bioRxiv (Cold Spring Harbor Laboratory),
Journal Year:
2024,
Volume and Issue:
unknown
Published: Oct. 12, 2024
Abstract
Food
choice
is
an
important
driver
of
speciation
and
invasion
novel
ecological
niches.
However,
we
know
little
about
the
mechanisms
leading
to
changes
in
dietary
preference.
Here,
use
three
closely-related
species
Drosophila
sechellia
,
D.
simulans
melanogaster
study
taste
circuit
food
evolution.
sechellia,
a
host
specialist,
feeds
exclusively
on
single
fruit
(
Morinda
citrifolia
noni)
-
latter
two
are
generalists
living
various
substrates.
Using
quantitative
feeding
assays,
recapitulate
preference
for
noni
detect
conserved
sweet
but
altered
bitter
sensitivity
via
calcium
imaging
peripheral
neurons.
Noni
surprisingly
activates
sensing
neurons
more
strongly
due
small
deletion
one
gustatory
receptor.
volumetric
ventral
brain,
show
that
instead
physiology,
species-specific
processing
sugar
signals
sensorimotor
circuits
recapitulates
differences
Our
data
support
receptor
alone
cannot
explain
rather
modifications
how
sensory
information
transformed
into
motor
commands.
New plant protection.,
Journal Year:
2024,
Volume and Issue:
unknown
Published: Nov. 7, 2024
Insects
rely
on
their
sense
of
smell
for
key
aspects
life,
such
as
finding
a
mate,
detecting
food
sources,
conveying
social
information,
and
alerting
conspecifics
about
potential
danger.
A
major
breakthrough
in
understanding
the
mechanisms
by
which
insects
detect
odorant
cues
was
achieved
25
years
ago
with
discovery
first
insect
receptors
(ORs),1-3
are
proteins
mainly
expressed
antennae
(Figure
1A).
Since
then,
combination
situ
hybridization,
immunostaining,
heterologous
expression
followed
functional
studies,
mutagenesis,
knockout
experiments,
physiological
behavioral
studies
has
revealed
that
ORs
seven-transmembrane
domain
unrelated
to
classical
G-protein-coupled
form
ligand-gated
ion
channels
consist
heteromeric
complexes.4
In
most
species
(Neoptera),
these
complexes
comprise
divergent,
ligand-specific
subunit
binds
volatile
(the
OR
subunit)
co-receptor
named
Orco,5
is
highly
conserved
across
species.6
Orco
does
not
bind
volatiles,
but
necessary
trafficking
dendritic
membrane
olfactory
sensory
neurons
assembly
OR-Orco
complex.7
Structural
bases
olfaction.
(A)
The
pea
aphid
expresses
at
OSNs
housed
antennae.
(B)
Side
view
an
OSN.
OR5
(green),
alarm
pheromone
receptor,
forms
heterotetrameric
complex
subunits
(Orco,
purple)
main
stoichiometry
1:3.
unbound
structure
(left),
channel
pore
closed.
Upon
ligand
binding
(right),
conformation
three
change,
modified,
enlarging
entry.
Ions
can
then
enter
travel
neuron
cytosol
via
lateral
pores,
leading
neuron's
electrical
response.
(C)
Top
OR5-Orco
tetrameric
(left)
ligand-bound
states
(right).
ORs,
receptors;
OSNs,
neurons.
last
years,
advances
cryogenic
electron
microscopy
approaches
software
innovations
have
enabled
researchers
establish,
independently,
very
tri-dimensional
structures
Orco8
OR9
atomic
scale.
These
achievements
revealed,
both
cases,
homotetrameric
pinwheel
surrounding
ion-conducting
pore,
strikingly
high
similarity
between
two
structures,
formed
one
transmembrane
helices
from
each
center
complex.
However,
full
insights
into
structural
basis
olfaction
were
awaited,
remained
unexplored.
new
groundbreaking
work
published
June
journal
Science,
been
deciphered
plant
pest,
Acyrthosiphon
pisum
(further
referred
Apis).10
More
precisely,
this
landmark
paper
focuses
receptor
aphid's
chemical
ecology,
ApisOR5-ApisOrco,
ApisOR5
previously
determined
essential
used
alert
danger.11
Both
apo-
(without
ligand)
ApisOR5-ApisOrco
heterocomplex
resolved
3–3.5
Å,
range
previous
studies.
Although
equal
2
OR-2
suspected,
study
unexpected
OR-three
stoichiometry,
confirmed
back-to-back
same
issue
Science
focusing
disease-vector
mosquito
species,
Aedes
aegyptii
(vector
yellow
dengue
fever)
Anopheles
gambiae
malaria).12
Despite
sequence
divergence,
overall
whether
or
ligand-bound,
similar
alone
alone8,
9:
it
presents
architecture,
intracellular
anchor
fourth
seventh
four
subunits,
ones
lining
central
conduits
opening
1B,C).
surprisingly,
established
Orco.
Interestingly,
further
fluorescent
experiments
computational
simulations
based
modeling
molecular
dynamics
suggest
1:3
2:2
may
coexist.
Whether
and/or
reflects
ApisOR5-Orco
vivo
remains
be
determined,
protein
studied
produced
vitro
expression.
fact,
even
more
than
observed
vitro.
Early
Lepidoptera
Diptera
challenged
express
only
type
OR,
addition
Orco.13,
14
Using
immunofluorescence,
single-nucleus
RNA
sequencing,
recent
discoveries
unconventional
co-expression
multiple
within
single
mosquitoes.15,
16
With
types
given
neuron,
would
different
assemble
making
1:1:2
ORx-ORy-Orco-Orco
complexes?
As
3:1
also
Wang
et
al.,
any
1:1:1:1
ORx-ORy-ORz-Orco
assemble?
Such
combinations
appear
multiples,
possibly
detection
spectrum
Yet,
known
if
co-expressed
neurons,
investigation
revolutionize
our
structures.
Comparison
allowed
defining
ligand-binding
pocket,
amino
acids
point
mutation
experiments.
importantly,
comparison
asymmetric
mechanism
homotetramers.
act
scaffolding
components,
change
much
upon
binding,
whereas
undergoes
conformational
modifications,
sequential
helix
rotations.
Ligand
results
direct
rotation
fifth
sixth
subunit,
part
helix,
permeation
path
extracellular
gate
allowing
entry
flux
pores
This
work,
coupled
OR-Orco,12
clarifies
distinct
roles
heterocomplex.
It
provides
crucial
mechanistic
how
recognition
leads
gating
influx.
Remarkably,
elucidated
date
Neoptera
basal
Archaeognatha,
those
related
gustatory
receptors,17,
18
evolved.
Thanks
pioneer
study,
we
predict
come,
diverse
us
decipher
tuning,
specificity,
sensitivity
evolved
meet
plethora
needs.
Moreover,
elucidation
interactions
acid
level
open
up
possibility
understand
accommodate
divergent
complexes,
question
all
utilizing
genome
contains
69
genes,
excluding
pseudogenes.19
Some
present
relative
conservation
sequences,
others
differentiation.
Resolving
additional
ApisOR-Orco
will
allow
alignments,
pinpointing
features
explain
could
Lastly,
details
activation
makes
possible
design
targeted
compounds
disrupt
processes
pest
disease
vectors,
supporting
innovative
control
potentially
effective
environmentally
friendly
strategies
agricultural
public
health
contexts.
Emmanuelle
Jacquin-Joly:
Funding
acquisition;
writing—original
draft;
conceptualization.
Work
Jacquin-Joly
Laboratory
supported
grants
French
National
Research
Agency
(ANR-20-CE20-0003),
Institute
Agriculture,
Food
Environment
(INRAE),
Government
(PNRI),
Embassy
China
(COMIX),
CAAS-INRAE
Associated
International
Plant
Protection,
ADOPT-IPM
EU-China
Joint
action
increase
development
adoption
IPM
tools
(European
Union's
Horizon
Europe
Innovation
program
Grant
Agreement
No
101060430).
author
declares
no
conflicts
interest.
Data
sharing
applicable
article
datasets
generated
analyzed
during
current
study.
bioRxiv (Cold Spring Harbor Laboratory),
Journal Year:
2024,
Volume and Issue:
unknown
Published: Oct. 12, 2024
Abstract
Food
choice
is
an
important
driver
of
speciation
and
invasion
novel
ecological
niches.
However,
we
know
little
about
the
mechanisms
leading
to
changes
in
dietary
preference.
Here,
use
three
closely-related
species
Drosophila
sechellia
,
D.
simulans
melanogaster
study
taste
circuit
food
evolution.
sechellia,
a
host
specialist,
feeds
exclusively
on
single
fruit
(
Morinda
citrifolia
noni)
-
latter
two
are
generalists
living
various
substrates.
Using
quantitative
feeding
assays,
recapitulate
preference
for
noni
detect
conserved
sweet
but
altered
bitter
sensitivity
via
calcium
imaging
peripheral
neurons.
Noni
surprisingly
activates
sensing
neurons
more
strongly
due
small
deletion
one
gustatory
receptor.
volumetric
ventral
brain,
show
that
instead
physiology,
species-specific
processing
sugar
signals
sensorimotor
circuits
recapitulates
differences
Our
data
support
receptor
alone
cannot
explain
rather
modifications
how
sensory
information
transformed
into
motor
commands.