors
two
nested
symbionts
(Tremblaya
and
Moranella)
within
their
bac teriocytes
(von
Dohlen
et
al. ,
2001).
The
genomes
of
Tremblaya
and
Moranella
reveal
a
tightly
interdependent
network
of
amino
acid
metabolism
between
the
symbionts
that
most likely
also
includes
the
host (McCutcheon,
Von
Dohlen,
2011).
The
nested
organization
of
these
symbionts
provides
an
opportunity
to
study
how 2
regulation
of
symbionts , and
metabolic
interactions
between
the
symbionts
and
the
host, are
influenced
by
an
additional
level
of
compartmentalization
from
wh at
is
observed
in
other
insects.
Leafhoppers Euscelidius
variegatus , leafhopper The
leafhopper
Euscelidius variegatus
does
not
have
an
association
with
an
ancient
obligate
symbiosis
but
presence
of
the
maternally
transmitted
primary
symbiont
BEV,
which
has
b een
sequenced,
affects
fecundity,
longevity
and
developmental
time.
Unlike
many
prim ary
symbionts,
this
symbiont
persists
both
within
tissues
and
freefloating
in
the
hemolymph,
suggesting
that
it
must
evade
host
immune
responses
or
that
the
host
recognizes
but
does
not
clear
its
beneficial
partner.
Facilitating
future
investigations,
the
symbiont
BEV
can
be
cultivated,
allo wing
for
manipulation
of
host - symbiont
associations
(Degnan
et
al. ,
2011).
True
Bugs Megacopta
cribraria ,
soybean
bug
or
kudzu
bug Riptortus
clavatus ,
broad -headed
bug Megalotomus
quinquespinosus ,
lupine
bug The
stinkbug
Megacopta
cribraria is
a
pest
on
soybean s
in
ma n y
parts
of
Asia
and
has
recently
invaded
North
America
(Jenkins
et
al. ,
2010),
where
it
is
spreading
rapidly
in
the
Southeastern
United
States.
The
bugs
are
born
symbiont
free
and
then
immediately
feed
on
symbiont
housing
capsules
left
near
the
eggs
by
their
mothers
(Hosokawa et
al. ,
2007a).
This
allows
for
easy
comparison
of
symbiont- free
and
symbiont- harboring
insects.
Work
on
Japanese
populations
suggests
that
the
symbiont
genotype
dictates
whether
a
Megacopta can
or
cannot
use
soybeans (Hosokawa et
al. ,
2007b).
The
symbiont
genome
has
been
sequenced.
M.
cribraria can
be reared
in
the
lab.
The
holy
grail
of
studying
host- microbe
interactions
is
to
be
able
to
work
wit h
experimentally
tractable
systems
in
which
host
and
symbiont
can
be
reared
separately,
allowing
for
(1)
easy
comparison
of
symbiont
and
symbiont - free
hosts,
and
(2)
genetic
manipulation
and
then
reintroduction
of
symbionts.
Unlike
most
insects,
which
pass
their
obligate
symbionts
vertically
from
one
generation
to
the
next,
broad - headed
bugs
acquire
their
symbiotic
Burkholderia bacteria
from
the
environment
in
every
generation
(Kikuchi et
al. ,
2011).
In
at
least
two
spec ies,
Riptortus
clavatus
and
Megalotomus
quinquespinosus ,
the
bacter ia
increase
developmental
rate and
adult
size (Kikuchi et
al. ,
2007)(N.M.
Gerardo,
unpublished
data) .
E nvironmental
acquisition
provides
several
benefits
for
the
study
of
symbiosis.
First,
because
the
bacteria
must
survive
outside
the
host,
they
can
be
cultivated,
facilitating
genetic
manipulations
of
the
symbiont
and
controlled
infections
of
the
host.
Second,
symbiotic
and
aposymbiotic
insects
can
be
ea sily
reared
and
compared.
This
model
is
an
excellent
parallel to
the
well - studied
symbioses
of
Vibrio bacteria
and
squid ,
and
of
rhizobial
bacteria
and
legume
plants ,
3
which
also
acquire
their
bacterial symbionts
from
the
environment.
Because
of
their
potential as
models
for
study
of
host- symbiont
interactions,
w e
suggest sequencing
of
one
Asian
(Riptortus
clavatus )
and
one
North
American
(Megalotomus
quinquespinosus )
host,
each
of
which
are
amenable
to
laboratory
rearing.
Cicadas,
Sharpshooters
and
Spittlebug s
( Auchenorrhyncha)
Diceroprocta
semicincta ,
cicada Homalodisca
vitripennis ,
g
lassy-winged
sharpshooter Clastoptera
arizonana,
spittlebug X ylem - feeding
insects
of
the
Auchenorrhyncha
are
sustained
by
symbiotic
consortia
centered
around
Sulcia
mu e lleri
(a
Bac teroidetes)
and
partnered
with
different
coresident
symbionts
from
very
different
bacterial
taxa.
In
all
cases
Sulcia synthesizes
the
majority
of
the
essential
amino
acids
while
the
bacterial
coresidents
synthesize
the
remaining
minority;
the
amino
acid
biosynthetic
capabilities
of
the
coresident
symbionts
are
perfectly
complementary
(McCutcheon,
Moran,
2010). Based
on
the
capabilities
of
the
bacteria,
each
host
is
predicted
to
play
a
role
in
transport
and
synthesis.
Genome
sequencing
of
Diceroprocta
semicincta,
Homalodisca
vitripennis and
Clastoptera
arizonana
will
facilitate
confirmation
of
these
predictions.
Additionally,
H.
vitripennis is
a
major
vector
of
the
bacterial
plant
pathogen
Xylella
fastidisoa,
which
is
the
cause
of
variety
of
plant
diseases,
including
Pierce’s
disease
in
grapes
and
phony
peach
disease.
Beetles
Lasioderma
se
rricorne ,
cigarette
beetle Stegobium paniceum ,
drug
store
beetle Dendroctonus
ponderosae ,
mountain
pine
beetle While
many
of
the
best - studied
insect- microbe
symbioses
involve
bacteria,
several
insects
have
fungal
rather
than
bacterial
partners.
The
complexity
of
fungal
eukaryotic
genomes
may
fundamentally
change
selection
pressure s
on
the
genome
of
their
insect
hosts
relative
to
selection
on
insects
with
bacterial
partners .
Lasioderma
serricorne and
Stegobium
paniceum have
fungal
endosymbionts
(Symbiotaphrina
kochii and
S.
buchneri ,
respectively)
that
live
inside
their
gut (Noda,
Kodama,
1996).
In
contrast,
Dendroctonus
ponderosae has
a
suite
of
ectosymbionts
that
they
use
to
line
their
broad
chambers .
The
genome
of
one
of
these
fungal
symbionts
( Grosmannia
clavigera)
has
been
sequenced
(DiGuistini
et
al.,
2011).
Sequencing
of
these
insects
would
provide
insight
into
three
pests
and
would
facilitate
exploration
of how
fungal
vs.
bacterial
symbionts,
and
how
endosymbionts
vs.
ectosymbionts,
impact
host
genome
evolution.
Termites Macrotermes
bellicosus ,
African
fungus -growing
termite Genome
sequences
of
two
fungus- growing
ants
( Atta
cephalotes
and
Acromyrmex
octospinosus
)
have
revealed
the
potential
for
genome
complementarity
between
4
insects
and
exosymbionts
(i.e., symbionts
that
live
outside
of
the
host)
(Suen et
al. ,
2011).
Specifically,
both
ants
are
missing
part
of
the
arginine
synthesis
pathway,
and
it
is
hypothesized
that
this
loss
is
compensated
for
by
the
fungi
that
the
ants’
cultivate
.
Sequencing
of
fungus - growing
termites
will provide
confirmation
of
such
complementarity
in
a
different
insect
lineage.
Sequencing
of
one
fungus- growing
termite,
Macrotermes
natalensis
is
underway,
and
we
suggest
sequencing
of
other
fungus - growers,
including
Macrotermes
bellicosus .
Categorization
of
Insect
-Symbiont
Systems
in
Terms
of
Key
Features This
list
is
not
meant
to
be
exhaustive
but
highlights
some
of
the
key
features
of
potentially
informative
hosts
of
obligate
symbioses.
Some
species
are
listed
more
than
once. Species
with
sequenced
symbiont
genomes but
no
available
host
genome • Megacopta
cribraria ,
soybean
bug • Cerataphis
brasiliensis,
palm
aphid
( sequencing
of
fungal
symbiont
underway)
• Ceratovacuna
nekoashi
• Cinara
cedri ,
cedar
aphid
• Planococus
citri ,
the
citrus
m ealybug •
Draeculacephala
minerva ,
green
sharpshooter
• Homalodisca
vitripennis,
glassy - winged
sharpshooter
• Clastoptera
arizonana,
spittlebug
• Dendroctonus
ponderosae ,
mountain
pine
beetle • Diceroprocta
semicincta ,
desert
cicada
• Pachypsylla
venusta ,
hackberry
petiole
gall
psyllid Species
with
easily
manipulated
symbiotic
associations
• Megacopta
cribraria ,
soybean
bug (symbiont
can
be
removed
before
birth)
• Riptor t us
clavatus,
b road- headed
bug
(bacteria
can
be
cultivated) • Megalotomus
quinquespinosus, broad- headed
bug
(bacteria
can
be
cultivated) • Euscelidius
variegatus ,
leafhopper
(bacteria
can
be
cultivated) • Glossiana
morsitans,
t setse
fly
(bacteria
can
be
genetically
manipulated) • Rhodnius
prolixus,
kissing
or
assassin
bug
(bacteria
can
be
genetically
manipulated) Species
with
unusual
or
atypical symbiotic
associations •
Tuberaphis
styraci (aphid
with
fungal
rather
than
bacterial
symbiont) • Cerataphis
brasiliensis
(aphid
with
fungal
rather
than
bacterial
symbiont) • Riptorus
clavatus ,
b road- headed
bug
(environmentally
acquire
symbiont
every
generation)
• Megalotomus
quinquespinosus ,
broad- headed
bug
(environmentally
acquire
symbiont
every
generation)
5
• Planococcus
citri (one
bacterial
symbiont
lives
inside
the
other)
Species
that
serve
as
o utgroups
to
those
with
well -studied
obligate
symbioses • Adelges
tsugae,
the
hemlock
wooly
adelgid
• Daktulosphaira
vitifoliae,
grape
phylloxera • Planococus
citri ,
the
citrus
mealybug Species
currently
proposed
for
sequencing
via
I5K
that
could
inform
studies
of
symbioses (as
of
Aug
1
2011) *
• Anasa
tristis, the
squash
bug • Attine
ants,
fungus growing
ants
(multiple
species
proposed)
• Cicadulina
mbila,
maize
leafhopper
• Cimex
lectularius,
bed
bug • Dendroctonus
spp. ,
pine
beetle s
(multiple
species
proposed)
• Euryaulax
carnifex,
sugarcane
spittlebug • Euscelidius
variegatus,
leafhopper
• Frankliniella
occidentalis,
western
flower
thrip
• Halyomorpha
halys,
brown
marmorated
stink
bug • Homolodisca
vitripennis,
glassy - winged
sharpshooter
• Lygus
lineolaris,
tarnished
plant bug • Macrosteles
quadrilineatus,
aster
leafhopper
• Nilaparvata
lugens,
brown
planthopper
• Oncopeltus
fasciatus,
large
milkweed
bug • Pemphigus
obesinymphae,
popular
petiole
gall
aphid • Planococcus
citri,
citrus
mealybug • Rhopalosiphum
padi,
bird
cheery- oat
bug • S caphoideus
titanus,
American
grapevine
leafhopper
• Schizaphis
graminum,
greenbug *
This
list
is
not
exhaustive
and
will
likely
expand
as
the
number
of
proposed
species
expands.
Completed or
c
urren t
i nsect
genome
projects
with
a ssociated
o bligate
symbioses • Acythrosiphon
pisum ,
pea
aphid • Aphis
gossypi ,
cotton
aphid • Camponutus
floridanus,
carpenter
ant
• Glossian
morsitans,
tsetse
fly
• Macrotermes
natalensis,
fungus - growing
termite
• Myzus
persicae,
green
peach
aphid
• Pediculus
humanus ,
body
louse
• Atta
cephalotes,
fungus - growing
ant •
Acromyrmex
octospinosus ,
fungus - growing
ant • Rhodnius
prolixus,
kissing
or
assassin
bug
6
References
Degnan
PH,
Bittleston
LS,
Hansen
AK,
Sabree
ZL,
Moran
NA,
Almeida
RPP
(2011)
Origin
and
Examination
of
a
Leafhopper
Facultative
Endosymbiont.
Current
Microbiology
62 ,
15651572
DiGuistini
S,
Wang
Y,
Liao
NY,
Taylor
G,
Tanguay
P,
Feau
N,
Henrissat
B,
Chan
S K,
Hesse- Orce
U,
Alamouti
SM,
Tsui
CKM,
Docking
RT,
Levasseur
A,
Haridas
S,
Robertson
G,
Birol
I,
Holt
RA,
Marra
MA,
Hamelin
RC,
Hirst
M,
Jones
SJM,
Bohlmann
J,
Breuil
C
(2011)
Genome
and
transcriptome
analyses
of
the
mountain
pine
beetle - fungal
symbiont
Grosmannia
clavigera,
a
lodgepole
pine
pathogen.
Proceedings
of
the
National
Academy
of
Sciences
of
the
United
States
of
America 108 ,
2504- 2509
Gerardo
NM,
Wilson
ACC
(2011)
The
power
of
paired
genomes.
Molecular
Ecology
20 ,
2038- 2040
Hongoh
Y,
Ishikawa
H
(2000)
Evolutionary
studies
on
uricases
of
fungal
endosymbionts
of
aphids
and
planthoppers.
Journal
of
Molecular
Evolution 51 ,
265- 277
Hosokawa
T,
Kikuchi
Y,
Fukatsu
T
(2007a)
How
many
symbionts
are
provided
by
mothers,
acquired
by
offspring,
and
needed
for
successful
vertical
transmission
in
an
obligate
insect - bacterium
mutualism?
Molecular
Ecology
16 ,
5316- 5325
Hosokawa
T,
Kikuchi
Y,
Shimada
M,
Fukatsu
T
(2007b)
Obligate
symbiont
involved
in
pest
status
of
host
insect.
Proceedings
of
the
Royal
Society
B -Biological
Sciences 274 ,
19791984
IAGC
(2010)
Genome
sequence
of
the
pea
aphid
Acyrthosiphon
pisum .
PLoS
Biology 8 ,
e1000313
Jenkins
TM,
Eaton
TD,
Suiter
DR,
Eger
JE,
Ames
LM,
Buntin
GD
(2010)
Preliminary
genetic
analysis
of
a
recently - discovered
invasive
true
bug
(Hemiptera:
Heteroptera:
Plataspidae)
and
its
bacterial
endosymbiont
in
Georgia,
USA.
Journal
of
Entomological
Science 45 ,
62- 63
Kikuchi
Y,
Hosokawa
T,
Fukatsu
T
(2007)
Insect - microbe
mutualism
without
vertical
transmission:
a
stinkbug
acquires
a
beneficial
gut
symbiont
from
the
environment
every
generation.
Applied
and
Environmental
Microbiology 73 ,
4308- 4316
Kikuchi
Y,
Hosokawa
T,
Fukatsu
T
(2011)
An
ancient
but
promiscuous
host - symbiont
association
between
Burkholderia
gut
s ymbionts
and
their
heteropteran
hosts.
Isme
Journal 5 ,
446- 460
McCutcheon
JP,
Moran
NA
(2010)
Functional
convergence
in
reduced
genomes
of
bacterial
symbionts
spanning
200
My
of
evolution.
Genome
Biology
and
Evolution 2 ,
708- 718
McCutcheon
JP,
Von
Dohlen
CD
(2011)
An
interdependent
metabolic
patchwork
in
the
nested
three- way
symbiosis
of
mealybugs.
Current
Biology in
press Moran
NA
(2006)
Symbiosis.
Current
Biology 16 ,
R866- R871
Noda
H,
Kodama
K
(1996)
Phylogenetic
position
of
yeastlike
endosymbionts
of
Anobiid
beetles.
Applied
and
Environmental
Microbiology 62 ,
162- 167
7
Shigenobu
S,
Watanabe
H,
Hattori
M,
Sakaki
Y,
Ishikawa
H
(2000)
Genome
sequence
of
the
endocellular
bacterial
symbiont
of
aphids
Buchnera sp.
APS.
Nature 407 ,
81- 86
Suen
G,
Teiling
C,
Li
L,
Holt
C,
Abouheif
E,
Bornberg- Bauer
E,
Bouffard
P,
Caldera
EJ,
Cash
E,
Cavanaugh
A,
Denas
O,
Elhaik
E,
Fave
MJ,
Gadau
JR,
Gibson
JD,
Graur
D,
Grubbs
KJ,
Hagen
DE,
Harkins
TT,
Helmkampf
M,
Hu
H,
Johnson
BR,
Kim
J,
Marsh
SE,
Moeller
JA,
Munoz - Torres
MC,
Murphy
MC,
Naughton
MC,
Nigam
S,
Overson
R,
Rajakumar
R,
Reese
JT,
Sco tt
JJ,
Smith
CR,
Tao
S,
Tsutsui
ND,
Viljakainen
L,
Wissler
L,
Yandell
MD,
Zimmer
F,
Taylor
J,
Slater
SC,
Clifton
SW,
Warren
WC,
Elsik
CG,
Smith
CD,
Weinstock
GM,
Gerardo
NM,
Currie
CR
(2011)
The
genome
sequence
of
the
leaf- cutter
ant
Atta
cephalotes reveals
insights
into
its
obligate
symbiotic
lifestyle.
PLoS
Genetics 7
von
Dohlen
CD,
Kohler
S,
Alsop
ST,
McManus
WR
(2001)
Mealybug
beta - proteobacterial
endosymbionts
contain
gamma - proteobacterial
symbionts.
Nature 412 ,
433- 436
Von
Dohlen
CD,
Moran
NA
(1995)
Molecular
phylogeny
of
the
Homptera:
a
paraphyletic
taxon.
Journal
of
Molecular
Evolution 41 ,
211- 223
Wilson
ACC,
Ashton
PD,
Calevro
F,
Charles
H,
Colella
S,
Febvay
G,
Jander
G,
Kushlan
PF,
Macdonald
SJ,
Schwartz
JF,
Thomas
GH,
Douglas
AE
(2010)
Genomic
insight
into
the
amino
acid
relations
of
the
pea
aphid
Acyrthosiphon
pisum with
its
symbiotic
bacterium
Buchnera
aphidicola .
Insect
Molecular
Biology 19 ,
249- 258
Wu
D,
Daugherty
SC,
Van
Aken
SE,
Pai
GH,
Watkins
KL,
Khouri
H,
Tallon
LJ,
Zaborsky
JM,
Dunbar
HE, Tran
PL,
Moran
NA,
Eisen
JA
(2006)
Metabolic
complementarity
and
genomics
of
the
dual
bacterial
symbiosis
of
sharpshooters.
PLoS
Biology 4 ,
1079- 1092
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