E olu ion
o
pho ope iod
sensing
in
plan s
and
algae
Glo ia
Se ano-Bueno
*
,
F ancisco
J
Rome o-Campe o, E a
Lucas-
Reina
*,**
,
Jose
M
Rome o
and
Fede ico
Val e de
Measu ing
day
leng h
con e s
a
s ong
i ness
imp o emen
o
pho osyn he ic
o ganisms
as
i
allows
hem
o
an icipa e
ligh
phases
and
ake
he
bes
decisions
p eceding
diu nal
ansi ions.
In
close
associa ion
wi h
signals
om
he
ci cadian
clock
and
he
pho o ecep o s,
pho ope iodic
sensing
cons i u es
also
a
p ecise
way
o
de e mine
he
passing
o
he
seasons
and
o
ake
annual
decisions
such
as
he
bes
ime
o
lowe
o
he
beginning
o
do mancy.
Pho ope iodic
sensing
in
pho osyn he ic
o ganisms
is
ancien
and
wo
majo
s ages
in
i s
e olu ion
could
be
iden i ied,
he
cyanobac e ial
ime
sensing
and
he
e olu iona y
ool
ki
ha
a ose
in
g een
algae
and
de eloped
in o
he
pho ope iodic
sys em
o
mode n
plan s.
The
mos
ecen
disco e ies
abou
he
e olu ion
o
he
pe cep ion
o
ligh ,
measu emen
o
day
leng h
and
ela ionship
wi h
he
ci cadian
clock
along
he
e olu ion
o
he
euka yo ic
g een
lineage
will
be
discussed
in
his
e iew.
Add ess
Plan
De elopmen
Uni ,
Ins i u e
o
Plan
Biochemis y
and
Pho osyn hesis,
CSIC-Uni e sidad
de
Se illa,
49 h,
Ame ico
Vespucio
A .,
41092
Se illa,
Spain
Co esponding
au ho :
Val e de,
Fede ico
([email p o ec ed].
es)
In oduc ion
Ea h
o a ion
a ound
i s
axis
and
a ound
he
sun
p oduces
p edic able
day
leng h
(pho ope iod)
changes
h ough
he
seasons
ha
plan s
use,
ia
sophis ica ed
mechanisms,
o
measu e
ime
and
ake
c ucial
physiological
decisions
[1].
Pho ope iodism,
o
he
abili y
o
de ec
day
leng h,
is
p esen
in
ea ly
pho osyn he ic
euka yo es
so
ha
algae
can
p oduce
se e al
pho ope iod
esponses
[2].
This
way,
du ing
he
g een
lineage
e olu ion,
pho ope iodism
pe aded
in o
he
majo
physiological
sys ems,
allowing
hem
o
p edic
he
passing
o
he
seasons
and
p epa e
plan s
o
yea - ound
p edic able
changing
condi ions.
The
pho ope iod
sensing
sys em
in ol es
a
way
o
de ec
ligh
(pho o ecep o s)
and
an
in e nal
sys em
o
measu e
ime
(ci cadian
clock).
In
ime
hey
became
so
impo an
o
unicellula
ee
li ing
algae
ha
o
some
ma ine
picoeuka yo es
90%
o
i s
ansc ip ome
is
con olled
by
he
clock
[3].
Howe e ,
mo e
e ol ed
and
lexible
species
like
mode n
plan s,
which
de eloped
he
capaci y
o
adap
o
di e en
en i onmen s,
ha e
educed
his
numbe
o
less
han
50%
[4].
Pa adoxically,
mo e
in e -
wined,
complex
sys ems
allowed
o
a
mo e
independen
esponse
o
ex e nal
cues,
hus
pe mi ing
he
coloniza-
ion
o
e e
demanding
new
niches
and
he
acquisi ion
o
no el
and
complex
physiological
unc ions
[5].
Pho o ecep o s
e olu ion
Li ing
o ganisms
use
a
clus e
o
pho o ecep o s
o
mea-
su e
he
quali y,
quan i y
and
di ec ion
o
ligh
o
modu-
la e
physiological
esponses
o
changing
ligh s
[6].
This
is
pa icula ly
impo an
o
pho osyn he ic
o ganisms
ha
equi e
ligh
ene gy
o
pho osyn hesis
and
consequen ly
o
g ow
and
de elop.
Pho o ecep o s
can
be
di ided
in o
h ee
g oups
acco ding
o
he
ligh
quali y
hey
de ec .
Red
and
a - ed
ligh s
a e
abso bed
by
phy och omes
(PHYs)
while
h ee
ypes
o
pho o ecep o s
pe cei e
he
blue/UV-A:
C yp och omes
(CRYs),
Pho o opins
(PHOTs)
and
h ee
plan -speci ic
LOV/F-box/Kelch-
epea
p o eins
ZEITLUPE
(ZTL),
FLAVIN-BIND-
ING
KELCH
REPEAT
F-BOX
(FKF),
and
LOV
KELCH
REPEAT
PROTEIN
2
(LKP2).
Finally,
UV
RESISTANCE
LOCUS
8
(UVR8)
was
ecen ly
shown
o
be
a
UV-B
pho o ecep o
[7].
Excellen
e iews
on
plan
and
algae
pho o ecep o
s uc u e
and
unc ion
ha e
ecen ly
been
published
[8–13].
The
speci ic
pho o ecep o
se
has
e ol ed
ac oss
pho o-
syn he ic
euka yo es
(Figu e
1).
In
he
chlo ophy e
model
alga
Chlamydomonas
einha d ii,
UV-B
ligh
is
de ec ed
by
UVR8
while
blue/UV-A
is
de ec ed
by
one
PHOT
(pho1),
wo
DASH
(D osophila,
A abidopsis,
Synechocys is
and
Human)
CRYs,
one
plan -like
CRY
(pCRY)
and
one
animal-like
CRY
(aCRY).
The
la e
can
espond
bo h
o
blue
and
ed
ligh
[12,14

,15].
In
he
e n
Adian um
capillus- ene is
ou
canonical
plan
PHYs
ha e
been
**
P esen
add ess:
IHSM-UMA-CSIC,
Depa amen o
de
Biologıı
´a
Molecula
y
Bioquı
´mica,
Uni e sidad
de
Ma
´laga,
29071
Ma
´laga,
Spain.
iden i ied,
wo
PHOTs
and
i e
CRYs
[16].
Fe ns
include
a
speci ic
neoch ome,
a
chime ic
pho o ecep o
consis ing
o
an
N- e minus
PHY
domain
and
se e al
C- e minus
PHOT
domains
ha
can
sense
bo h
blue
and
ed/ a - ed
ligh
o
egula e
chlo oplas
mo emen
and
pho o opism
[6].
Howe e ,
UV-B
pho o ecep o s
ha e
no
been
desc ibed
in
e ns,
hei
absence
jus i ied
by
hei
g ow h
habi s
unde
low-ligh
angiospe m
canopies.
In
he
model
plan
A abidopsis
haliana,
ed/ a - ed
ligh s
a e
de ec ed
by
i e
PHYs
(A-E),
blue/UV-A
by
wo
PHOTs,
h ee
CRYs,
and
ZTL/FKF1/LKP2
p o eins
[6,11,13],
while
UV-B
by
a
canonical
UVR8
(Figu e
1a).
Inc ease
in
pho o ecep o s
numbe
and
unc ion
du ing
plan
e olu-
ion
has
been
ela ed
o
i ness
imp o emen
[9].
In
plan s
and
algae,
pho ope iod
egula es
a
numbe
o
p ocesses
including
pho omo phogenesis,
g ow h,
lowe -
ing,
s ess
ole ance
and
ci cadian
hy hms
[16,17,18

].
In
da kness,
some
o
hese
pa hways
a e
inhibi ed
by
CON-
STITUTIVE
PHOTOMORPHOGENIC
1
(COP1),
a
RING- inge
E3
ubiqui in
ligase.
Du ing
he
day,
COP1
is
inhibi ed
by
he
pho o ecep o s
allowing
he
ac i a ion
o
pho ope iodic-dependen
p ocesses
(Figu e
1a).
A
nigh ,
COP1
in e ac ion
wi h
SUPPRESSOR
OF
PHY-
TOCHROME
A
(SPA1)
a ge s
he
ansc ip ion
ac o s
ELONGATED
HYPOCOTYL
5
(HY5)
and
CON-
STANS
(CO)
o
ubiqui ina ion
and
deg ada ion,
sup-
p essing
pho omo phogenesis
and
lowe ing
espec i ely
[20,21].
Pho oac i a ed
CRY1,
CRY2
and
PHYA
di ec ly
bind
SPA1
and
inhibi
he
o ma ion
o
COP1-SPA1
complex
[19].
PHYB
also
p omo es
COP1-SPA1
dissoci-
a ion
and
pho omo phogenic
de elopmen
[22].
COP1
in e ac ion
wi h
EARLY
FLOWERING
3
(ELF3)
induces
deg ada ion
o
GIGANTEA
(GI),
a
ci cadian
clock
associa ed
p o ein,
p ocess
inhibi ed
by
CRY1/
CRY2
in
blue
ligh
[23].
Upon
UV-B
i adia ion,
UVR8
Figu e
1
C PHO1
C CRY
dash
C CRY
dash C CRYa
C CRYp
UVR8
PHO1
PHO2
CRY1
CRY2
CRY
DASH
FKF1
ZTL
LKP2
PHYB
PHYA
PHYE
PHYD
PHYC
COP1
CO GIHY5
COP1
HY5
UV-B
ole ance
Pho o-
mo phogenesis
Flowe ing Ci cadian
hy hm
C UVR8
C COP1
C HY5
UV-B
ole ance
C COP1
C CO
S a ch bios
yn e
sis
Cell cycle
(a) (b)
Cu en Opinion in Plan Biology
Ligh
signal
ansduc ion
and
pho ope iodic
egula ion
by
COP1
in
A.
haliana
(a)
and
C.
einha d ii
(b).
In
A.
haliana,
pho oac i a ed
CRY1,
CRY2,
PHYA
and
PHYB
inhibi
COP1
allowing
accumula ion
o
e ec o s
and
esul ing
in
he
speci ic
ligh
esponses.
Unde
UV-B,
COP1
ac s
as
posi i e
egula o
ac i a ing,
among
o he s,
UVR8,
HY5
and
consequen ly
up egula ing
UV-B
ole ance
genes.
UV-B
signal
ansduc ion
is
conse ed
in
C.
einha d ii,
al hough
C HY5
implica ion
has
no
been
in es iga ed
(dash
lines).
A ows
indica e
posi i e
egula ion,
while
ba s
ep esen
nega i e
egula ion.
Low
le els
o
C CO
exp ession
obse ed
in
c c ya
mu an
sugges
a
conse ed
CRY-
COP1-CO
pa hway,
al hough
C COP1
implica ion
has
no
been
desc ibed
(dash
lines).
Pho o ecep o s
no
in ol ed
in
COP1
egula ion
a e
shown
in
g ey.
PRR9,
PRR7
and
PRR5
p esen
a
se ies
o
successi e
exp ession
peaks
a
ea ly
mo ning,
mid-day
and
a e noon
espec i ely
(Figu e
2c)
and
hei
p o ein
p oduc s
bind
o
he
same
posi ions
a
he
CCA1
p omo e
whe e
a
G-box
can
be
ound,
ep essing
i s
exp ession
du ing
he
en i e
day,
and
comple ing
he
posi i e/nega i e
eedback
mo ning
loop
[31].
TOC1
(PRR1)
is
di ec ly
ep essed
by
CCA1
using
he
e ening
elemen
loca ed
in
i s
p omo e .
TOC1
in
u n
also
ac s
as
a
ep esso
o
CCA1
o ming
he
cen al
nega i e
eedback
loop
[31].
PRRs
homologues
ha e
been
iden i-
ied
in
all
plan
axa.
A
single
PRR
gene
was
iden i ied
in
he
O.
au i
genome
(O TOC1)
p esen ing
a
simila
exp es-
sion
p o ile
as
TOC1
and
PRR5
(Figu e
2c)
and
symme ic
o
he
one
in
O CCA1,
sugges ing
ha
he
cen al
loop
was
al eady
es ablished
in
algae
and
is
conse ed
ac oss
he
en i e
euka yo ic
g een
lineage
[29

].
Addi ionally,
an
e ening
elemen
has
been
ound
in
he
p omo e
o
O TOC1
p o iding
suppo ing
e idence.
None
o
he
wo
PRRs
iden i ied
in
Chlamydomonas
ollow
simila
exp ession
p o iles
o
any
o
he
PRRs
in
A abidopsis,
which
sugges s
a
di e gen
e olu ion
in
Chlamydomonas
in
he
egula ion
o
ci cadian
hy hms
[32].
Fou
di e en
PRRs
we e
ound
in
he
Physcomi ella
(a
moss
ha
seems
o
ha e
de i ed
om
he
di ec
e olu iona y
line
o
mode n
plan s)
genome.
All
hese
genes
exhibi
he
same
exp es-
sion
pa e n,
peaking
a
dusk
wi h
hei
oughs
a
dawn.
No
di e si ica ion
in
hei
peaking
ime
poin s
like
he
A abidopsis
PRR9/7/5
is
obse ed,
possibly
because
hese
genes
a e
he
esul
o
e y
ecen
duplica ion
e en s
[33].
The
hi d
eedback
loop
is
called
he
e ening
loop
whe e
TOC1
also
plays
a
key
ole
oge he
wi h
GI
and
ZTL
(Figu e
2).
Bo h
genes
ha e
been
shown
o
be
ansc ip-
ionally
co- egula ed
di ec ly
by
CCA1,
PRRs
and
TOC1
[27

,31,34

].
In
u n,
GI
and
ZTL
a e
known
o
o m
a
complex
in ol ed
in
blue
ligh
and
empe a u e
sensing
ha
induces
TOC1
deg ada ion
by
he
26S
p o easome
[35].
I
is
ele an
o
no e
ha
A abidopsis
ZTL
homo-
logue,
FKF1,
oge he
wi h
GI,
media es
CYCLING
DOF
FACTORs
(CDFs)
deg ada ion
and
he
subse-
quen
CO
ac i a ion
[36],
a
connec ion
be ween
he
ci cadian
clock
and
pho ope iodic
lowe ing.
No
po en ial
GI
homologue
has
been
iden i ied
in
mic oalgae
and
Physcomi ella,
bu
i
is
p esen
in
o he
b yophy es
such
as
Ma chan ia
o
Selaginella
and
he
seed
plan s
Picea
and
O yza,
sugges ing
ha
his
gene
is
exclusi e
o
land
plan s
[33].
GI
plays
also
a
c ucial
ole
in
he
empe a u e
compensa ion
o
he
A abidopsis
ci cadian
clock
[37]
and
he
de ec
in
empe a u e
compensa ion
obse ed
in
Physcomi ella
clock
has
been
asc ibed
o
he
absence
o
GI
[33].
ZTL
p esen s
h ee
di e en
p o ein
domains:
N- e minal
LOV
in ol ed
in
blue
ligh
sensing,
F-box
ha
media es
p o ein
ubiqui ina ion,
and
mul iple
C-
e minal
Kelch
domains
in ol ed
in
p o ein
in e ac ions.
Simila
o
GI,
ZTL
homologs
ha e
only
been
iden i ied
in
monome izes
and
in e ac s
wi h
COP1,
p omo ing
he
exp ession
o
HY5,
which
is
esponsible
o
ac i a ion
o
UV-B
esponsi e
genes
[24].
In
Chlamydomonas
cells
g own
unde
blue
ligh ,
C CO
(Chlamydomonas
CO
homo-
log
[18

])
ansc ip
le els
a e
lowe ed
in
he
c c ya
mu an
[15],
sugges ing
a
possible
C CO
ac i a ion
by
C CRYa.
Besides,
UV-B
pe cep ion
and
signalling
in
Chlamydomo-
nas
is
media ed
by
C UVR8
ha
in e ac s
wi h
C COP1,
al hough
C HY5
implica ion
has
no
been
demons a ed
[14

].
RING- inge
E3
ligases
homologues
o
COP1
can
be
also
ound
in
o he
mic oalgae.
The e o e,
i
seems
ha
a
cen al
ole
o
COP1-like
signalling
mechanisms
was
al eady
es ablished
in
chlo ophy es
and
e ol ed
o
he
complexi y
ound
in
mode n
plan s.
Ci cadian
clocks
in
algae
and
plan s
Ci cadian
clocks
a e
molecula
mechanisms
ha
gene a e
hy hmic
o
oscilla ing
signals
wi h
a
pe iod
o
app oxi-
ma ely
24
hou s.
They
a e
ubiqui ous
sys ems
p esen
in
almos
all
euka yo ic
o ganisms,
bu
in
spi e
o
he
long
e olu iona y
dis ance
among
hem,
hey
a e
composed
o
s ikingly
simila
gene
ne wo ks
comp ising
in e wined
posi i e
and
nega i e
eedback
loops
[25].
These
genes
a e
no
always
o hologues,
sugges ing
a
con e gen
and
independen
e olu iona y
his o y.
Recen ly,
high
h oughpu
sequencing
and
genome-wide
phylogene ics
a e
s a ing
o
un eil
an
in e es ing
e olu ion
o
he
gene
ne wo k
unde pinning
he
ci cadian
clock
composi ion
in
he
g een
lineage.
Th ee
in e locked
eedback
loops
ha e
been
iden i ied
in
he
model
species
A abidopsis;
mo ning,
cen al
and
e en-
ing
loops
(Figu e
2a)
[26].
The
key
gene
in
he
mo ning
loop
is
CIRCADIAN
CLOCK-ASSOCIATED
1
(CCA1)
ha
codes
o
a
MYB
ansc ip ion
ac o
[27

]
wi h
a
con-
se ed
N- e minal
SHAQKYF
mo i
(Figu e
2b).
MYB
amily
has
gone
h ough
an
in ense
p ocess
o
ampli ica-
ion
and
unc ional
di e si ica ion
in
he
g een
lineage
[28]
and
CCA1
homologues
a e
p esen
in
e e y
plan
axa,
om
he
single
copy
gene
O CCA1
in
Os eococcus
[29

]
o
he
la ge
gene
amily
in
A abidopsis
including
CCA1,
LATE
ELONGATED
HYPOCOTYL
(LHY)
and
REV-
EILLE
(RVE)
4,
6
and
8
[30].
All
hese
homologues,
wi h
he
excep ion
o
Chlamydomonas,
exhibi
he
same
exp es-
sion
pa e n
as
A abidopsis
CCA1:
A
peak
a
dawn
and
a
ough
a
dusk
(Figu e
2c).
ChIP-seq
da a
has
shown
ha
CCA1
binds
di ec ly
o
he
p omo e s
o
he
o he
key
genes
in
he
mo ning
loop,
he
PSEUDO-RESPONSE
REGULATOR
9,
7
and
5
(PRR9/7/
5)
ecognizing
a
speci ic
DNA
sequence
called
e ening
elemen
[27

]
(Figu e
2a).
PRRs
a e
ep esso s
ha
con ain
in
hei
N- e minus
a
ecei e -like
domain
(RLD)
simila
o
he
one
in
RESPONSE
REGULATORS
in ol ed
in
he
His-Asp
phospho elay
sys em,
while
in
he
C- e mi-
nus
hey
p esen
a
CO,
COL1
and
TIME
OF
CAB
EXPRESSION
1
(TOC1)
domain
(CCT).
In
A abidopsis
Figu e
2
(a)
(b)
(c)
Mo ning Loop Cen al Loop E ening Loop
PRR 5/7/9 CCA1/LHY TOC1 ZTL GI LUX
RLD
RLD wi h DDK mo i
CCT
SHAQKYF Myb
LOV
Fbox
Kelch
GARP Myb
No malized Gene Exp ession
No malized Gene Exp ession
No malized Gene Exp essio
No malized Gene Exp essio
A abidopsis
haliana
Os eococcus
au i
Os eococcus
au i
Physcomi ella
pa en s
TOC1
PRR5
PRR7
PRR9
ZTO
ZT2
ZT4
ZT6
ZT8
ZT10
ZT12
ZT14
ZT16
ZT18
ZT20
ZT22
ZT24
ZTO
ZT2
ZT4
ZT6
ZT8
ZT10
ZT12
ZT14
ZT16
ZT18
ZT20
ZT22
ZT24
ZTO
ZT2
ZT4
ZT6
ZT8
ZT10
ZT12
ZT14
ZT16
ZT18
ZT20
ZT22
ZT24
ZTO
ZT2
ZT4
ZT6
ZT8
ZT10
ZT12
ZT14
ZT16
ZT18
ZT20
ZT22
ZT24
O CCA1
O TOC1
CCA1
A abidopsis
haliana
O yza sa i a
Picea abies
Selaginella
moellendo ii
Chlamydomonas
einha d ii
AT5G24470
AT2G46830
AT1G01060
AT5G61380
AT5G57360
AT2G18915
AT1G22770 AT3G46640
AT5G02810
AT2G46790
Os03g17570
Os08g06110 Os02g40510
Os02g05700
Os06g47890
Os01g08700
Os01g74020
Os11g05930
MA_71728g0010 MA_115536g0010 MA_71728g0010 MA_70291g0010MA_10427223g0010 MA_3352g0010
15421531 15422641 15415582 15403652 15410828
Pp3c16_18610
Pp3c3_37540 Pp3c16_18460
Pp3c15_13960
Pp3c4_2590 3
Pp3c25_4920
Pp3c25_5040
C e16.g676421
C e12.g514400
O 06g01320 O 13g01890 O 12g01470
C e02.g094150 C e10.g430750
Cu en Opinion in Plan Biology
E olu ion
o
ci cadian
clocks
om
algae
o
plan s.
(a)
T ansc ip ional
ne wo k
unde pinning
he
ci cadian
clock
in
A abidopsis
haliana
based
on
occupancy
p o iling
by
high
h oughpu
sequencing
o
ChIP-seq
o
CCA1,
TOC1,
PRR5,
PRR7
and
PRR9.
Th ee
di e en
loops
a e
iden i ied,
he
mo ning
loop
cons i u ed
by
CCA1
and
PRR9/7/5,
Howe e ,
he e
a e
di e se
and
speci ic
pho ope iodic
lowe ing
egula o y
s a egies.
In
he
sho
day
(SD)
plan
ice,
CO
homologue
unc ions
as
an
inhibi o
in
LD
and
ac i a o
in
SD
[45],
while
ano he
COL
sup-
p esses
lowe ing
ega dless
o
day
leng h
[46].
In
Med-
icago
and
pea,
CO
seems
o
ha e
no
signi ican
e ec
in
lowe ing
ime
and
speci ically
in
he
la e ,
FT
exp ession
is
con olled
solely
by
a
CDF
gene
[47,48].
None heless,
e olu ion
goes
e en
u he ,
al e ing
lowe ing
ime
a
he
species
le el
by
na u al
a ia ion
in
he
cis- egula o y
elemen s
o
he
CO
p omo e
[49

].
Mo eo e ,
a
local
adap a ion
o
eco ypes
o
di e en
lowe ing
s a egies
depending
on
hei
geog aphic
loca ion
has
been
desc ibed
[50].
These
examples
and
o he s
[51–54]
show
how
plan s
ha e
adap ed
o
op imize
hei
ep oduc i e
iming.
Al hough
he
belie
ha
CO
is
a
widesp ead
cen al
elemen
in
he
angiospe ms
lowe ing
pa hway
is
gene -
a ing
con o e sy
[47,55

],
he
GI-CDFs-CO-FT
co e
is
highly
conse ed
among
dis an ly
ela ed
lowe ing
plan s.
In
ac ,
i
has
been
shown
ha
COLs
and
DOFs
egula o s
ha e
coe ol ed
om
single
common
algal
ances o s,
ollowing
he
inno a ion,
ampli ica ion
and
di e gence
model
o
gene
e olu ion
by
duplica ion
[56].
C.
einha d ii
is
conside ed
o
be
he
ep esen a i e
species
o
his
common
ances o ,
in
which,
a
single
copy
gene
o
CO
(C CO)
ha
con ols
he
exp ession
o
a
single
copy
DOF
(C DOF)
has
been
cha ac e ized
[18

,57

].
C CO
is
a
cen al
hub
in ol ed
in
key
physiological
p ocesses
such
as
ca bon
me abolism
and
cell
cycle,
so
ha
i s
exp ession
is
con olled
by
pho ope iod
and
i s
mu a ion
se e ely
e ec s
he
capaci y
o
he
algae
o
syn hesize
s a ch
and
o
synch onize
cell
di ision
and
g ow h
[18

,56].
Fu he mo e,
C DOF
induces,
unlike
A abidopsis,
C CO
exp ession
in
SD
by
di ec
binding
o
i s
p omo e .
Howe e ,
in
LD,
i
ep esses
cell
cycle
p og ession
in
a
C CO-independen
way
[57

]
(Figu e
3).
Su p isingly,
bo h
genes
phenocopied
i s
homologue
unc ions
in
A abidopsis
when
ec opically
exp essed;
C CO
inducing
lowe ing
ime
while
C DOF
delays
i
[18

,57

].
Cu iously,
COL1
(which
sha es
80%
amino
acid
simila i y
wi h
CO)
o e exp ession
p oduces
no
change
in
lowe ing
ime
and
his
migh
e eal
ano he
e olu iona y
aspec :
I
mus
be
he
e ia y
s uc u e
o
he
algal
p o eins
wha
is
conse ed
and
ecognized
by
he
plan
egula o y
mechanisms
o
emula e
i s
plan
homologue
unc ion
[56].
This
does
no
seem
o
be
an
isola ed
e en
because
a
simila
case
was
obse ed
when
oma o
CDFs
we e
exp essed
in
A abidopsis
[58].
land
plan s,
al hough
he
h ee
domains
o
ZTL
ha e been
sepa a ely
iden i ied
in
di e en
p o eins
in
Physco-mi ella,
so
ha
hese
p o eins
could
o m
a
complex unc ionally
equi alen
o
ZTL
[33].
Al e na i ely,
a close
inspec ion
o
he
RLD
domains
in
he
PRR
genes in
Physcomi ella
and
Os eococcus
has
e ealed
a
po en ial phosphoacep o
DDK
mo i
ha
is
no
p esen
in
he
PRRs
o
land
plan s.
This
could
indica e
ha
hese
PRRs o m
pa
o
a
His -Asp
phospho elay
sys em.
In
ac , His idine
kinases
con aining
an
N- e minal
LOV
domain has
been
iden i ied
in
Os eococcus
whe e
i
has
been shown
o
espond
o
blue
ligh ,
bind
la in
and
ha e
a ci cadian
unc ion
[38].
The e o e,
hese
LOV-HKs
could possibly
ake
he
ole
o
ZTL
in
Physcomi ella,
Chlamy-
domonas
and
Os eococcus.
The
e ening
loop
includes
also
LUX
ARRHYTHMO, ELF3
and
ELF4
ha
ep ess
ci cadian
genes
nigh exp ession
[39].
LUX
homologs
ha e
been
ound
in
all plan
axa
examined
bu
no
unc ional
cha ac e iza ion
is desc ibed.
Po en ial
ELF3/4
o hologues
ha e
been
iden- i ied
in
Physcomi ella
[33]
and
o he
land
plan s
[40]
bu he e
seem
o
be
no
o hologues
in
Chlamydomonas
[41]
o
Os eococcus.
The e o e,
i
seems
ha
he
cen al
CCA1/LHY
and
TOC1
loop
was
es ablished
e y
ea ly
in mic oalgae
and
he
subsequen
loops
and
addi ional
con- ol
le els
ook
place
du ing
he
cou se
o
he
e olu ion
o land
plan s.
This
way,
he
mo e
complex
he
clock,
he mo e
esponses
can
be
ex ac ed
om
i
o
con ol
new physiological
p ocesses,
such
as
he
abo e
men ioned
empe a u e
compensa ion
exe ed
by
GI
[33].
This could
explain
how
land
plan s
acqui ed
a
much
mo e e sa ile
con ol
o
he
ex e nal
condi ions,
enhancing hei
plas ici y
and
capaci y
o
colonize
new
ae ial
niches.
E olu ion
o
he
pho ope iod
pa hway
The
long
day
(LD)
A.
haliana
plan
and
i s
pho ope iodic
con ol
o
lowe ing
ime
has
been
he
model
o
day leng h
sensing
s udies.
In
A abidopsis
CO
p o ein
ep e-sen s
a
cen al
hub
ha
con ols
lowe ing
in
he
p ope season
(Figu e
3,
igh ).
B ie ly,
CO
exp ession
is
egu-la ed
by
ci cadian
clock
and
pho ope iodic
inpu s
h ough GI-FKF1,
he
CDFs
and
FLOWERING
BHLHs (FBHs).
CO
p o ein
s abili y
is
con olled
by
pho o e-cep o s,
E3
ubiqui in
ligases
[42]
and
h ough
he
in e -ac ion
wi h
o he
p o eins
[43,44].
These
complex
egu-la o y
laye s
allow
he
co ec
exp ession
o
he
lo igen FLOWERING
LOCUS
T
(FT)
gene
ha
p omo es lowe ing.
(Figu e
2
Legend
Con inued)
he
cen al
loop
wi h
TOC1
and
CCA1
and
inally,
he
e ening
loop
o med
by
TOC1,
GI,
ZTL
and
LUX.
(b)
Iden i ica ion
o
o hologues
ci cadian
clock
p o eins
in
di e en
plan
axa
including
gene
ID
om
speci ic
da abases.
No ice
how
p o eins
in
he
mo ning
and
cen al
loops
a e
conse ed
ac oss
he
en i e
g een
lineage,
while
he
key
p o eins
in
he
e ening
loop,
ZTL
and
GI,
a e
only
p esen
om
Selaginella
on.
P o ein
domains
(RLD,
CCT,
Myb,
LOV,
Fbox
and
Kelch)
a e
colo -coded
iden i ied
on
he
able
on
he
le .
(c)
Conse a ion
o
he
exp ession
p o iles
o
CCA1,
PRR9/7/5
and
TOC1
om
A abidopsis
haliana
(le )
and
O CCA1
and
O TOC1
om
Os eococcus
au i
( igh )
in
24
hou s
expe imen s
a
12
hou s
ligh /12
hou s
da k
pho ope iod.
CCA1
and
O CCA1
p esen
simila
exp ession
p o iles
peaking
a
dawn
wi h
a
ough
a
dusk.
O TOC1
and
TOC1
exhibi
simila
exp ession
pa e ns
peaking
a
dusk
wi h
a
ough
a
dawn.

In
ascula
plan s,
a
g ea
numbe s
o
DOFs
and
COLs
unc ions
ha e
been
inhe i ed
om
hei
common
ances-
o .
Fo
example,
CO
igge s
s a ch
biosyn hesis
and
he
DOF
ansc ip ion
ac o
OBP1
con ols
cell
cycle
[59,60].
So,
no
only
DOF-CO
module
has
coe ol ed,
bu
also
a
se
o
genes
o
key
egula o y
ne wo ks
associa ed
o
hese
genes.
Addi ionally,
COLs
and
DOFs
ha e
acqui ed,
h oughou
e olu ion,
a
wide
epe oi e
o
plan -speci ic
ligh -dependen
unc ions
[5,61,62]
leading
o
mo e
com-
plex
o ganism
wi h
a
highe
pho ope iod
plas ici y.
Discussion
O e
e olu iona y
ime,
pho osyn he ic
o ganisms
ha e
lea n
o
li e
and
ex ac
in o ma ion
om
pe iodic
changes
in
sunligh
[1,2].
As
he
complexi y
o
o ganisms
inc eased,
so
did
hei
capaci y
o
espond
o
he
en i-
onmen
and
pa adoxically,
o
become
mo e
independen
om
i s
igou s
and
mo e
p ecise
a
aking
c ucial
li e
decisions,
such
as
he
bes
ime
o
he
yea
o
lowe
o
he
bes
ime
o
he
day
o
g ow.
The
massi e
amoun
o
in o ma ion
a ising
om
compa a i e
genomics
p ojec s
is
allowing
us
o
unde s and
pho ope iodic
sensing
wi h
an
e olu iona y
pe spec i e.
Acknowledgemen s
The
au ho s
would
like
o
hank
unding
om
p ojec s
BIO2011-28847-
C02-00
and
BIO2014-52425-P
(Spanish
Minis y
o
Economy
and
Compe i i eness,
MINECO)
pa ially
suppo ed
by
FEDER
unding.
Re e ences
and
ecommended
eading
Pape s
o
pa icula
in e es ,
published
wi hin
he
pe iod
o
e iew,
ha e
been
highligh ed
as:

o
special
in e es

o
ou s anding
in e es
1.
Lage c an z
U:
A
he
end
o
he
day:
a
common
molecula
mechanism
o
pho ope iod
esponses
in
plan s.
J.
Exp.
Bo .
2009,
60:2501-2515.
Figu e
3
Common
ances o
DOFs
SD
LD
Cell cycle
COLs Flowe ing
S a ch
byosin hesis
S a ch
byosin hesis
S em elonga ion
Bud Do mancy
Tube g ow h
Cell cycle
G ow h egula o
C:N me abolism
Lipid me abolism
Seed de elopemen
Lipid me abolism
Ni ogen me abolism
Response o ligh s imulus
...
...
...
C CO
FT
CO
PHYB
PHYA
FBHs
CDFs
HOS1
COP1
CRY2
C DOF
FBHCOP1HOS1
FT
GI
GI
FKF1
Cu en Opinion in Plan Biology
E olu ion
o
he
pho ope iod
pa hway
elemen s
om
a
common
ances o .
In
A abidopsis
( igh )
he
main
elemen s
o
lowe ing
pho ope iod
pa hway
a e
shown.
G ey
and
pu ple
p o eins
ep esen
phy oc omes
and
E3
ubiqui ine
ligase
p o eins,
espec i ely.
S aigh
and
dash
a ows
show
ansc ip ional
and
pos - ansc ip ional
egula ion,
espec i ely.
Colo ed
ci cles
ep esen
ligh
quali y.
In
Chlamydomonas
(le )
C CO
and
C DOF
a e
he
i s
known
elemen s
in ol ed
in
pho ope iodic
signaling
( he e
is
no
e idence
o
GI
and
FT
p o eins
p esence
in
g een
algae).
Al hough
HOS1,
COP1
and
FBHs
o hologues
a e
p esen
in
he
Chlamydomonas
genome,
no
unc ional
cha ac e iza ion
has
been
done.
The
big
amily
o
COLs
and
DOFs
in
angiospe ms
has
plan
speci ic
unc ions.
Howe e ,
o he
unc ions
a e
sha ed
wi h
he
Chlamydomonas
p o eins
(dash
lines).
2.
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MJ:
Pho ocon ol
o
de elopmen
in
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Annu.
Re .
Plan
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Plan
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A,
Li e ani
S,
Bou e
R
e
al.:
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o
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he
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Michael
TP,
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B e on
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egula o y
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O iz-Ma chena
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o
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Li
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Rizzini
L,
Fa o y
JJ,
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Li
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Toku su
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o
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o
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ed
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e n
mu an s
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o
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o
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A abidopsis
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o
CO
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in
o de
o
de e mine
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elucida e
pa
o
he
ansc ip-
ional
ne wo k
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o
he
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inding
ha
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si es
a e
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e
al.:
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he
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he
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o
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O CCA1
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unc ionally
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a
common
e olu iona y
o igin
o
ci cadian
clock
in
he
g een
lineage
ha
is
al eady
es ablished
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PY,
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imekeeping
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a
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e
al.:
A
G-Box-like
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is
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e
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Huang
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e
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o
he
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he
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o
he
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his
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he
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egulome
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o
he
ansc ip ional
ne wo k
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o
he
e ening
loop.
They
showed
ha
TOC1
ac s
as
a
ep esso .
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Miyazaki
Y,
Takase
T,
Kiyosue
T:
ZEITLUPE
posi i ely
egula es
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a
wa m
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e
al.:
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oles
o
FKF1,
GIGANTEA,
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ZEITLUPE
p o eins
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he
egula ion
o
CONSTANS
s abili y
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e
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o
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e
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euka yo ic
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a
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ole
o
he
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e
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om
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in e ac s
wi h
CONSTANS
o
ep ess
FLOWERING
LOCUS
T
ansc ip ion,
de ining
a
lowe ing
ime
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44.
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S aub
D,
Eguen
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U:
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ec ui men
o
CONSTANS
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a
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ime ic
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e
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a
majo
pho ope iod
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quan i a i e
ai
locus
in
ice,
is
closely
ela ed
o
he
A abidopsis
lowe ing
ime
gene
CONSTANS.
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46.
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P,
Wu
F,
Tan
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Zhang
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Ma
W:
A
CONSTANS-like
ansc ip ional
ac i a o ,
OsCOL13,
unc ions
as
a
nega i e
egula o
o
lowe ing
downs eam
o
OsphyB
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o
Ehd1
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e
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o
LATE
BLOOMER2
as
a
CYCLING
DOF
FACTOR
homolog
e eals
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di e gen
ea u es
o
he
lowe ing
esponse
o
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pea.
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Hech
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e
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o
CONSTANS-LIKE
genes
sugges s
ha
a
cen al
ole
o
CONSTANS
in
lowe ing
ime
con ol
is
no
e olu iona ily
conse ed
in
Medicago
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Rosas
U,
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e
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ime
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a ia ion
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o
he
ecen
o igin
o
CO
p omo e
polymo phism
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how
i s
na u al
a ia ion
egula es
lowe ing
ime
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di e en A abidopsis
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Vanhala
T,
No mann
KR,
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M
e
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ime
adap ion
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X
e
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o
ice
OsDo 12.
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52. Lee
Y,
An
G:
OsGI
con ols
lowe ing
ime
by
modula ing
hy hmic
lowe ing
ime
egula o s
p e e en ially
unde
sho
day
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Kloos e man
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MDMC
e
al.:
Na u ally
occu ing
allele
di e si y
allows
po a o
cul i a ion
in
no he n
la i udes.
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54.
Cao
D,
Li
Y,
Lu
S
e
al.:
GmCOL1a
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GmCOL1b
unc ion
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Simon
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Rı
¨l M,
De
Mon aigu
A,
Wo
¨ zel
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Coupland
G:
E olu ion
o
CONSTANS
egula ion
and
unc ion
a e
gene
duplica ion
p oduced
a
pho ope iodic
lowe ing
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he
B assicaceae.
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elegan
demons a ion
o
how
he
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o
a
co e
pho ope iodic
gene
has
a
deep
e ec
on
he
adap a ion
and
lowe ing
beha iou
o
a
whole
amily
o
plan s
and
he
possible
con e gence
o
his
unc ion
in
di e en
plan
lineages.
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Rome o-Campe o
FJ,
Lucas-Reina
E,
Said
FE,
Rome o
JM,
Val e de
F:
A
con ibu ion
o
he
s udy
o
plan
de elopmen
e olu ion
based
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gene
co-exp ession
ne wo ks.
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Lucas-Reina
E,
Rome o-Campe o
FJ,
Rome o
JM,
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F:
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e olu iona ily
conse ed
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plan
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unc ional
cha ac e iza ion
o
C DOF
in
algae
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plan s,
CO-DOF
module
is
shown
o
be
conse ed
h oughou
he
g een
linage
e olu ion.
58.
Co ales
A-R,
Nebaue
SG,
Ca illo
L
e
al.:
Cha ac e iza ion
o
oma o
Cycling
Do
Fac o s
e eals
conse ed
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new
unc ions
in
he
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o
lowe ing
ime
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e
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con ol
o
ca bon
dis ibu ion
du ing
he
lo al
ansi ion
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Radziejwoski
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Busch
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e
al.:
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ansc ip ion
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OBP1
is
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in
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cycle
egula ion
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he
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pho ope iodic
iming
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ole
o
he
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Zinc
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ansc ip ion
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amily
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