PERSPECTIVE ARTICLE
published: 23 Feb ua y 2015
doi: 10.3389/ pls.2015.00093
On ep oduc ion in ed algae: u he esea ch needed a
he molecula le el
Pila Ga cía-Jiménez and Ra ael R. Robaina*
Depa amen o de Biología, Uni e sidad de Las Palmas de G an Cana ia, Las Palmas de G an Cana ia, Spain
Edi ed by:
Elena M. K ame , Ha a d
Uni e si y, USA
Re iewed by:
Madelaine E. Ba le , Uni e si y o
Massachuse s Amhe s , USA
Yoji Nakamu a, Na ional Resea ch
Ins i u e o Fishe ies Science, Japan
*Co espondence:
Ra ael R. Robaina, Depa amen o
de Biología, Uni e sidad de Las
Palmas de G an Cana ia, 35017 Las
Palmas de G an Cana ia, Cana y
Islands, Spain
e-mail: [email p o ec ed]
Mul icellula ed algae (Rhodophy a) ha e some o he mos complex li e cycles known in
li ing o ganisms. Economically aluable seaweeds, such as phycocolloid p oduce s, ha e
a iphasic (game ophy e, ca pospo ophy e, and e aspo ophy e) li e cycle, no o men ion
he in ica e al e na ion o gene a ions in he edible “sushi-alga” no i. I is a well-known ac
ha ep oduc i e p ocesses a e con olled by one o mo e abio ic ac o (s), including day
leng h, ligh quali y, empe a u e, and nu ien s. Likewise, endogenous chemical ac o s
such as plan g ow h egula o s ha e been epo ed o a ec ep oduc i e e en s in some
ed seaweeds. S ill, in he genomic e a and gi en he high h oughpu echniques a
ou disposal, ou knowledge abou he endogenous molecula machine y lags a behind
ha o highe plan s. Any po en ial e ec i e con ol o he ep oduc i e p ocess will
en ail e isi ing mos o hese esul s and ac s o answe basic biological ques ions as
ye un esol ed. Recen esul s ha e shed ligh on he in ol emen o se e al genes in
ed alga ep oduc i e e en s. In addi ion, a wo king species cha ac e ized by a simple
ilamen ous a chi ec u e, easy cul i a ion, and accessible genomes may also acili a e ou
ask.
Keywo ds: Rhodophy a, seaweeds, ep oduc ion, ligh , ho mones, pho o ecep o s, signaling
RHODOPHYTA AND REPRODUCTION. MERGING APPLIED
AND FUNDAMENTAL KNOWLEDGE INTEREST
As ecen ly e iewed (Rebou s e al., 2014), he seaweed indus y
p oduces some 10 billion US$. Among he species exploi ed, he
ed seaweeds (Rhodophy a) Eucheuma/Kappaphycus,Po phy a,
and G acila ia occupy a leading posi ion (Kappaphycus alone
gene a es 1.3 billion US$ while he no i ma ke is es ima ed
a 1.5 billion US$). Ne e heless, his indus y mos ly elies
on he exploi a ion o na u al popula ions o p imi i e aqua-
cul u e me hods, i s expansion being es ic ed by he lack o
echnical and knowledge ad ances. An example o his can be
seen in he absence o con ol o ep oduc i e ai s ha would
allow us o inc ease p oduc ion, s ain selec ion and b eeding,
a majo s ep o wa d which has been achie ed in land plan
cul u e.
Rhodophy a a e classi ied as A chaeplas ida, along wi h glau-
cophy es and Vi idiplan ae (land plan s and g een algae) om
which hey di e ge 1,500 Mya (Yoon e al., 2004). Like o he
algal g oups, ed algae comp ise a my iad o species wi h di -
e en ypes o body a chi ec u e, anging om he unicellula
and ilamen ous o he blade o pseudo-pa enchyma ous as he
mos complex, pa icula ly in he case o indus ially aluable
seaweeds (Cole and Shea h, 1995). Thei ex emely complex li e
cycles include he ansi ion om unicellula i y o complex mul-
icellula bodies, he unde lying molecula bases o which a e
i ually unknown. The diploid “conchocelis” and he meio ic-
de i ed conchospo es sus ain he indus y o “sushi,” since he
iny unicellula meiospo e, he conchospo e, g ows and de elops
in o he haploid lea y hallus, which is he edible phase (D ew,
1949, 1954).
O he economically aluable ed algae, such as he p oduce s
o he phycocolloids aga o ca ageen, ha e a igene ic li e cycle
in which he haploid unicellula meio ic e aspo es ge mina e
o p oduce bo h a male and a emale mul icellula game o-
phy e halli (Cole and Shea h, 1995). Fe iliza ion occu s when
a spe ma ium e ilizes a ca pogonium on he emale game o-
phy e. The e ilized ca pogonium de elops in o a s uc u e called
he cys oca p (diploid) a e complex cell di e en ia ion e en s,
leading o he accumula ion o mi o ic diploid ca pospo es.
E en ually, diploid ca pospo es a e eleased and de elop
in o e aspo ophy es ha p oduce he meio ic e aspo es
(Figu e 1).
Recen e iews con inue o ocus on a ple ho a o ex e nal
ac o s ha con ol algal ep oduc ion such as ligh (in ensi y,
quali y, pho ope iod), empe a u e, season, nu ien s (be hey
ino ganic o o ganic), bio ic ac o s (ex acellula algal p od-
uc s, bac e ial associa ion, animal g azing), osmo ic s ess, pH
o he medium, wa e mo ion and mechanical shock, pollu ion,
and adia ions, and he bulk o knowledge accumula ed as o
he pa icula condi ions on which hese ex e nal ac o s exe
hei con ol (D ing, 1988; Bo ne e and Puijalon, 2011; Ag awal,
2012).
Ligh and empe a u e a e managed e ec i ely o un he
in ensi e cul i a ion sys em o Po phy a, bu he e is a gene al
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Ga cía-Jiménez and Robaina Molecula esea ch and ed mac oalgal ep oduc ion
FIGURE 1 | (A) Apical po ion o a spo ophy e b anch o Bonnemaisonia
hami e a, scale ba =120 µm. (B) Pu a i e game ophy e spo eling, scale
ba =25 µm. (C) Apex o a imma u e game ophy ic halli, scale
ba =100 µm. (D) Diag am o pu a i e igene ic li e cycle in he ed alga
Bonnemaisonia comp ising he game ophy es (haploids), he so-called
ca pospo ophy e ha de elops on he emale game ophy e a e e iliza ion,
and he spo ophy e (diploid) (adap ed om B. genicula a in She lin and
Polanshek, 1978. No a scale).
consensus ha inc easing ou knowledge o he unde lying
molecula basis o cell g ow h, de elopmen and ep oduc ion in
his species, and in economical impo an seaweeds in gene al,
will imp o e aquacul u e p ac ices (Sahoo e al., 2002; Nakamu a
e al., 2013).
As we will see below, he same si ua ion occu s when he
e ec o plan ho mones on seaweed ep oduc ion is consid-
e ed, al hough some ad ances a he molecula le el ha e been
made on he in ol emen o ce ain genes. Almos no hing is
known abou how he ex e nal signals a e ansla ed in o he
molecula mechanisms known o unde lie any de elopmen al o
ep oduc i e e en comp ising cell g ow h and di e en ia ion.
Whils his ask was add essed o land plan s some ime ago,
in he genomic e a and gi en he high h oughpu echniques
a ou disposal, ou knowledge ega ding algae in gene al, and
seaweeds in pa icula , lags a behind ha o highe plan s and
animals. Le us he e o e e iew wha is al eady known abou
plan s and should be e isi ed in ed algae o un eil he sec e s o
wha , no doub , is also ope a ing a he molecula le el o con ol
ep oduc ion.
REPRODUCTION GENES IN RED ALGAE. DISPARATE MODEL
SPECIES AND APPROACHES
As seen in he mos ecen bibliog aphic epo s, and is e iden in
his special edi ion, majo ad ances a e aking place in he b own
alga since he adop ion o Ec oca pus siliculosus as he model
species and he gene alized use o high h oughpu echniques.
This includes key genes in he li e cycle ansi ion, de elopmen al
pa e n, e c. (Pe e s e al., 2004; Cock e al., 2010; Coelho e al.,
2011; Le Bail e al., 2011; A un e al., 2013). I E. siliculosus
was chosen mainly because o he pa icula axonomic posi ion
o b own algae and he e olu iona y lineage- ela ed in o ma ion
ha could be e ie ed om i (Pe e s e al., 2004), in ed algae, no
gene al consensus has been eached as o ei he he model species
o echnical app oaches and s a egies. Consequen ly, limi ed
ad ances ha e been achie ed o da e, pa icula ly ega ding he
ep oduc i e e en .
Po phy a species (Rhodophy a, Bangiophyceae)—o a he
Po phy a/Py opia species, as se e al species has been eassigned
as Py opia (Su he land e al., 2011)—ha e been p oposed as
model species, pe haps because o hei economic alue. The
genome and symbion - ee genome ha e been sequenced (Chan
e al., 2012; Nakamu a e al., 2013), and 1% o he genes
(10,327 o al genes p edic ed) we e anno a ed as ela ed o ep o-
duc ion in P. yezoensis, using he es ima ion p o ided by GO
Slim in he Blas 2Go so wa e (Nakamu a e al., 2013). The e-
o e, his genomic app oach always aces a se ious cons ain ,
since hese genes a e commonly assigned o pu a i e biologi-
cal p ocesses and unc ions based on he in o ma ion a ailable
o o he o ganisms, ha may simply lack genes and unc ions
ela ed o impo an li e cycle o ep oduc ion e en s in ed
algae.
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Ga cía-Jiménez and Robaina Molecula esea ch and ed mac oalgal ep oduc ion
Table 1 | An o e iew o he complex ligh sensing–plan ho mones in e ac ion, highligh ing he key molecula ac o s implica ed.
Phy och ome C yp och ome Pho o opins
Abscisic acid BBX2, HY51BBX2, HY51BBX2, HY51
PIF1/PIL52MYC2?3® MYC2?3®
CIB4,5®
E hylene PIF3, ERF16E hylene syn hesis inhibi o ?7
PIF5, DELLA?7
Auxins PAR, HFR1, PIL17PKS, 14-3-3 l, PIN, PGP, AUX/LAX8
Gibbe ellins DAG, PIF3, PIF4, PIF1/PIL5 COP1, HY52
Cy okinins COP1, HY52
Jasmonic acid MYC2?3
B assinos e oids PIF4, BZR19
All o he in o ma ion comes om highe plan s, mos ly A abidopsis haliana. P ominen ole a e played by ansc ip ion ac o s (TF) and p o eins able o in e ac wi h
hem. PIF a e a amily o bHLH TF able o bind di ec ly o G-BOX in DNA; HY5 is a nuclea cons i u i e TF; BZR1 is a TF able o bind o PIF4 du ing b assinos e oids
e ec on pho omo phogenesis; CIB is a bHLH TF ha speci ically con ols Flowe ing Time locus; MYC2 is a bHLH TF in A abidopsis; DELLA a e p o eins ha
in e ac s wi h PIF; COP1 is a ing inge ubiqui in ha p omo es HY5 deg ada ion; HFR1 is a p o ein able o in e ac wi h PIF o BBX2, a zinc inge s p o eins able
o ep ess o modula e he ac ion o ansc ip ion ac o s. The emaining ac o s a e mo e speci ic o he plan ho mones o he pho o ecep o signaling pa hways.
®Deno es pa icipa ion in ep oduc i e e en s (i.e., lowe ing). De ails on how hey in e ac can be ound in he o iginal e e ences (1Xu e al., 2014;2Lau and Deng,
2010;3Gup a e al., 2012;4Liu e al., 2013;5Fe nando and Coupland, 2012;6Zhong e al., 2012;7Alabadí and Blázquez, 2009;8Hohm e al., 2013;9Jaillais and G égo y,
2012). ? Deno es pending con i ma ion.
The same wide genome app oach has ecen ly been used o
epo he genome and gene anno a ion o he edible ca ageeno-
phy e alga Chond us c ispus, he I ish moss (Collén e al., 2013).
An impo an scien i ic backg ound o knowledge exis s o C.
c ispus, o he ex en ha i has been p oposed as he model
ed alga (Collén e al., 2014). The 9,606 genes anno a ed o
C. c ispus ha e p oduced a e y use ul bulk o in o ma ion o
he in e p e a ion o he o ces d i ing he e olu ion o euka y-
o ic genomes (Collén e al., 2013). In e es ingly, C. c ispus has
c yp och omes (Collén e al., 2013), which a e impo an in
pho osensing and he egula ion o he ep oduc ion by ligh and
ho mones, as discussed below (Table 1). The phases o he li e
cycle o C. c ispus a e easily accessible and hus equen ly used
o expe imen s, bu hey migh be no so easy o handle i he
comple ion o he li e cycle is equi ed, as is he case o ep oduc-
ion s udies, o which mu an s a e equi ed. Mo eo e , he e is an
appa en absence o sho age o well-known key elemen s in he
egula o y ne wo k (i.e., absence o phy och omes, pho o opins,
and a a he small amoun o ansc ip ion-associa ed p o eins).
The e o e, he u ili y o C. c ispus as a model species o he s udy
o ce ain aspec s o algal g ow h and de elopmen du ing li e
cycle comple ion (i.e., ligh con ol o ep oduc ion) emains a
ma e o deba e.
Analysis o he ansc ip omes has e ealed p e e en ial genes
exp essed in game ophy es o spo ophy es. In Po phy a pu pu ea,
an unusual elonga ion ac o (EF-1a) was exp essed only in
he spo ophy e while a second gene, EF, was exp essed equally
in he spo ophy e and he game ophy e (Liu e al., 1996).
The PyKPA1 gene, which encoded a sodium pump, was di -
e en ially exp essed in he game ophy e as compa ed o he
spo ophy e, which seems o depend on he p esence o speci ic
p omo e elemen s (Uji e al., 2012, 2013). Apa om Po -
phy a/Py opia, o he species also conside ed o be o economic
in e es , such as he aga ophy ic species, ha e been s udied.
In his ega d, ca pospo ophy e-speci ic genes we e iden i ied
in G acila iopsis ande sonii (Kamiya e al., 2011). In G acila ia
lemanei o mis, a emale game ophy e-speci ic gene, GMF-01, has
been epo ed (Chen e al., 2011) while an ubiqui in gene
was also cha ac e ized as pa icula ly ac i e du ing he ca -
pospo ophy e o ma ion (Ren e al., 2009). In G i i hsia japonica,
he GjFP-1 gene, encoding a hea -shock p o ein 90, may be
in ol ed in he di e en ia ion o emale game ophy e (Lee e al.,
1998).
O he app oaches ha e made i possible o each candida e
gene(s) in ol ed in ep oduc ion. This is he case o he GiODC
gene in G a eloupia imb ica a, which encodes he o ni hine deca -
boxylase (ODC, EC. 4.1.1.17). The ODC s a s he syn hesis o
he common polyamines pu escine, spe midine, and spe mine
by deca boxyla ing he o ni hine o p oduce pu escine; hese
subs ances a ec spo e ma u a ion and libe a ion as desc ibed
below (Ga cía-Jiménez e al., 1998; Ma ián e al., 2000; Guzman-
U iós egui e al., 2002, 2012; Sac amen o e al., 2004, 2007).
GiODC was cloned using a somewha labo ious app oach by
means o degene a ed p ime s designed om conse ed p o ein
mo i s, ollowed by ch omosome walking by iPCR o comple e
he sequence (Ga cía-Jiménez e al., 2009). GiODC exp ession
a ied acco ding o cys oca p di e en ia ion wi h lowe le els in
he e ile, as compa ed o he in e ile, issue (Ga cía-Jiménez
e al., 2009).
All o hese indings a e clea ly con ibu ing o ou knowledge
abou ep oduc ion in ed seaweeds, whe he achie ed h ough a
wide genome s a egy using high h oughpu me hods as done
in Po phy a/Py opia o Chond us, o using a candida e gene
app oach as in he case o ODC in G a eloupia imb ica a. Ne -
e heless, he weakes poin s ill emains on how his—pe haps
species-speci ic—in o ma ion can be ansla ed in o da a ha is
ele an o mos ed seaweeds; how o cons uc a eliable “ ed
seaweed concep ual amewo k” o knowledge on ep oduc ion
om hese dispa a e app oaches and species s a egies. F om ou
poin o iew his could only be s a ed o achie e using a species
ha is easy o handle, wi h ela i ely sho gene a ion imes, and
ul ills he c i e ia needed o unde go gene ic ans o ma ion,
www. on ie sin.o g Feb ua y 2015 | Volume 6 | A icle 93 |3
Ga cía-Jiménez and Robaina Molecula esea ch and ed mac oalgal ep oduc ion
which cons i u es he cu en bo leneck in he molecula biology
o seaweeds (see Mikami, 2014).
LIGHT AND PLANT HORMONES SIGNALING AND
INTERACTION. THE WAY TO UNVEIL THE MOLECULAR
SECRETS OF RED ALGAL REPRODUCTION?
In pho osyn he ic euka yo es, like algae, ligh is he d i ing
o ce o g ow h and de elopmen ; i is he sou ce o ene gy,
bu also he signal igge ing bo h ege a i e and ep oduc-
i e de elopmen al e en s. Ligh is pe cei ed h ough amilies
o pho o ecep o s: phy och omes ( ed/ a ed adia ion), UVR8
(UV-B), and memb ane associa ed pho o opins, c yp och omes,
and he membe s o he ZTL/FKF1/LKP2 amily which abso b
UV-A/blue ligh (Hohm e al., 2013 and e e ences he ein). In
u n, he exis ence and he ype o pho o ecep o s in aqua ic
o ganisms ha e a ac ed scien i ic a en ion, due o he pecu-
lia cha ac e is ics o he in e ac ion o ligh in he aqua ic
en i onmen . Thus, he p esence o di e se genuine pho o e-
cep o s, such as pho o opins, au och omes (blue abso bing),
neoch omes—a kind o chime ic phy och ome, c yp och omes,
and phy och omes in ma ine algae has been epo ed and
e iews ha e been p oduced, which include u u e applied dimen-
sions (Kianianmomeni and Hallmann, 2014). In e es ingly, as
a as signal ansduc ion is conce ned, he pho o opin mech-
anism seems o be conse ed be ween algae and highe plan
(Huang e al., 2002; Onode a e al., 2005; P ochnik e al.,
2010).
In seaweeds, plan ho mones ha e been epo ed o a ec
g ow h and de elopmen (Chan e al., 2006; Baweja e al., 2009).
Conce ning ep oduc ion e en s, in G a eloupia imb ica a (as G.
do ypho a), he le els o he polyamines pu escine, spe midine,
and spe mine changed as he cys oca ps ma u a e. Subsequen ly,
i was obse ed ha hese polyamines, pa icula ly spe mine,
a o ed he ma u a ion, libe a ion, and g ow h o ca pospo es
in G a eloupia imb ica a and Hyd opun ia co nea (as G acila ia
co nea;Ga cía-Jiménez e al., 1998; Ma ián e al., 2000; Guzman-
U iós egui e al., 2002, 2012; Sac amen o e al., 2004, 2007). In
addi ion, e hylene has been epo ed o accele a e he ma u a ion
o e aspo angia in P e ocladiella capillacea (Ga cía-Jiménez and
Robaina, 2012)
In ecen yea s ex ensi e knowledge has been accumula ed
abou ligh , pho o ecep o s and plan ho mone in e ac ion, and
c oss alk a he molecula le el in highe plan s, pa icula ly du -
ing he e en s occu ing a wo physiological scena ios: seedling
pho omo phogenesis and shade a oidance (Gyula e al., 2003;
Lau and Deng, 2010). T ansc ip ion ac o s o se e al amilies,
p o ein–p o ein in e ac ion, as well as pos - ansla ional p o-
ein modi ica ion a e in ol ed (Alabadí and Blázquez, 2009;
Lau and Deng, 2010; Fe nando and Coupland, 2012; Gup a
e al., 2012; Jaillais and G égo y, 2012; Zhong e al., 2012;
Liu e al., 2013). Table 1 p o ides an o e iew o he complex
sys em ope a ing in he ligh –pho o ecep o s–plan ho mones
in eg a ed ne wo k. All o his impo an in o ma ion has so
a p o ed o be ele an o highe plan s, pa icula ly o he
model species A abidopsis haliana, and i is comple ely unknown
whe he he key elemen s highligh ed also ope a e in seaweeds,
despi e he ac ha he in luence o pho o ecep o s and plan
ho mones on ep oduc ion has been epo ed, as p e iously
men ioned.
T ansc ip ion ac o s con olled by pho o ecep o s, such as he
PIF amily (Alabadí and Blázquez, 2009; Lau and Deng, 2010;
Jaillais and G égo y, 2012; Zhong e al., 2012), along wi h o he s
unde he con ol o plan ho mones, such as HY5 (Lau and Deng,
2010; Xu e al., 2014), a e e y impo an playe s in he in eg a ed
ne wo k (Table 1). O he ac o s a ec ing plan g ow h and de el-
opmen , like ci cadian clock senso s ha con ol endogenous
le els o plan ho mones (i.e., auxin), o empe a u e also seem
o ac by modula ing he ac i i y o PIF ansc ip ion ac o s, hus
connec ing impo an abio ic ac o s and de elopmen (Lei a
and Quail, 2011).
Finally, by way o u u e pe spec i e, in ou labo a o y we ha e
ecen ly adop ed Bonnemaisonia hami e a (Bonnemaisoniaceae)
as a wo king species. Cul u es o he spo ophy e (T ailliella) phase
ha e been es ablished so a , and wo k is p og essing owa d
he induc ion o he di e en ia ion o game ophy es, using em-
pe a u e and pho ope iod, and plan ho mones (Figu es 1A–C).
Should he comple ion o he li e cycle may be accomplished in
he nex u u e as a basic equi emen o a wo king species, i
emains o ind an app op ia e genomic s uc u e (a compac o
simple genome, a small numbe o genes, impo an unc ional
ansc ip omic in o ma ion, e c.), bu he e is li le in o ma ion
on he B. hami e a genome so a . Ne e heless, e en in he long
un, wi h B. hami e a o any o he simila and mo e adequa e
species, i is ime o e isi his scena io in seaweeds bu ocusing
on he molecula s andpoin ; why no s a iden i ying wi hin
he ising genomic/ ansc ip omic da a o all o any o hese
egula ing ac o s shown in Table 1?
ACKNOWLEDGMENT
The au ho s wan o hank he suppo ob ained om he Spanish
Minis e io de Economía y Compe i i idad (Plan Nacional, g an s
# BFU2003-01244; 2006-06918; 2010-17248).
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Con lic o In e es S a emen : The au ho s decla e ha he esea ch was con-
duc ed in he absence o any comme cial o inancial ela ionships ha could be
cons ued as a po en ial con lic o in e es .
Recei ed: 10 No embe 2014; accep ed: 04 Feb ua y 2015; published online: 23
Feb ua y 2015.
Ci a ion: Ga cía-Jiménez P and Robaina RR (2015) On ep oduc ion in ed
algae: u he esea ch needed a he molecula le el. F on . Plan Sci. 6:93. doi:
10.3389/ pls.2015.00093
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