F on ie s in Plan Science | www. on ie sin.o g 1 Ma ch 2019 | Volume 10 | A icle 281
REVIEW
published: 20 Ma ch 2019
doi: 10.3389/ pls.2019.00281
Edi ed by:
Lam-Son T an,
RIKEN, Japan
Re iewed by:
Manuel Nie es-Co dones,
Cen e o Edaphology and
Applied Biology o Segu a,
Spanish Na ional Resea ch
Council (CSIC), Spain
Fe nando Aleman,
The Sc ipps Resea ch Ins i u e,
Uni edS a es
*Co espondence:
José M. Pa do
[email p o ec ed]
Special y sec ion:
This a icle was submi ed o
Plan Abio ic S ess,
a sec ion o he jou nal
F on ie s in Plan Science
Recei ed: 07 Decembe 2018
Accep ed: 20 Feb ua y 2019
Published: 20 Ma ch 2019
Ci a ion:
Ragel P, Radda z N, Leidi EO,
Quin e o FJ and Pa do JM (2019)
Regula ion o K+ Nu i ion in Plan s.
F on . Plan Sci. 10:281.
doi: 10.3389/ pls.2019.00281
Regula ion o K+ Nu i ion in Plan s
PaulaRagel1,2, Na aliaRadda z1, Edua doO.Leidi3, F anciscoJ.Quin e o1 and
JoséM.Pa do1*
1 Ins i u o de Bioquímica Vege al y Fo osín esis, Consejo Supe io de In es igaciones Cien í icas y Uni e sidad de Se illa,
Se ille, Spain, 2 Cen e o O ganismal S udies, Uni e si ä Heidelbe g, Heidelbe g, Ge many, 3 Ins i u o de Recu sos
Na u ales y Ag obiologia de Se illa, Consejo Supe io de In es igaciones Cien i icas, Se ille, Spain
Mode n ag icul u e elies on mine al e iliza ion. Unlike o he majo mac onu ien s,
po assium (K+) is no inco po a ed in o o ganic ma e bu emains as soluble ion in he
cell sap con ibu ing up o 10% o he d y o ganic ma e . Consequen ly, K+ cons i u es
a chie osmo icum o d i e cellula expansion and o gan mo emen s, such as s oma a
ape u e. Mo eo e , K+ anspo is c i ical o he con ol o cy oplasmic and luminal pH
in endosomes, egula ion o memb ane po en ial, and enzyme ac i i y. No su p isingly,
plan s ha e e ol ed a la ge ensemble o K+ anspo e s wi h de ined unc ions in nu ien
up ake by oo s, s o age in acuoles, and ion ansloca ion be ween issues and o gans.
This e iew desc ibes c i ical anspo p o eins go e ning K+ nu i ion, hei egula ion,
and coo dina ed ac i i y, and summa izes ou cu en unde s anding o signaling pa hways
ac i a ed by K+ s a a ion.
Keywo ds: plan nu i ion, po assium, ni a e, egula ion, long-dis ance anspo
INTRODUCTION
Po assium (K+) is o pa amoun impo ance in plan cell physiology. K+ is an essen ial
mac onu ien ha ul ills c i ical unc ions ela ed o enzyme ac i a ion, osmo ic adjus men ,
u go gene a ion, cell expansion, egula ion o memb ane elec ic po en ial, and pH homeos asis
(Hawkes o d e  al., 2012). While he K+ concen a ion in he soil solu ion may a y widely
om 0.01 o 20 mM, plan cells main ain a ela i ely cons an concen a ion o 80–100 mM
in he cy oplasm (Rod iguez-Na a o, 2000). Mo eo e , plan s accumula e la ge amoun s o
K+ in hei acuoles, su passing pu ely nu i ional equi emen s. Hence, K+ is he mos abundan
ca ion in plan cells, comp ising up o 10% o plan d y weigh and o en exceeding he ca.
2% ha suppo s nea -maximal g ow h a es (Whi e and Ka ley, 2010). The e is a s eep
cu ilinea ela ionship be ween he issue concen a ion o K+ and plan g ow h, om which
a c i ical concen a ion o K+ suppo ing 90% o maximum yield can be de e mined. Abo e
his concen a ion, g ow h has no co ela ion wi h he inc eased K+ con en , bu a lowe K+
concen a ions, g ow h declines apidly. Consequen ly, K+ e iliza ion is common p ac ice in
mode n ag icul u e and abou 40–60% o c op yields a e a ibu able o comme cial e ilize
use (S ewa e  al., 2005). Howe e , ag icul u al e iliza ion is a om being ine- uned wi h
nu i ional equi emen s.
K+ is aken up om he soil solu ion by oo epide mal and co ical cells. Once K+ is
inside he oo symplas , i may be s o ed in acuoles, whe e i ul ills osmo ic unc ions, o
is anspo ed o he shoo ia xylem (Pa do and Rubio, 2011). In u n, shoo cells may also
supply s o ed K+ o edis ibu ion ia phloem. In his ansi om he soil o he di e en
Ragel e al. Regula ion o K+ Nu i ion in Plan s
F on ie s in Plan Science | www. on ie sin.o g 2 Ma ch 2019 | Volume 10 | A icle 281
plan o gans, K+ c osses a ious cell memb anes h ough K+-
speci ic anspo sys ems (Figu e 1). Coo dina ed ope a ion
o he di e en anspo sys ems wi hin he plan o secu e
K+ up ake om he soil and deli e y o he di e en plan
o gans equi es complex K+ sensing and signaling mechanisms.
Because o he ex ao dina y di e si y o K+ anspo e s in
plan cells and he physiological and de elopmen al p ocesses
in which hey a e in ol ed, his e iew is ocused on he
molecula mechanisms media ing K+ up ake and elease a he
plasma memb ane le el, wi h an emphasis on K+ abso p ion
om he soil and dis ibu ion h oughou he plan due o
he ele ance o hese p ocesses in plan nu i ion. S o age o
K+ in o acuoles is ea ed only b ie ly and eade s a e e e ed
o o he comp ehensi e e iews desc ibing anspo sys ems
ope a ing a he onoplas (Ma inoia e  al., 2012; Ahmad and
Maa huis, 2014; Eisenach and De Angeli, 2017; Ma inoia,
2018). Las , because o he ex ensi e in e ac ions o ni ogen
and K+ in plan mine al nu i ion, wesumma ize he coo dina ed
egula ion o NO3− and K+ up ake and long-dis ance anspo
in A abidopsis.
Up ake and dis ibu ion o K+ in plan cells is ca ied ou
by a a ie y o anspo e p o eins ca ego ized in o se e al
amilies wi h a ied s uc u es and anspo mechanisms ha
comp ise he channel amilies Shake -like ol age-dependen ,
he andem-po e (TPK), and he wo-po e channels (TPC)
(Hed ich, 2012), he ca ie -like amilies KT/HAK/KUP (Nie es-
Co dones e  al., 2014a; Li e  al., 2018), HKT unipo e s and
sympo e s (Hamamo o e al., 2015), and ca ion-p o on an ipo e s
(CPA). The CPA amily is he la ges one and includes he
NHX, CHX, and KEA an ipo e s (Sze and Chan oj, 2018).
In his e iew, we desc ibe he s uc u e and di e si y o he
main K+ anspo e amilies whose membe s con ibu e
subs an ially o K+ nu i ion. O he p o eins wi h unce ain
oles o desc ip ions o anspo ac i i ies wi hou candida e
p o eins ha e been omi ed.
TRANSPORT PROTEIN FAMILIES
INVOLVED IN K+ NUTRITION
K+-Selec i e Channels
The i s K+ anspo e wi h a ole in nu ien up ake was
he Shake -like, ol age-ga ed, and K+-selec i e channel AKT1
(Hi sch e  al., 1998). Al hough ol age-ga ed (VG) channels
o plan s a e phylogene ically ela ed o animal Shake channels,
hey a e dis inc and include addi ional unc ional domains
(Jegla e  al., 2018). The basic a chi ec u e o VG channels
consis s o ou α-subuni s su ounding a cen al aqueous po e
o K+ pe mea ion. Each subuni con ains six ansmemb ane
segmen s, named S1–S6, which can bedi ided in o wo di e en
modules: he i s ou α-helices o m a ol age-senso domain
ha con ains mul iple posi i ely cha ged esidues ha mo es
wi hin he memb ane in esponse o ol age. This mo emen
is di ec ly coupled o he opening o closing o he channel.
The segmen s S5, S6, and he po e loop, o m he po e domain,
named P, whe e each o he ou subuni s con ibu es equally
o he pe mea ion pa hway. Mo eo e , plan α-subuni s ha e
a long C- e minal egion cons i u ing mo e han hal o he
p o ein (Figu e 2). This cy osolic ail includes se e al unc ional
domains: (1) a linke egion (C-linke ) p oximal o he po e
FIGURE 1 | T anspo e s in ol ed in K+ up ake by oo s and in e -o gan pa i ion. HAK5, AKT1, and non-selec i e cyclic nucleo ide-ga ed ca ion channels (CNGC)
all con ibu e o K+ nu i ion, albei a di e en anges o subs a e concen a ions, om low- o high-a ailabili y, espec i ely. K+ e lux h ough he
ou wa d- ec i ying GORK channel acili a es he ine- uning o plasma memb ane elec ical po en ial, and allows epola iza ion unde ci cums ances ha p omo e
depola iza ion, such as salini y s ess. In he oo s ele, he ou wa d- ec i ying SKOR channel eleases K+ in o he xylem essels o nu ien deli e y o he shoo s.
The ni a e anspo e NRT1.5 acili a es K+ uploading in o he xylem ei he by elec ical coupling wi h o he K+-selec i e anspo e s o di ec ly ac ing as
K+/H+ an ipo e . In ae ial issues, an a ay o K+-in lux channels and KT/HAK/KUP ca ie s allow he up ake o he incoming K+ in o g een cells. K+ is s o ed inside
acuoles by NHX exchange s and eleased back o he cy osol by TPK and TPC1 channels, and possibly also by KT/HAK/KUP ca ie s a he onoplas
( he acuole in oo cells is omi ed o simplici y). The plasma memb ane ou wa d K+ channel AKT2 eleases K+ in o he phloem o e u ning K+ o he oo and o
acili a e he uploading o pho osyn ha es in o he phloem sap.
Ragel e al. Regula ion o K+ Nu i ion in Plan s
F on ie s in Plan Science | www. on ie sin.o g 3 Ma ch 2019 | Volume 10 | A icle 281
ha ansduces con o ma ional changes ha ga e he channel
and ha may also de e mine he a ge memb ane (Nie es-
Co dones e  al., 2014b; Jegla e  al., 2018); (2) a conse ed
and essen ial cyclic nucleo ide-binding homology domain
(CNBHD) whose unc ion is no he binding o cNMP bu
o media e he in e ac ions be ween subuni s wi hin he channel
e ame ; (3) an anky in domain ( ound in only six ou o
he nine A abidopsis VG channels), which may media e he
binding o in e ac ing p o eins (Michaely and Benne , 1992);
and (4) a dis al KT/KHA domain ich in hyd ophobic and
acidic esidues, ha is unique o plan K+ channels, and is
in ol ed in channel e ame iza ion and clus e ing a he
memb ane (Da am e  al., 1997; Eh ha d e  al., 1997;
Zimme mann e  al., 2001; D eye e  al., 2004).
Plan ol age-ga ed K+ channels a e di ided in o h ee
sub amilies ega ding hei esponse o he memb ane po en ial
(D eye and Uozumi, 2011): (1) Inwa d- ec i ying (Kin) channels
ha in A abidopsis include AKT1, AKT6, KAT1, and KAT2;
hey open a hype pola ized memb ane po en ials allowing he
up ake o K+. (2) Ou wa d- ec i ying (Kou ) channels ha
media e K+ elease because hey open a depola ized memb ane
po en ials; his g oup is composed o SKOR and GORK channels.
(3) Weakly ec i ying (Kweak) channels ha can media e bo h
K+ up ake and elease, and whose A abidopsis ep esen a i e
is AKT2. In addi ion, he A abidopsis KC1 (KAT3) is an
elec ically silen Shake -like p o ein ha in e ac s wi h and
egula es unc ionali y o he Kin channels AKT1, KAT1, KAT2,
and AKT2, bu no he Kou channels (Jeanguenin e al., 2011).
This in e ac ion nega i ely shi s he ac i a ion h eshold o
Kin channels and dec eases he mac oscopic inwa d conduc ance
compa ed o ha o homome ic channels (D eye e al., 1997;
Duby e  al., 2008; Geige e  al., 2009). He e ome iza ion o
di e en subuni s o Kin channels is o g ea impo ance o
inc ease he unc ional di e si y and egula ion o di e en
cell ypes (D eye e al., 1997; Vé y and Sen enac, 2003; Xicluna
e  al., 2007; Jeanguenin e  al., 2008; Lebaudy e  al., 2008;
Lebaudy e  al., 2010). Al hough his beha io has also been
sugges ed o ou wa d- ec i ie (Kou ) channels, he e ome iza ion
has been epo ed only among subuni s o Kin o Kou ,
p e en ing o ma ion o he e ome ic s uc u es be ween he
wo subuni ypes (D eye e  al., 2004).
K+-Up ake Ca ie s
P o eins o he KT/HAK/KUP amily a e p esen in plan s,
ungi, bac e ia, and e en i uses (G eine e  al., 2011; San a-
Ma ia e  al., 2018), and hey a e o en associa ed wi h K+
anspo ac oss memb anes and K+ supply. In bac e ial genomes,
K+ ca ie s o his amily a e encoded by single-copy genes
named kup. In Esche ichia coli, kup is a cons i u i e low-a ini y
up ake sys em ha ope a es as K+-H+ sympo e (Zakha yan
and T chounian, 2001). In ungi, he homologous p o eins a e
encoded by HAK1-like genes p esen as one- o wo-copy in
AB
C
FIGURE 2 | Topological models o he main ion anspo e s in ol ed in K+ nu i ion. (A) Vol age-ga ed K+ channels con ain six ansmemb ane domains
(S1–S6); S4 is he ol age-senso cha ac e ized by he a ay o posi i ely cha ged amino acids (+). The long C- e minal ail con ains se e al conse ed
domains: C-linke , a cyclic nucleo ide binding homologous domain (CNBHD), an anky in domain (ANK), and a inal egion ich in hyd ophobic and acidic esidues
(KHA). (B) HKT anspo e s ha e a channel-like s uc u e ha con ains ou iden ical subuni s (a–d), each comp ising wo ansmemb ane helices (M1 and M2)
connec ed by he P-loop in ol ed in ion selec i i y. (C) KT/HAK/KUP anspo e s ha e 12 pu a i e ansmemb ane domains (TMs). TM1-5 and TM6-10 a e
p edic ed o old in he same con o ma ion bu showing in e se symme y.
Ragel e al. Regula ion o K+ Nu i ion in Plan s
F on ie s in Plan Science | www. on ie sin.o g 4 Ma ch 2019 | Volume 10 | A icle 281
mos species. In con as o bac e ial kup, ungal HAK genes
a e s ongly induced by K+ s a a ion and he encoded p o eins
media e high-a ini y K+ anspo (Beni o e  al., 2011). In
plan s, hese anspo e s a e known as KT, HAK, o KUP
(KT/HAK/KUP amily) and hey a e ep esen ed by mul iple
genes in hei genomes. Membe s o his amily ha e been
widely associa ed wi h high-a ini y K+ up ake om he soil,
while o he s may unc ion in bo h low-a ini y and/o high-
a ini y anspo (Luan e  al., 2009; Ve y e  al., 2014) and
o he oles ela ed, o example, o K+ ansloca ion, con ol
o wa e mo emen a he plan le el, sal ole ance, osmo ic/
d ough esponses, anspo o o he alkali ca ions, and
de elopmen al p ocesses in plan s, such as oo hai g ow h
and auxin dis ibu ion (Li e al., 2018; San a-Ma ia e al., 2018).
These di e se unc ions o KT/HAK/KUP anspo e s may all
esul om hei c i ical oles in cellula K+ homeos asis.
KT/HAK/KUP genes a e no p esen in animal cells, wha could
indica e ha hey a e c ucial o K+ anspo in o ganisms
acing ex e nal solu ions wi h luc ua ing and e y low K+
concen a ions, o en in he μM ange (Ashley e  al., 2006).
Based on he p esen knowledge, KT/HAK/KUP genes a e
p esen in all plan genomes, which con as s wi h ha in he
o he kingdoms, whe e hey a e only p esen in ce ain species
(G abo , 2007; G eine e al., 2011). This di e ence may e lec
he impo ance o hese anspo e s o he plan ’s way o li e.
KT/HAK/KUP anspo e s o land plan s a e classi ied
acco ding o hei sequence homology in o six clus e s o clades
(I–VI), wi h clade VI including only membe s o b yophy es
(San a-Ma ia e al., 2018). Phylogene ic analysis shows ha all
KT/HAK/KUPs om algae di e ge om land plan clades,
sugges ing ha he di e si ica ion in o hese g oups ook place
a e he coloniza ion o land by g een o ganisms (San a-Ma ia
e  al., 2018). The KT/HAK/KUP g oup om angiospe ms
displays a high and a he a iable numbe o membe s in
he di e en plan species genomes ha ha e been sequenced
so a . Fo ins ance, he e a e 13 genes in A abidopsis, 16 in
peach, 17 in g ape ine, 20 in Medicago, 21 in Cassa a, 27 in
ice, maize, and B achypodium, and 57 in Panicum i ga um
(Song e  al., 2015; Nie es-Co dones e  al., 2016a,c; Ou e  al.,
2018). Membe s o KT/HAK/KUP amily in angiospe m a e
classi ied among clades I–V (Nie es-Co dones e  al., 2016c).
The KT/HAK/KUP anspo e s in ol ed in K+ up ake om
he soil a e clus e ed in o a dis inc subg oup o clade I, e med
Ia (Nie es-Co dones e  al., 2016c) and ha we call he ein
HAK1-like anspo e s by analogy wi h he ungal coun e pa s.
This subg oup includes ba ley H HAK1 (San a-Ma ía e  al.,
1997; Gie h and Mäse , 2007), A abidopsis A HAK5 (Rubio
e  al., 2000; Gie h e  al., 2005), ice OsHAK1 and OsHAK5
(Bañuelos e  al., 2002), peppe CaHAK1 (Ma inez-Co de o
e  al., 2004), oma o LeHAK5 (Nie es-Co dones e  al., 2007),
and Thellungiella ThHAK5 (Alemán e al., 2009b). High-a ini y
K+ anspo has been demons a ed o all he HAK1-like
anspo e s in he e ologous exp ession sys ems (Nie es-Co dones
e  al., 2014a). On he o he hand, A KUP7, belonging o clade
V, could bein ol ed in K+ up ake om low o mode a e ex e nal
K+ concen a ions (Han e al., 2016), and hus he pa icipa ion
in K+ up ake om soil o p o eins om di e en clades should
no bedisca ded. In e es ingly, o he membe s o clade Icould
be ela ed wi h K+ up ake by cells om specialized issues.
DmHAK5 om Venus ly aps is implica ed in he up ake o
K+ eleased om he diges ed p ey in he bi-lobed cap u e
o gan (Sche ze e al., 2015), whe eas he quinoa CqHAK5-like
d i es K+ in lux in o cells o he lea sal bladde s o con ibu e
o he osmo ic balance o he cy osol agains he osmo ic
p essu e o he sal -con aining acuoles (Bohm e  al., 2018).
KT/HAK/KUP anspo e s a e phylogene ically ela ed o he
supe amily o acid-polyamine-o ganoca ion (APC) anspo e s
ha comp ises seconda y ac i e anspo p o eins esponsible
o unipo , sympo , and an ipo o a wide ange o subs a es
(Vas e ma k e  al., 2014). Taking as empla e c ys al s uc u es
o p oka yo ic APC anspo e s, compu a ional 3D modeling
o A KUP7 (Ahn e al., 2004; Al-Younis e al., 2015; San a-Ma ia
e  al., 2018), A KUP4/TRH1 (Da as e  al., 2015), OsHAK1 (Rai
e al., 2017), A KUP1/TRH1 (San a-Ma ia e al., 2018), A HAK5
(San a-Ma ia e  al., 2018), and H HAK1 (San a-Ma ia e  al.,
2018) has been epo ed. The s uc u al models (Figu e 2) show
he p esence o common a ibu es among all o hem: (1) a
hyd ophobic co e con aining 10–14 ansmemb ane (TM)
segmen s; and (2) h ee cy osolic domains— he N- and C- e mini
and a egion con aining app oxima ely 70 esidues si ua ed
be ween second and hi d TMs (loop II–III). Al hough, he
s uc u e o he po e egion has no been desc ibed ye , se e al
wo ks ha e analyzed he e ec o mu a ions on he unc ion
o hese anspo e s (San a-Ma ia e  al., 2018). So a , esul s
indica ed ha se e al pa s o he p o ein may con ibu e o
se ing he Vmax o he anspo e and ha he egion including
om N- e minus o loop II–III may con ibu e in de e mining
i s Km. Fu he mo e, sequence alignmen s show ha , al hough
he e is no ex ensi e sequence conse a ion, 40 amino acid
esidues a e conse ed in exac ly he same posi ion in all
he euka yo ic HAK anspo e s and in he Kup bac e ial
anspo e s (Rod iguez-Na a o, 2000). Six o hese conse ed
esidues a e included in a highly conse ed mo i in he
i s ansmemb ane domain whose consensus sequence is
GVVYGDLGTSPLY ( he amino acids conse ed in all p o eins
a e in bold) (Rod iguez-Na a o, 2000). A helical-wheel
ep esen a ion o his ansmemb ane agmen loca es h ee
glycine esidues on he same side o he helix, which in he
case o a e ame ic s uc u e may ope a e as a subs a e
selec i i y il e analogous o he GXGYGD mo i highly
conse ed in K+ channels. Rega ding his, i has been sugges ed
ha A KUP4/TRH1 may o m homodime s (Da as e al., 2015),
likely in ol ing he in e ac ion be ween C- e minus domains
and less likely be ween loops II–III.
Con a y o VG channels ha a e all a ge ed o he plasma
memb ane, KT/HAK/KUP anspo e s ha e been epo ed in
di e en subcellula compa men s (Table 1). The majo i y o
he cha ac e ized anspo e s o he KT/HAK/KUP amily a e
loca ed in he plasma memb ane, al hough no all o hem
a e in ol ed in K+ nu i ion. Fo ins ance, A KUP4/TRH1 seems
o pa icipa e in auxin anspo ela ed wi h oo g a i opism
and oo hai de elopmen (Rigas e al., 2013), whe eas A KUP6
ac s in la e al oo ini ia ion and de elopmen in he auxin
and ABA c oss alk signaling pa hways (Osakabe e  al., 2013).
Ragel e al. Regula ion o K+ Nu i ion in Plan s
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HKT P o eins
The ample epe oi e o anspo e s encoded in he genome
o plan s includes p o eins ha a e collec i ely known as High
a ini y K+ T anspo e s (HKTs; Figu e 2) despi e he ac ha
hese p o eins acili a e Na+-selec i e unipo o Na+-K+ sympo
wi h a channel-like ac i i y (Beni o e  al., 2014). Phylogene ic
and unc ional analyses dis inguished wo HKT sub amilies
(Pla en e  al., 2006). Membe s o sub amily I (HKT1) a e
ubiqui ous in plan s, Na+-selec i e, and mos ly in ol ed in Na+
eci cula ion h ough ascula issues, as bes exempli ied by
A HKT1;1 (Suna pi e  al., 2005). Membe s o sub amily II
(HKT2) ha e been ound only in monoco yledonous species.
Al hough hey a e all K+-pe meable, mechanis ically HKT2s
can ope a e as ei he Na+-K+ sympo e s o K+-selec i e unipo e s
[ e iewed by Beni o e al. (2014)]. HKT2-like p o eins o ce eals
ha e been in ol ed in K+ nu i ion.
K+ UPTAKE BY ROOTS
The up ake o K+ by oo s (o en measu ed wi h ubidium as
ace ) exhibi s a biphasic kine ics in esponse o inc easing
ex e nal concen a ions co esponding o high- and low-a ini y
anspo sys ems, which wo k a low (<1 mM) and high
(>1mM) ex e nal K+ concen a ions espec i ely (Eps ein e al.,
1963; Gie h and Mäse , 2007). A high concen a ion in he
soil solu ion, K+ c osses he memb ane mos ly h ough channels.
The channels simply gi e a pa h o he ions allowing hem
o mo e down he elec ochemical g adien . A low K+
concen a ion, ac i e anspo e sys ems a e needed in o de
o pull K+ inside he cell agains i s elec ochemical g adien .
Howe e , s udies in se e al plan species ha e shown ha channels
may be in ol ed in K+ up ake in he high-a ini y ange o K+
concen a ions (Rubio e  al., 2010) as long as he memb ane is
su icien ly hype pola ized, i.e. highly elec onega i e inside (Hi sch
e  al., 1998; Spalding e  al., 1999; Gie h and Mäse , 2007;
Rubio e  al., 2010).
The sensi i i y o NH4+ is an impo an cha ac e is ic o high-
a ini y K+ up ake media ed by ca ie s ha has been used as
a ool o he iden i ica ion o addi ional high-a ini y anspo
sys ems (San a-Ma ía e al., 1997; Nie es-Co dones e al., 2007).
NH4+-sensi i e and -insensi i e componen s o high-a ini y K+
up ake ha e been iden i ied in A abidopsis (Spalding e al., 1999),
ba ley (San a-Ma ia e  al., 2000), peppe (Ma inez-Co de o
e  al., 2005), and ice (Bañuelos e al., 2002; Chen e  al., 2015).
Resul s indica e ha he NH4+-sensi i e componen o K+ up ake
is likely media ed by KT/HAK/KUP anspo e s (HAK1-like
anspo e s), whe eas inwa d- ec i ie K+ channels (AKT1-like
channels) cons i u e he NH4+-insensi i e pa hway (San a-Ma ia
e al., 2000; Nie es-Co dones e al., 2014a). Toge he , AKT1-like
channels and HAK1-like anspo e s a e now hough o
cons i u e he main sys ems o K+ up ake in plan s unde low-K+
concen a ions (Table 2). Howe e , he NH4+-sensi i e and
-insensi i e pa hways appea o con ibu e di e en ly o high-
a ini y K+ up ake depending on he plan species and he ionic
ex e nal concen a ion o anspo ed subs a es, mainly K+, NH4+,
and Na+ (Aleman e  al., 2011; Nie es-Co dones e  al., 2016c).
Among he inwa d- ec i ying K+ channels o A abidopsis, only
AKT1 and A KC1 a e abundan ly exp essed in oo issues (Rein anz
e al., 2002). A KC1 exp essed alone emains in he endoplasmic
e iculum, bu i can be ec ui ed o he plasma memb ane o
egula e AKT1 ac i i y (Duby e  al., 2008; Geige e  al., 2009;
Honsbein e  al., 2009; Wang e  al., 2010). In addi ion, AKT1 is
posi i ely egula ed by he p o ein kinase complex comp ising
he kinase CIPK23 and one o he wo al e na i e calcium-
dependen egula o y subuni s CBL1 and CBL9 (Li e  al., 2006;
TABLE 1 | Sub-cellula loca ion o selec ed A abidopsis, ba ley, ice, and Physcomi ella pa ens KT/HAK/KUP anspo e s.
T anspo e /loca ion Plasma memb ane Tonoplas ER-like memb anes Thylakoid memb anes Re e ences
A HAK5 √Qi e al., 2008
A KUP4/TRH1 √√√ Rigas e al., 2013
A KUP5 √Jaquinod e al., 2007;
Whi eman e al., 2008
A KUP6 √Osakabe e al., 2013
A KUP7 √ √ Han e al., 2016
A KUP8 √Jaquinod e al., 2007;
Whi eman e al., 2008
A KUP12 √ √
Kle mann e al., 2004;
Jaquinod e al., 2007;
Whi eman e al., 2008
H HAK1 √Senn e al., 2001
OsHAK1 √Chen e al., 2015
OsHAK5 √Yang e al., 2014
OsHAK10 √Bañuelos e al., 2002
OsHAK21 √Shen e al., 2015
PpHAK2 √Ha o e al., 2013
PpHAK3 √Ha o e al., 2013

Ragel e al. Regula ion o K+ Nu i ion in Plan s
F on ie s in Plan Science | www. on ie sin.o g 6 Ma ch 2019 | Volume 10 | A icle 281
Xu e  al., 2006). AKT1 possesses an in insic K+ senso educing
channel conduc ance a submillimola ex e nal K+ concen a ions.
Despi e his K+ senso , upon ac i a ion by he CIPK/CBL complex
a low ex e nal K+, he homome ic AKT1 channels open a
ol ages posi i e o EK, a condi ion po en ially esul ing in cellula
K+ leakage (Geige e  al., 2009). Inco po a ion o he A KC1
subuni in o he channel complex, howe e , shi s he ol age
dependence o AKT1 owa d mo e nega i e po en ials (ca. −70mV)
o p e en K+ loss (Geige e  al., 2009; Wang e  al., 2010; Wang
e al., 2016). In o he wo ds, AKT1/KC1 he e ome iza ion ende s
he channel mo e e icien a blocking K+ pe mea ion in he
ou wa d di ec ion. The physical in e ac ion o he CIPK23/CBL1
complex is speci ic o AKT1 channels and does no in ol e he
A KC1 subuni . The gain-o - unc ion mu a ion A KC1-D (G322D
subs i u ion in ansmemb ane S6) was eco e ed in he cipk23
mu an backg ound. A KC1-D enhanced he inhibi ion o AKT1
channel ac i i y and es ic ed K+ leakage h ough AKT1 unde
low-K+ condi ions, he eby inc easing he ole ance o nu ien
s ess (Wang e  al., 2016). Al hough he double mu an ak 1
KC1-D was sensi i e o low-K+, indica ing ha KC1-D ac ion is
h ough AKT1, an addi ional indi ec e ec o mu a ion KC1-D
h ough HAK5 canno be uled ou . By inhibi ing AKT1 and
shi ing i s ol age dependence owa d a mo e nega i e di ec ion,
he plasma memb ane could become hype pola ized in he KC1-D
mu an , he eby enhancing he exp ession and ac i i y o HAK5
and imp o ing ne K+ up ake.
Se e al mechanisms o AKT1 deac i a ion ha e been p oposed.
The PP2C- ype p o ein phospha ase AIP1 in e ac s wi h and
inac i a es he AKT1 channel, coun e ac ing he ac i a ion by
CIPK23in oocy es (Lee e al., 2007). In p inciple, hese indings
a e e idence o a phospho yla ion/dephospho yla ion swi ch ha
egula es AKT1 channel ac i i y, bu i should be no ed ha
no phospho yla ion o AKT1 by CIPK23 and dephospho yla ion
by AIP1 has been demons a ed conclusi ely (Hashimo o e al.,
2012). Ins ead, ou componen s, CIPKs, CBLs, PP2Cs, and
AKT1, appea o in e ac mu ually and o m a molecula complex
whose speci ic composi ion could ul ima ely egula e channel
ac i i y (Lan e  al., 2011). In his model, PP2C phospha ases
in e ac wi h he kinase domain o CIPKs o coun e ac kinase-
media ed ac i a ion o AKT1. Upon calcium signaling, CBLs
in e ac wi h PPC2C o inhibi hei phospha ase ac i i y while
simul aneously ac i a ing he pa ne ing CIPKs. On he o he
hand, CBL10, a egula o y subuni o CIPK24/SOS2 bu no o
CIPK23, also in e ac s di ec ly wi h AKT1 and nega i ely modula es
AKT1 ac i i y by compe ing wi h CIPK23 o bind AKT1 (Ren
e  al., 2013). Since CBL10 unc ion is ela ed o salini y s ess
a he han o mine al nu i ion (Kim e  al., 2007; Quan e  al.,
2007; Lin e  al., 2009), his c oss- egula ion may cons i u e a
mechanism o p e en salini y-induced K+ loss hough AKT1.
In line wi h his, he ni ic oxide (NO) ha accumula es unde
salini y s ess also inhibi s he K+ up ake media ed by AKT1.
The link is indi ec since NO igge ed he accumula ion o
py idoxal 5′-phospha e (PLP), an ac i e o m o i amin B6,
ha in u n ep essed he ac i i y o AKT1in Xenopus oocy es
and A abidopsis oo p o oplas s (Xia e  al., 2014).
In A abidopsis, he ol age-ga ed channel GORK (gua d cell
ou wa d- ec i ying K+) is he majo ou wa d- ec i ying K+
channel in gua d cells whe e i con ibu es o K+ e lux o
dec easing u go and s oma al closu e (Ache e al., 2000; Hosy
e  al., 2003). In addi ion, GORK is exp essed in oo ou e
cell laye s (epide mal, oo hai s, and co ex) o A abidopsis
and hus GORK is conside ed a majo pa hway o s ess-
induced K+ leakage om oo cells, e.g. by exposu e o oo s
o high sal (I ashikina e  al., 2001; Demidchik e  al., 2010;
Demidchik e al., 2014). P oduc ion o hyd oxyl adicals (HO˙)
in salinized oo s s imula es a d ama ic K+ e lux media ed by
GORK om oo cells (Demidchik e  al., 2010). The oxida i e
and sal s esses cause p og ammed cell dea h (PCD) and
collapse memb ane po en ial in oo cells o A abidopsis haliana
in a K+-dependen manne . Acco dingly, he A abidopsis go k1-1
mu an showed no K+ ou wa dly di ec ed cu en s in esponse
o HO˙. Besides, a e exposu e o high NaCl le els, he mu an
go k1-1 displayed lowe ac i i y o p o eases and endonucleases
o PCD, which in he wild ype was d ama ically enhanced
by K+ loss in oo cells (Demidchik e  al., 2010).
Bo h he exp ession le el and channel ac i i y o GORK
a e signi ican ly up egula ed by inc easing le els o he abscisic
acid (ABA) and jasmona e. S imuli ha ele a ed endogenous
ABA concen a ions, e.g. d ough , osmo ic s ess, o cold, led
o he up- egula ion o GORK ansc ip s (Becke e al., 2003;
Suhi a, 2004) while ea men wi h salicylic acid inhibi ed he
p esence o ac i e GORK channels and imp o ed salini y
ole ance h ough p e en ion o K+ e lux. Recen s udies
demons a ed ha calcium-dependen p o ein kinase 21 (CPK21)
phospho yla ed GORK and sugges ed ha 14-3-3 p o eins
con ol GORK ac i i y h ough binding wi h CPK21. This
kinase phospho yla es h ee amino acid esidues in he
C- e minus o GORK, T344, S518, and S649. Binding o 14-3-3
o CPK21 s ongly s imula ed i s kinase ac i i y and inc eased
TABLE 2 | Compa ison o AKT1 channels and HAK1/HAK5 anspo e s om
A abidopsis and ice wo king a di e en anges o ex e nal K+ concen a ions.
The up ake sys ems wo king in addi ion o AKT1 and HAK1/HAK5 likely include
CHX exchange s (Zhao e al., 2008) and cyclic nucleo ide-ga ed channels
(CNGC) ha may con ibu e o K+ abso p ion when he ex e nal K+ concen a ion
is su icien ly high (Caballe o e al., 2012).
Ex e nal [K+] A abidopsis Rice
<10μM A HAK5 OsHAK1
10–100μM A HAK5
A KUP7
A AKT1
OsHAK1
OsHAK5
OsAKT1
100–200μM A HAK5
A AKT1
OsHAK1
OsHAK5
OsAKT1
200μM–1mM A AKT1 OsHAK1
OsHAK5
OsAKT1
1–10mM A AKT1
O he sys ems
(CHX, CNGC)
OsAKT1
Unknown sys ems
>10mM O he sys ems
(CHX, CNGC)
Unknown sys ems
Ragel e al. Regula ion o K+ Nu i ion in Plan s
F on ie s in Plan Science | www. on ie sin.o g 7 Ma ch 2019 | Volume 10 | A icle 281
GORK phospho yla ion ( an Klee e  al., 2018). On he o he
hand, he phospha ase A PP2CA in e ac s physically wi h GORK
inhibi ing i s cu en (Le oulon e  al., 2016). Thus, A PP2CA
could ha e an an agonis ole o CPK21 on he egula ion o
GORK ( an Klee e  al., 2018). These esul s imply ha he
salini y-induced memb ane depola iza ion oge he wi h he
Ca2+- and CPK21-dependen phospho yla ion ac oge he o
ac i a e GORK and o epola ize he plasma memb ane by
means o eleasing pa o he cy osolic K+. Mo eo e , he
peak o he sal -induced K+-e lux in he aha2 mu an , de oid
o a majo iso o m o he plasma memb ane H+-ATPase, was
s onge and mo e sus ained han in he wild- ype, sugges ing
ha H+-pumps ake o e memb ane epola iza ion a e he
ini ial K+-loss o e-enac K+ up ake ( an Klee e  al., 2018).
Recen ly, Sapona o e  al. (2017) showed ha 14-3-3 p o eins
a e also capable o modula ing KAT1, al hough in his case
14-3-3 bound di ec ly o he KAT1 C- e minus a ec ing bo h
he ol age dependency o he channel and he numbe o
channel molecules in he memb ane (So oco nola e al., 2008).
K+-H+ sympo has long been conside ed he likely ca aly ic
mechanism o plan KT/HAK/KUP anspo e s based on he
demons a ion ha K+-H+ sympo ope a es in K+-s a ed
Neu ospo a c assa and on he modynamical conside a ions ega ding
he s eep K+ g adien ha KT/HAK/KUP p o eins a e able o
achie e ac oss cell memb anes ha exceeds wha could be eached
by coupling he K+ up ake o he memb ane po en ial solely
(Rod iguez-Na a o, 2000). Un il ecen ly, e o s o exp ess plan
KT/HAK/KUP p o eins in Xenopus oocy es o measu e K+ cu en s
had ailed, bu wo k wi h he DmHAK5 anspo e om Venus
ly aps showed ha co-exp ession o he co esponding cRNA
wi h ha o CBL9/CIPK23 (bu no DmHAK5 alone) gene a ed
inwa d K+ and Rb+ cu en s in Xenopus oocy es ha we e s imula ed
by low ex e nal pH (Sche ze e al., 2015). Mo eo e , sal bladde s
o he halophy e Chenopodium quinoa ha accumula e sal s o
e y high concen a ions exp ess a HAK-like ac i i y d i ing
high-a ini y and selec i e K+ up ake ha was dependen on acidic
ex e nal pH and by he CIPK23/CBL1 kinase module o A abidopsis
(Bohm e al., 2018). Elec ophysiological eco dings in ice oo s
showed ha he ac i i y o OsHAK1 was s ongly elec ogenic
and depola izing. Plo s o he OsHAK1-dependen K+-induced
memb ane depola iza ion had a slope o 29 mV pe decade o
ex e nal K+ concen a ion, sugges ing he co- anspo o wo
mono alen ca ions (a 59 mV slope is o be expec ed om an
unip o anspo mo ing only single K+ ions) (Nie es-Co dones
e al., 2017). Toge he , hese da a s ongly sugges ha plan KT/
HAK/KUP p o eins ope a e as K+-H+ sympo e s. Residues
in ol ed in K+ binding and/o anspo ha e no been iden i ied;
howe e , mu an p o eins wi h esidue subs i u ions o membe s
o he KT/HAK/KUP amily ha e been desc ibed as showing
modi ied a ini y o K+, Na+, and/o Cs+, o inc eased Vmax
(Aleman e  al., 2014).
HAK1-like anspo e s a e subjec o complex ansc ip ional
and pos - ansla ional egula ions, al hough s udies ha e been
ca ied ou almos exclusi ely in A abidopsis A HAK5 (Jung
e  al., 2009; Rubio e  al., 2014; Ragel e  al., 2015). Unde any
s ess condi ions ha di ec ly a ec K+ acquisi ion, such as K+
dep i a ion o salini y, high-a ini y K+ up ake sys ems should
be ansc ip ionally o pos - ansla ionally ac i a ed in o de o
main ain he K+ supply and K+/Na+ homeos asis. Acco dingly,
all cha ac e ized HAK1-like anspo e s exhibi low exp ession
le els in oo s unde con ol condi ions, a e highly up- egula ed
upon K+ dep i a ion and apidly down- egula ed when K+ is
esupplied ( e iewed by (Li e  al., 2018)). Fu he mo e, i has
been commonly obse ed ha o he ions, pa icula ly NH4+,
NO3−, Na+, and Pi, also egula e he exp ession o HAK1-like
genes and no always in he same way (Nie es-Co dones e  al.,
2019). Fo example, NH4+ educes he ansc ip ional induc ion
by K+ s a a ion o he peppe CaHAK1 (Ma inez-Co de o
e  al., 2005) and A abidopsis A HAK5 (Qi e  al., 2008), bu
enhances he exp ession o LeHAK5 in oma o (Nie es-Co dones
e  al., 2007). The p esence o NaCl p e en s he induc ion o
LeHAK5 by K+ s a a ion (Nie es-Co dones e  al., 2007), bu
p o okes a s ong and ansien up- egula ion o H HAK1 (Fulgenzi
e  al., 2008). Thus, he A abidopsis model canno be comple ely
ex ended o o he plan species, c ops among hem. In con as
o HAK1-like anspo e s, KT/HAK/KUP p o eins belonging
o clus e s II–V show di e se exp ession pa e ns and mos o
hem do no exhibi ansc ip ional egula ion in esponse o
K+ de iciency (Ahn e  al., 2004; Li e  al., 2018). Fo example,
A KUP7 (clus e V, plasma memb ane) ansc ip is no induced
by low-K+ (Han e al., 2016) and A KUP12 (clus e III, chlo oplas )
is down- egula ed a e K+ esupply (A mengaud e  al., 2004).
Rega ding he ansc ip ional egula ion o genes encoding
HAK1-like anspo e s, i has been shown ha he e ec o
he nu ien de iciency and sal s esses on ansc ip ional
exp ession o A HAK5 and LeHAK5 is associa ed wi h changes
in he oo cell memb ane po en ials (Nie es-Co dones e  al.,
2008; Rubio e  al., 2014); he hype pola iza ion o he plasma
memb ane o oo cells induces ansc ip ion o bo h genes.
Suppo ing his, ThHAK5 o Thellungiella halophila (sal c ess,
a.k.a. Eu ema salsuginea) is exp essed o highe le els han
A HAK5 unde sal s ess, while oo s o T. halophila main ained
a mo e nega i e memb ane po en ial han A abidopsis oo s
(Volko and Am mann, 2006; Alemán e  al., 2009b; Rubio
e al., 2014). Besides memb ane hype pola iza ion, he exp ession
o A HAK5 is also induced, unde K+-limi ing condi ions, as
esul o signaling cascades ha in ol e ROS p oduc ion,
phy oho mones, and ansc ip ion ac o s. Low-K+ s ess, alike
o he nu ien -dep i ed condi ions, p omo es an inc ease o
e hylene ha posi i ely egula es ROS p oduc ion in oo s (Shin
and Schach man, 2004; Jung e  al., 2009). Roo s dep i ed o
K+ induce he exp ession o genes in ol ed in e hylene
biosyn hesis and signaling, and in ROS me abolism, p omo ing
wo- old highe le els o e hylene and he inc ease in hyd ogen
pe oxide (H2O2) concen a ions. Bo h e hylene and ROS gi e
ise o enhanced ansc ip ion o HAK5 in A abidopsis and
oma o (Rodenas e  al., 2018). In A abidopsis, H2O2 p oduced
by he NADPH oxidase RHD2/RbohC egula es he exp ession
o A HAK5 in esponse o K+ de iciency (Shin and Schach man,
2004) and i has been p oposed ha pe oxidase RCI3 (Ra e
Cold Inducible gene 3) con ibu es o ROS p oduc ion du ing
A abidopsis oo esponse o K+ de iciency (Kim e  al., 2010).
In he case o e hylene-induced A HAK5 ansc ip ion, he
in e media ies in e hylene signaling CTR1 (Cons i u i e T iple
Ragel e al. Regula ion o K+ Nu i ion in Plan s
F on ie s in Plan Science | www. on ie sin.o g 8 Ma ch 2019 | Volume 10 | A icle 281
Response (1) and EIN2 (E hylene Insensi i e (2) a e pa ially
in ol ed. Resul s also sugges he exis ence o o he signaling
pa hways o an EIN2-independen e hylene ou e ha may
play an impo an ole in low-K+ signaling (Jung e al., 2009).
Gene ic hie a chy indica es ha e hylene signaling ac s ups eam
o ROS when plan s a e dep i ed o K+ (Jung e  al., 2009).
Ne e heless, i has also been specula ed ha a posi i e eedback
may s imula e e hylene-induced ROS p oduc ion (Wang e al.,
2002). O he ho mones ha e been shown o be in ol ed in
K+ dep i a ion signaling and esponse, o ins ance jasmonic
acid (A mengaud e  al., 2004), auxin (Jung e  al., 2009; Hong
e  al., 2013), ABA (Kim e  al., 2010), cy okinins (Nam e  al.,
2012), and gibbe ellins h ough DELLA p o eins (Oli e uk e al.,
2017). Cy okinins a e known o egula e mac onu ien
homeos asis by con olling he exp ession o ni a e, phospha e,
and sul a e anspo e s. Cy okinin con en dec eases unde
K+-s a ed condi ions, and cy okinin-de icien mu an s, unde
same condi ions, display enhanced accumula ion o bo h ROS
and A HAK5 ansc ip s (Nam e  al., 2012). By con as ,
cy okinin- ecep o mu an s los he esponsi eness o low-K+,
including ROS accumula ion and oo hai g ow h. In e es ingly,
he cy okinin/e hylene a io is posi i ely co ela ed wi h oma o
shoo biomass, sugges ing ha he balance be ween bo h
ho mones is impo an in de e mining he plan igo a low-K+
supply, bu wi h an in e se ole in oma o compa ed o
A abidopsis, whe e cy okinin/e hylene a io was nega i ely
co ela ed wi h ole ance o K+ dep i a ion (Jung e  al., 2009;
Nam e  al., 2012).
In addi ion o low nu ien condi ions, sal s ess (and
p esumably o he abio ic s esses) esul s in modi ica ions o
A HAK5 exp ession o he low-K+ esponse. Mild sal s ess
does no induce A HAK5 exp ession bu i s exp ession le els
g adually inc eased ollowing an inc ease in NaCl concen a ions
(Ahn e  al., 2004; Hong e al., 2013). This sugges s ha plan s
may ecognize high Na+ le els as K+ dep i a ion. Howe e ,
he induc ion o A HAK5 exp ession by low K+ was supp essed
by sal s ess in A abidopsis (Nie es-Co dones e  al., 2010),
bu no in T. halophila (Alemán e  al., 2009a). As discussed
abo e, unde sal s ess condi ions, T. halophila egis e s a
mo e nega i e oo memb ane po en ial han A. haliana (Volko
and Am mann, 2006), which may explain he exp ession o
ThHAK5 unde hese condi ions (Alemán e  al., 2009a).
In ecen yea s, se e al ansc ip ion ac o s (TFs), and hei
a ge sequences, ha e been iden i ied in he A HAK5 p omo e .
Among hem, ARF2 (Auxin Response Fac o 2) is he only
one desc ibed so a o wo k as nega i e egula o o A HAK5
ansc ip ion (Zhao e  al., 2016). In e es ingly, ARF2 has been
ound o bein ol ed in many phy oho mone-signaling pa hways,
bu i seems no o pa icipa e in auxin signaling. Unde K+-
su icien condi ions, channel-media ed K+ up ake would
beene ge ically mo e a o able han sympo h ough A HAK5,
and hence A HAK5 should be shu down (Zhao e  al., 2016).
In hose condi ions, ARF2 binds o he auxin- esponsi e elemen s
(AuxREs) wi hin he A HAK5 p omo e and ep esses
ansc ip ion. When plan s a e subjec ed o low-K+ s ess, ARF2
is apidly phospho yla ed by an unknown kinase and loses
DNA binding ac i i y. ARF2 is emo ed om he A HAK5
p omo e , which elie es he ep ession on A HAK5 ansc ip ion.
In u n, o he TFs bind o he A HAK5 p omo e and ac i a e
i s ansc ip ion. These TFs up- egula ing A HAK5 exp ession
unde K+ s a a ion include RAP2.11, which binds o he
e hylene- esponsi e elemen (ERE) and he GCC-box o he
A HAK5 p omo e , and whose exp ession is s imula ed by
e hylene and ROS, alike A HAK5 (Kim e al., 2012). TFs DDF2,
JLO, bHLH121, and TFII_A also in e ac wi h he ups eam
egion o A HAK5, bu he speci ic binding mo i o each o
hem has no been iden i ied ye (Hong e  al., 2013). All o
hese ansc ip ion ac o s a e su icien o ac i a e A HAK5
exp ession in he e ologous sys ems, bu none o hem is absolu ely
equi ed. When K+ is esupplied, ARF2 becomes dephospho yla ed
again and ep esses A HAK5 exp ession (Zhao e  al., 2016).
Thus, i is appa en ha egula ion o he ac i i y o TFs ac ing
on A HAK5 ansc ip ion (posi i ely o nega i ely) is necessa y
o de e mine coope a i ely he accumula ion o he co esponding
ansc ip s (San a-Ma ia e  al., 2018).
Al hough a gene al nu ien dep i a ion s imulus is su icien
o he ansc ip ional ac i a ion o A HAK5 and LeHAK5 genes,
a educ ion o in e nal K+ is equi ed o he induc ion o a
unc ional HAK5-media ed high-a ini y K+ up ake in A abidopsis
and oma o oo s (Rubio e  al., 2014), sugges ing he exis ence
o pos - ansc ip ional egula ion in plan a. Recen ly, i was
shown ha ac i a ion o high-a ini y K+ up ake media ed by
A HAK5 (Ragel e  al., 2015), DmHAK5 om Venus ly aps
(Sche ze e  al., 2015), and CqHAK om quinoa (Bohm e  al.,
2018) is media ed by he CBL-in e ac ing p o ein kinase (CIPK)/
calcineu in B-like p o ein (CBL) complex comp ising CIPK23
and CBL1/9 p o eins o A abidopsis. No ably, his CIPK23/CBL1,9
module also ac i a es AKT1 channel, ha oge he wi h A HAK5
cons i u es he main K+ up ake pa hway in A abidopsis oo s
(Xu e  al., 2006; Lee e  al., 2007). Bo h he p o ein kinase
A CIPK23 and he Ca2+ senso A CBL1 a e necessa y and
su icien o ac i a ion o he high-a ini y K+ anspo e
A HAK5 in yeas (Ragel e  al., 2015). Besides A CBL1, o he
CBLs (A CBL8/9/10) a e able o bind A CIPK23 and ac i a e
A HAK5 o complemen K-up ake de ec i e yeas g ow h. The
educ ion in he K+ concen a ion p oduces a speci ic Ca2+
signa u e in he cy osol (Figu e 3) (Behe a e  al., 2017) ha
would be eco ded by A CBL1, p omo ing CIPK23/CBL1 complex
o ma ion, and he ac i a ion o A HAK5 by phospho yla ion
a he cy osolic N- e minus (Ragel e  al., 2015), in a simila
way ha was desc ibed o AKT1 (Xu e  al., 2006; Lee e  al.,
2007). The enhancemen o g ow h a low-K+ o yeas cells
co-exp essing A HAK5, A CIPK23, and A CBL1 seems o
esul om modi ica ion o he kine ic p ope ies o he
anspo e (Km dec ease and Vmax inc ease), likely h ough
he phospho yla ion-induced con o ma ional changes o A HAK5
(Ragel e al., 2015). Howe e , since physical in e ac ion be ween
CIPK23/CBL1 and A HAK5 is also equi ed o ull ac i a ion
o A HAK5in yeas , he a icking o he anspo e o plasma
memb ane has been p oposed as a second mechanism o A HAK5
egula ion by CIPK23/CBL1 complex. Suppo ing his idea, he
A HAK5 p o ein was mainly de ec ed in he endoplasmic e iculum
o K+-su icien plan s, while K+ s a a ion p oduced an en ichmen
o A HAK5 p o ein in he plasma memb ane (Qi e  al., 2008).
Ragel e al. Regula ion o K+ Nu i ion in Plan s
F on ie s in Plan Science | www. on ie sin.o g 9 Ma ch 2019 | Volume 10 | A icle 281
In he e ologous sys ems, he A abidopsis CIPK23/CBL1,9 complex
enabled he ac i a ion o a ious membe s om clade Io KT/
HAK/KUP anspo e s, such as peppe CaHAK1 (Ragel e  al.,
2015) and Venus ly ap DmHAK5 (Sche ze e  al., 2015), bu
no o oma o SlHAK5 o he Eu ema salsuginea EsHAK5 (Ragel
e al., 2015). These esul s sugges ed ha he ac i a ion mechanism
by CIPK23/CBLs complexes is e olu iona ily conse ed, bu no
he phospho yla ion si e and/o he a ge sequence ecogni ion,
which may a y among dis an plan species. Acco dingly, a
quime ic oma o HAK5 p o ein ha con ained he 15 i s amino
acids o CaHAK1 could be ac i a ed by CIPK23/CBL1 in yeas
(Ragel e  al., 2015).
Since he wo main con ibu o s o K+ up ake in A abidopsis,
AKT1 and HAK5, a e egula ed by he CIPK23/CBL1,9 complex,
he coo dina ed egula ion o hese anspo sys ems dese es
a en ion. Unde K+-su icien condi ions, K+ up ake by HAK5
would beene ge ically mo e expensi e han pe mea ion h ough
he AKT1 channel. The H+-pumping ac i i y o plasma memb ane
ATPases, which is used o many seconda y anspo p ocesses,
c ea es pe se an elec ical cha ge (nega i e inside) ha su ices
o d aw signi ican amoun s o K+ in o he cy osol. A a egula
s eady memb ane po en ial o −120 o −180mV, oo epide mal
cells could sus ain a 100–1,000- old inwa d-di ec ed g adien o
K+. Howe e , coupling K+ up ake o H+ in lux no only e u ns
H+ o he cy oplasm bu also is mo e depola izing han simple
K+ pe mea ion, which in u n imposes a g ea e demand on
he H+-pumps and ATP consump ion. We specula e ha unde
such condi ions o K+ su iciency, he plasma memb ane is no
hype pola ized (o no enough), signaling phy oho mones a e
no p oduced, and he e o e ansc ip ion o HAK5 is no ac i a ed.
AKT1 would be ope a ional h ough he physical in e ac ion
wi h CIPK23 (and possibly o he CIPKs) (Lee e  al., 2007). As
he K+ concen a ion ou side dec eases, he unc ion o AKT1
becomes inc easingly hampe ed and ull ac i a ion by he Ca2+-
dependen CIPK23/CBL1,9 complex is equi ed o sus ain K+
up ake, while he KC1 sa egua d p e en s K+ leakage h ough
AKT1 (Wang e al., 2016). CIPK23 is known o display di e en
s a es o ac i a ion, depending on ac o s ha a ec he ac i a ion
o CIPKs by ups eam kinases (Ba ajas-Lopez e  al., 2018) and
CBL binding (Cha es-Sanjuan e  al., 2014). Thus, a mild K+
dep i a ion may p oduce a pa ially ac i a ed CIPK23 ha would
becompe en o ac i a ing AKT1 bu no HAK5, whe eas se e e
K+ dep i a ion leads o HAK5 ansc ip ion and o ull ac i a ion
o CIPK23, which would hen becompe en o ac i a ing HAK5
(Ragel e al., 2015). The CIPK23 is i sel induced ansc ip ionally
by low-K+ s ess (Xu e  al., 2006), which could also enhance
he esponse o nu i ional s ess.
The pa icipa ion o Ca2+ senso s in high-a ini y K+ up ake
could mechanis ically connec K+ s a a ion wi h o he abio ic
s esses, o ins ance: salini y, wa e a ailabili y, oxygen
de iciency (hypoxia) o absence (anoxia), mechanical s ess,
cold s ess, hea y me al s ess, and o he nu ien dep i a ions,
all sha ing cy osolic ee Ca2+ as a second messenge (Wilkins
e  al., 2016). Cu en hinking is ha he speci ici y o Ca2+
signaling is de e mined by he ampli ude and du a ion (and
possible oscilla ion) o he cy osolic Ca2+ inc ease, o en e e ed
o as he “calcium signa u e” ha is elici ed by he s imulus.
K+ de iciency e okes wo successi e Ca2+ signals in oo s
exhibi ing di e en spa ial and empo al speci ici y (Behe a
e  al., 2017). The i s one is cha ac e ized by a ansien
and as Ca2+ inc ease wi hin 1 min in he pos me is ema ic
elonga ion zone (mos p ominen ly in he ascula issue and
endode mis), ollowed by a Ca2+ e u n nea ly o basal
concen a ions in <7 min. The second wa e (seconda y Ca2+
FIGURE 3 | Regula o y ci cui y egula ing A HAK5 exp ession and ac i i y. K+ s a a ion is p obably sensed as hype pola iza ion o he plasma memb ane,
which, oge he wi h ele a ed e hylene and ROS le els, leads o exp ession o he HAK5 gene. Se e al ansc ip ional ac i a o and ep esso ac o s ha e been
iden i ied, bu hei placemen in speci ic signaling pa hways is unce ain. Subsequen ly, calmodulin-like (CML) and calcineu in B-like (CBL) Ca2+-binding
p o eins ec ui and ac i a e p o ein kinases ILK1 and CIPK23 ha acili a e he a icking o HAK5 o he plasma memb ane and i s biochemical ac i a ion,
espec i ely. CIPK23 also s imula es he K+-up ake channel AKT1. K+ eplenishmen depola izes he memb ane and e u ns he sys em o homeos a ic le els.
Ragel e al. Regula ion o K+ Nu i ion in Plan s
F on ie s in Plan Science | www. on ie sin.o g 16 Ma ch 2019 | Volume 10 | A icle 281
o cen al impo ance o plan nu i ion and dese e addi ional
esea ch. The a ailabili y o no el gene ically encoded K+ senso s
(Bischo e al., 2017) ha could be a ge ed o a ious cellula
compa men s o p ede ined cells and issues will be powe ul
ools o moni o he dynamics o cellula K+ wi h unp eceden ed
spa io empo al esolu ion.
AUTHOR CONTRIBUTIONS
All au ho s ha e con ibu ed o li e a u e sea ch, discussion,
and w i ing o he manusc ip . PR and JP assembled all sec ions.
PR and FQ p epa ed he Figu es. All au ho s checked and
app o ed he manusc ip .
FUNDING
This wo k was suppo ed by g an BIO2015-70946-R o FQ,
and by g an s BFU2015-64671-R and BIO2016-81957-REDT
om AEI-MINECO (co- inanced by he Eu opean Regional
De elopmen Fund), and he SSAC g an PJ01318205 om he
Ru al De elopmen Adminis a ion, Republic o Ko ea, o JP.
ACKNOWLEDGMENTS
We acknowledge suppo o he publica ion ee by he CSIC
Open Access Publica ion Suppo Ini ia i e h ough i s Uni
o In o ma ion Resou ces o Resea ch (URICI).
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