Physiologia Plantarum 163: 414–431.

2018 ISSN 0031-9317

Functioning of potassium and magnesium in photosynthesis,

photosynthate translocation and photoprotection
Merle Tränknera,* , Ershad Tavakolb and Bálint Jáklic
a
Institute of Applied Plant Nutrition (IAPN), Georg-August University Goettingen, 37075 Goettingen, Germany
b K+S Kali GmbH, 34131 Kassel, Germany
c
Department of Crop Science, Section of Plant Nutrition & Crop Physiology, Georg-August University Goettingen, 37075 Goettingen, Germany

Correspondence Potassium (K) and magnesium (Mg) are mineral nutrients that are required in
*Corresponding author, large quantities by plants. Both elements critically contribute to the process
e-mail: traenkner@iapn-goettingen.de
of photosynthesis and the subsequent long-distance transport of photoassimi-
Received 15 January 2018; lates. If K or Mg is not present in sufficient quantities in photosynthetic tissues,
revised 22 March 2018 complex interactions of anatomical, physiological and biochemical responses
result in a reduction of photosynthetic carbon assimilation. As a consequence,
doi:10.1111/ppl.12747 excessive production of reactive oxygen species causes photo-oxidation of
the photosynthetic apparatus and causes an up-regulation of photoprotec-
tive mechanisms. In this article, we review the functioning of K and Mg
in processes directly or indirectly associated with photosynthesis. Focus is
given to chloroplast ultrastructure, light-dependent and -independent reac-
tions of photosynthesis and the diffusion of CO2 – a major substrate for pho-
tosynthesis – into chloroplasts. We further emphasize their contribution to
phloem-loading and long-distance transport of photoassimilates and to the
photoprotection of the photosynthetic apparatus.

include optimal nutrient supply. Potassium and mag-

Introduction
Almost all plant species on Earth are autotroph and pro-
duce complex carbon compounds by the process of pho-
tosynthesis in which solar energy is captured. The solar
energy capture is the basis for productivity and the net
amount of carbon which is photosynthetically assimi-
lated in 1 year by the vegetation, the so called net primary
production, is suggested to be 104.9 Pg (Field 1998) (1
Pg = 1015 g). The net primary production is considered
the available amount of energy that can be transferred
from plants to other levels of trophic webs in ecosys-
tems (Haberl et al. 2007), e.g. human consumption of
agricultural commodities. Agricultural production is sug-
gested to grow by 60–100% in the next four decades
(Krausmann et al. 2013), outlining the importance of
photosynthesis and ensuing processes. For unabated
photosynthesis, optimal conditions are required which
nesium are essential mineral plant nutrients that criti-
cally contribute to the process of photosynthesis and the
subsequent long-distance transport of photoassimilates.
Among the mineral nutrients, nitrogen (N) is generally
required in the largest quantity by plants, followed by
potassium (K), phosphorus (P), calcium (Ca) and magne-
sium (Mg). Plants take up both mineral Mg and K only
in the cationic form (as Mg2+ and K+ ). High K concen-
trations in the soil solution inhibit Mg uptake and may
induce Mg deficiency in plants (Salmon 1963, Heenan
and Campbell 1981).
Within plants, most metabolically active Mg is bound
or incorporated into cellular compartments (Waters
2011), with highest concentrations in chloroplasts (Kar-
ley and White 2009). A significant share of Mg in leaves
is bound as the central atom in the tetrapyrrole ring of
chlorophyll a and b molecules, which are the major

Abbreviations – APX, ascorbate peroxidase; GR, glutathione reductase; LHCII, light harvesting complex II; NPQ,
non-photochemical quenching; PPFD, photosynthetic photon flux density; PS, photosystem; Rca, Rubisco activase; ROS,
reactive oxygen species; RuBP, ribulose-1,5-bisphosphate; SLM, specific leaf mass; SOD, Fe- and CuZn-superoxide dismutase.

414 © 2018 The Authors. Physiologia Plantarum published by John Wiley & Sons Ltd on behalf of Scandinavian Plant Physiology Society.
This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution
and reproduction in any medium, provided the original work is properly cited.
pigments for photosynthetic light absorption (Wilkinson
et al. 1990). In contrast, K is not part of organic macro-
molecules and exclusively present in its ionic form (K+ )
or in weak complexes from which it is easily exchanged
(Marschner 2012). In cells, K+ is present in two major
pools, the vacuole and the cytosol. In the latter, K+ is
the most abundant cation. K and Mg are both mutually
involved in a number of physiological processes, includ-
ing the activation of numerous enzymes and regulation
of the cation-anion balance (Marschner 2012). K+ serves
as the most important inorganic osmotic compound in
plant cells, and thus, sufficient K supply is crucial for
the regulation of turgor-driven processes like stomatal
movement (Fischer 1968) and cell elongation (Mengel
and Arneke 1982). K facilitates the diffusion of CO2 from
the atmosphere into chloroplasts (Jákli et al. 2017). K
and Mg are additionally involved into phloem-mediated
sucrose transport and the distribution of photoassimilates
within the plant.
Both K and Mg play prominent roles in processes that
are tightly associated with photosynthesis and photosyn-
thate translocation (Fig. 1). So far, the role of K and Mg
in photosynthesis and associated processes has not been
covered in a comprehensive review. Many reviews focus
on the movement of K or Mg within plants (Shaul 2002,
Gierth and Mäser 2007, Britto and Kronzucker 2008,
Szczerba et al. 2009), on the contribution of these ele-
ments (especially K) to stress alleviation (Cakmak 2005,
Wang et al. 2013) or, in somewhat broader approaches,
on their status in global agriculture (Römheld and Kirkby
2010, Cakmak 2013, Gransee and Führs 2013, Zörb
et al. 2014). Therefore, our main objective is to close this
gap by providing a comprehensive overview of the pro-
cesses that are affected, facilitated and regulated by Mg
and K in photosynthesis, photoassimilate translocation
and photoprotection.
We will first highlight the role of Mg and K in the
light-independent and light-dependent photosynthetic
processes including (1) CO2 diffusion through the leaf
boundary layer, stomata and mesophyll, (2) chloro-
plast ultrastructure, (3) chlorophyll synthesis and (4)
Rubisco activation and activity (Fig. 1A–D). Then, we
will evaluate the role of Mg and K in photoassimilate
translocation (Fig. 1E). Finally, we will highlight pho-
toprotective responses, including non-photochemical
quenching (NPQ), scavenging of reactive oxygen species
(ROS), photorespiration, chloroplast movement and leaf
movement.
K and Mg involvement in photosynthesis
Rates of photosynthetic CO2 assimilation are stable over
a broad range of K and Mg concentrations within leaves.
Physiol. Plant. 163, 2018
However, it has long been recognized that adequate
K and Mg nutrition is required to maintain the pho-
tosynthetic activity of crops (e.g. Cooper et al. 1966,
Terry and Ulrich 1973, Peoples and Koch 1979). Below
a certain threshold of leaf K, assimilation rates drop
drastically. The tissue K concentration that is critical
for photosynthetic functioning of crops (i.e. the tissue
K concentration where net assimilation is 95% of its
maximum under experimental conditions) is reported
between 12.5 and 14.0 mg K g−1 dry matter in oilseed
rape (Lu et al. 2016a), 13.0 mg g−1 in soybean (Singh and
Reddy 2017), 22.3 mg g−1 in sunflower (Jákli et al. 2017)
and 26.0 mg g−1 in cotton (Gerardeaux et al. 2010) (crit-
ical values for Singh and Reddy (2017), Jákli et al. (2017)
and Gerardeaux et al. (2010) are calculated from the
model equations presented in the respective publications
describing the relationship between leaf K concentration
and net assimilation). Critical leaf Mg concentrations for
photosynthesis have not been reported, but concentra-
tions of 0.7 mg g−1 leaf dry matter may be required to
achieve 90% of maximum yield (Smith et al. 1985).
Restrictions in CO2 diffusion
In the light-independent photosynthetic reactions atmo-
spheric CO2 is fixed via enzymatic carboxylation. The
rate of CO2 fixation during this process not only depends
on bio- and photochemical processes, but also on the
quantity of CO2 that is available for Rubisco in the
chloroplast stroma. A number of resistances restrict
the diffusion of CO2 from the atmosphere into the
leaf-internal airspace and further through cell wall,
plasma membrane, cytosol, chloroplast envelope and
stroma (Fig. 1A).
Boundary layer diffusion
The first resistance against CO2 movement from the
atmosphere towards the leaf surface is posed by the leaf
boundary layer. In this thin layer adjacent to the leaf
surface, turbulent exchange is suppressed and the trans-
fer of molecules is characterized by diffusion (Schuepp
1993). The thickness of the boundary layer, and thus its
conductivity to CO2 diffusion, is determined by the leaf
energy balance (Woodrow et al. 1990) rather than by
biochemical parameters and is hence not likely to be
directly influenced by leaf nutrient status. Therefore, it
has been largely neglected in studies of nutrient effects
on CO2 exchange. However, due to its osmotic proper-
ties, K deficiency causes a loss of turgor potential (Carroll
et al. 1994), and this can substantially affect leaf inclina-
tion of plants. Boundary layer conductance is a function
of both radiation interception and wind speed (Martin
et al. 1999). A change in average leaf inclination under
415
Fig. 1. Localization of anatomical, physiological and biochemical responses in plants to potassium and magnesium deficiency that are related to
photosynthesis and photoassimilate translocation. 1) K deficiency alters leaf anatomy, and thus, mesophyll diffusion of CO2 . 2) Both K and Mg
deficiencies alter the ultrastructure of chloroplasts. 3) Mg is the central atom of the chlorophyll pigment and also required for its biosynthesis.
4) Both K and Mg reduce Rubisco quantity and activity and Mg additionally functions in Rubisco activation. 5) K and Mg are required for source – sink
translocation of photoassimilates, as they have important functions in apoplastic phloem loading of sucrose.

conditions of K deficiency may therefore substantially
affect boundary layer properties and thus change its con-
ductivity to molecular diffusion, with effects on pho-
tosynthesis, transpiration and water-use efficiency (Col-
latz et al. 1991, Schuepp 1993, Bridge et al. 2013). This
effect appears to be unique to K deficiency and is not
likely to result from a deficiency of Mg, as Mg does
not contribute to osmoregulation. We are, however, not
aware of any study directly relating K or Mg nutrition
to boundary layer conductance, but its general concept
should be considered when transferring results from leaf
chamber measurements – where boundary layer effects
are largely avoided by strong air mixing – to the field.
Stomatal conductance
CO2 enters the leaf through the stomatal pores. Their
aperture is mediated by the stomatal guard cells, which
pose the first actively regulated resistance to the move-
ment of CO2 into leaves. The important role of K+ for the
regulation of stomatal guard cells and the efficiency of
stomatal movement is well documented (Fischer 1968,
Humble and Raschke 1971). K+ is the major inorganic
osmolyte, driving the changes in guard cell turgor that
are required for stomatal movement. Dynamic regula-
tion of stomatal aperture requires large quantities of K+
to be rapidly exchanged between apoplast, cytosol and
vacuoles of stomatal guard cells (Roelfsema and Hedrich
2002, Andrés et al. 2014). Transport of K+ through the
plasma membrane of stomatal guard cells is mediated
by voltage-gated inward-rectifying K+ channels, and is
accompanied by influx of counter-ions (NO3 − , Cl− ) and
synthesis of malate in the cytosol. Increased concentra-
tions of ions decrease the guard cell water potential and
cause an influx of water. As a result, guard cell volume
increases and the stomata open.

416 Physiol. Plant. 163, 2018

 Due to the osmotic role of K in guard cell regula-
tion, it is not surprising that stomatal conductance is
frequently reported to decrease under K-deficient condi-
tions (e.g. Terry and Ulrich 1973, Zhao et al. 2001, Jákli
et al. 2017). Nevertheless, and regardless of the impor-
tance of K+ in guard cell regulation, changes in stomatal
conductance do not limit photosynthesis predominantly,
even when total leaf K concentrations are below the criti-
cal level for photosynthesis (Sen Gupta et al. 1989, Zhao
et al. 2001, Jin et al. 2011). The contribution of stomatal
limitations to the total limitation of photosynthesis was
estimated at about 15% in sunflower (Jákli et al. 2017)
and did not increase even under severe K deficiency. The
fraction of stomatal limitation even decreased from 55
and 50% to 36 and 20%, respectively, in two varieties of
K-deficient oilseed rape (Lu et al. 2016a).
There is evidence that the velocity with which stom-
ata react to environmental or biochemical feedbacks is
diminished in K-deficient alfalfa (Lindhauer 1983) and
olive tree (Erel et al. 2013). Erel et al. (2013) suggested
that a functional substitution of K+ by Na+ might be
responsible for alternations in the velocity of stomatal
movement in olive, since the transport of Na+ through
cell membranes is slow compared to the transport of K+ .
Some reports indicate that under combined K defi-
ciency and water-limitation, stomatal control may
be lost in perlite-grown sunflower and olive plants,
resulting in an inhibition of drought-induced stom-
atal closure (Fournier et al. 2005, Arquero et al. 2006,
Benlloch-González et al. 2008, 2010). In accordance
with the general concept, the authors do not attribute
their results to a loss of osmotic stomatal control, but to
an inhibition of the ABA signaling pathway by excessive
ethylene production in the leaves. These results are not
supported by findings of Jákli et al. (2017), who report
decreased rates of stomatal conductance in K-deprived
and PEG-stressed sunflower grown in nutrient solution,
and Erel et al. (2013), who did not find any effect of K
deficiency on stomatal conductance in drought stressed,
perlite-grown olive.
The origin of this contradiction remains specula-
tive, and the interaction effect of K deficiency and
water-limitation is still debated. For well-watered con-
ditions, the general consensus remains that stomatal
functioning is well maintained even when leaf K concen-
trations are below the critical values for photosynthesis.
Jákli et al. (2017) suggested that the reduction of stomatal
conductance under K-deficient conditions is a reaction
to low rates of CO2 assimilation in order to maximize
water-use efficiency.
In contrast to K, Mg has no active function in stomatal
control. Therefore, the causality suggested by Sun et al.
(2001) – who attributed decreased CO2 assimilation in
Physiol. Plant. 163, 2018
Mg-deficient Pinus radiata to reduced stomatal conduc-
tance – appears quite unlikely. The decline in net assimi-
lation that is commonly observed under Mg deficiency is
rather caused by non-stomatal factors. This assumption is
supported by numerous studies reporting no effect of Mg
deficiency on stomatal conductance or leaf-internal CO2
concentrations (e.g. Lasa et al. 2000, Tang et al. 2012,
Yang et al. 2012). However, unlike for K (Lu et al. 2016a,
2016b, Jákli et al. 2017), a quantitative analysis of photo-
synthetic limitations in Mg-deficient plants has not been
published so far.
Mesophyll conductance
After entering the leaf through the stomatal pore, a
series of resistances further object the movement of
CO2 through the leaf mesophyll and therefore affect the
CO2 concentration in chloroplasts. These resistances are
aggregated as (their inverse) ‘mesophyll conductance’ to
CO2 diffusion and are summarized in a recent review by
Berghuijs et al. (2016). After diffusion through the leaf
internal air space, CO2 dissolves in the apoplastic water
of the cell walls. Once in the liquid phase, CO2 is present
as either dissolved CO2 or HCO3 − and further diffuses
through the pores of the cell wall, the plasma membrane,
the cytosol, the chloroplast envelope and the chloroplast
stroma, where enzymatic CO2 fixation is taking place.
There is common agreement that mesophyll conduc-
tance is reduced under low K supply, which is most
commonly associated with leaf anatomical changes.
Limitations to photosynthesis that originate from
restricted CO2 diffusion are attributable to mesophyll
rather than stomatal conductance (e.g. Terry and Ulrich
1973, Jin et al. 2011, Battie-Laclau et al. 2014). Jákli
et al. (2017) reported that the fraction of total photosyn-
thesis limitation that results from mesophyll conductance
increased from 45 to 64% in non-symptomatic leaf area
of K-deficient sunflower compared to K-sufficient plants,
and Lu et al. (2016a) showed an increase of mesophyll
limitation from 28 to 50% in K-inefficient oilseed rape
under low K supply. They did, however, not find a sig-
nificant effect of K deficiency on mesophyll limitations
in a K-efficient variety of oilseed rape. Battie-Laclau
et al. (2014) could likewise not show an effect of K
deficiency on mesophyll limitations in eucalyptus,
although absolute values of mesophyll conductance
declined, indicating species- and even variety-specific
co-regulation between mesophyll- and biochemical
limitations of photosynthesis.
Many variables affect the diffusion of CO2 inside
leaves. Gaseous diffusion is largely determined by leaf
anatomical properties such as leaf thickness and the
volume ratio of leaf-internal airspace to mesophyll cells,
417
which both affect the specific leaf mass (SLM). Numer-
ous studies show that deficient K supply significantly
increases SLM, (O’Toole et al. 1980, Cakmak et al.
1994b, Pettigrew 1999, Gerardeaux et al. 2010, Jin
et al. 2011, Lu et al. 2016b). SLM of K-deficient leaves
are enhanced by decreased leaf thickness (O’Toole
et al. 1980, Battie-Laclau et al. 2014) and reduced
leaf-internal airspace (Zhao et al. 2001, Battie-Laclau
et al. 2014). Moreover, K is an osmotic driver of cell
extension and K deficiency results in smaller mesophyll
cells (Mengel and Arneke 1982, Claussen et al. 1997).
Decreased leaf thickness, leaf-internal airspace and cell
size reduce the chloroplast surface area exposed to the
leaf-internal airspace (Giuliani et al. 2013) and, thus,
mesophyll conductance. In addition, Lu et al. (2016b)
observed a greater distance between chloroplasts and
cell walls in K deficient Brassica napus, increasing the
overall pathway length for liquid phase CO2 diffusion
and, thus, mesophyll conductance.
Besides being affected by anatomical properties, an
increase in SLM can also be attributed to an increase
in non-structural carbohydrates within K-deficient leaves
(Cakmak et al. 1994b, Gerardeaux et al. 2010). Ger-
ardeaux et al. (2010) report that 15% of the SLM increase
under K deficiency was attributed to an increase in solu-
ble sugar concentrations. Based on purely physical stud-
ies by Carroll et al. (2014), Hölttä et al. (2017) suggested
that an increase in sugar concentration could decrease
the rate of liquid phase CO2 diffusion. Increased concen-
trations of sugars in the liquid phase of the leaf mesophyll
might therefore contribute to the reduction of mesophyll
conductance under K deficiency.
Mesophyll conductance is not only sensitive to leaf
anatomical traits and solute concentrations, but might
additionally be affected by the expression of proteins
such as aquaporins that facilitate leaf-internal CO2 diffu-
sion. Kanai et al. (2011) demonstrated the importance of
adequate K nutrition for the functioning of aquaporins for
water uptake and transport. There is strong evidence that
the transport of not only water but also of CO2 through
plasma- and chloroplast-membranes is substantially sup-
ported by aquaporins, and it is reported that decreased
expression of the tobacco aquaporin NtAQP1 can cause
a 20% reduction in mesophyll conductance (Flexas et al.
2006, Uehlein et al. 2008). Although direct experimen-
tal evidence is still missing, an involvement of aquaporin
activity in the overall decrease of mesophyll conduc-
tance under K deficiency is possible.
Furthermore, CO2 diffusion through the cytosol and
the chloroplast stroma is likely to be facilitated by the
activity of carbonic anhydrases, a group of enzymes that
catalyze the interconversion between CO2 and HCO3 −
and might therefore increase the rate of CO2 delivery
418
to Rubisco (Berghuijs et al. 2017). Increased leaf K con-
centrations enhanced the activity of carbonic anhydrases
in leaves of Brassica juncea (Mohammad and Naseem
2006), but a general evidence for the linkage between
carbonic anhydrase activity and mesophyll conductance
under K-deficient conditions is missing so far.
To summarize the effect of K deficiency on mesophyll
conductance, we conclude that a decrease in photo-
synthesis under K deficiency can be largely attributed
to an increase in leaf internal CO2 -transfer resistance,
resulting in low mesophyll conductance. Increased sugar
concentrations and SLM most likely contribute to the
overall decline in mesophyll conductance. A reduction
in chloroplast surface area exposed to the leaf-internal
airspace and increased intracellular pathway length for
liquid phase diffusion seem to be the most important fac-
tors limiting CO2 mesophyll diffusion. The contribution
of the different traits to the overall reduction of meso-
phyll conductance is highly species-specific (Tomás et al.
2013) and can also vary between varieties of the same
species (Lu et al. 2016a, 2016b).
In contrast to K, no study exists on the relation between
Mg nutrition and mesophyll conductance. We can hence
only speculate on possible effects of Mg on the dif-
fusion of CO2 through the leaf mesophyll. Similar to
K deficiency, increased SLM is reported for leaves of
Mg-deficient plants (Cakmak et al. 1994b, Li et al. 2017),
which is attributed to an accumulation of soluble car-
bohydrates as a consequence of impaired phloem load-
ing (e.g. Cakmak et al. 1994b, Lavon et al. 1995). As
discussed above, increased concentrations of sugars in
the liquid phase of the leaf mesophyll might affect its
conductivity to CO2 diffusion. However, as mentioned
previously, a systematic limitations analysis is needed to
quantify the contribution of stomatal and mesophyll lim-
itations to photosynthesis of Mg-deficient plants.
Chloroplast ultrastructure
The ultrastructure of chloroplasts is formed by the organi-
zation of the internal membrane system. Part of the mem-
branes stack up into cylindrical structures, which form
the so-called grana, while part of the membranes remains
unstacked, the stroma lamellae. K+ and Mg2+ both
facilitate a well-structured organization of grana and
stroma lamellae, therefore support chloroplast integrity,
the efficiency of light absorption, Rubisco diffusion and,
as a consequence, carbon assimilation. Under Mg and
K deficiency damage of chloroplast ultrastructure was
observed as such that the lamella structure was irreg-
ular, loose and partly dispersed in the cytoplasm and
the amount of grana and lamellae was reduced (Hall
et al. 1972, Zhao et al. 2001, Jia et al. 2008). In contrast,
Physiol. Plant. 163, 2018
increasing Mg concentrations resulted in many distin-
guished stacked membranes (Rumak et al. 2010). Grana
stacking mainly depend on van der Waals attraction
forces and electrostatic repulsion (Puthiyaveetil et al.
2017). Electrostatic repulsion is controlled by mem-
brane surface charges and the ion concentrations in the
milieu surrounding the thylakoid membranes. Screen-
ing of net negative surface charges by K+ as a mono-
valent cation, and more efficiently Mg2+ as a diva-
lent cation, reduces the electrostatic repulsion force.
Puthiyaveetil et al. (2017) showed that at low K+ activ-
ities, stacking is hindered because repulsive forces dom-
inate. In contrast, at high K+ and Mg2+ concentrations
(>100 mM K+ and 5 mM Mg2+ ) grana stacking was well
developed. Furthermore, it is suggested that changes
in the lateral micro-organization of LHCIIs and subse-
quent segregation of the two photosystems (PSs) occurs
at low Mg2+ concentrations (Stys 1995, Stoitchkova et al.
2006). However, grana stacking require higher Mg2+
concentrations than the segregation of PSs (Stoitchkova
et al. 2006).
Grana formation enhances the stromal volume,
thus generates more space for free diffusion of macro-
molecules in the densely crowded stroma (Anderson
et al. 2008). Enhancement of stromal volume might alle-
viate macromolecular crowding and thus, aid diffusion
of Rubisco and facilitate high rates of carbon fixation
(Anderson et al. 2008).
Chlorophyll
Chlorophyll a and b are the major pigments for the
absorption of light energy and synthesis of both pigments
requires Mg. A common response to Mg deficiency is
the reduction of chlorophyll concentrations as demon-
strated in numerous studies (Mengutay et al. 2013, Faust
and Schubert 2016, Tränkner et al. 2016). However, con-
sidering chlorophyll a and b separately, the response is
not uniform. In sugar beet, chlorophyll a and b concen-
trations decreased under Mg deficiency (Hermans et al.
2004). In coffee, the response is cultivar specific as there
were no changes in the chlorophyll a/b ratio in cv. Catuaí
(Da Silva et al. 2014) whereas in cv. Acaiá chlorophyll
a/b concentrations fluctuated over the experimental time
without clear correlation with the Mg deficiency.
Biosynthesis of chlorophyll starts with the insertion of
Mg into protoporphyrin IX (Fig. 1C). The insertion of Mg
is catalyzed by Mg-chelatase, an enzyme consisting of
40, 70 and 140-kDa subunits, designated ChlI, ChlD and
ChlH subunits, respectively. For the insertion of Mg into
protoporphyrin IX, the catalytic cycle of Mg-chelatase
undergoes two steps (Masuda 2008). The first step is
the activation step where the subunits I and D form a
Physiol. Plant. 163, 2018
complex with ATP and Mg2+ . The subunit H binds to
protoporphyrin IX and Mg2+ , and presumably contains
the active site for chelation. The second step includes the
Mg chelation into protoporphyrin IX that requires ATP
hydrolysis. In vitro studies demonstrated that chelation
of 1 magnesium requires hydrolysis of 15 ATP, making
Mg chelation an expensive reaction coupled to ATP
hydrolysis (Reid and Hunter 2004). The activity of Mg
chelatase is sensitive to free Mg concentrations and
thus, depends on diurnal cycling. When illuminated, the
free Mg concentrations in the chloroplast stroma can
increase up to 6 mM allowing a flux into the chlorophyll
biosynthetic pathway (Reid and Hunter 2004). Vicia faba
plants grown under Mg-deficient conditions showed a
decrease in the transcript abundance of Mg chelatase
subunit H even in tissues where the Mg concentrations
did not fall below the critical level (Neuhaus et al. 2013).
Hence, analysis of Mg chelatase H transcript abundance
might function as an early indicator for Mg deficiency.
The biosynthesis of chlorophyll primarily generates
chlorophyll a. Part of the chlorophyll a is oxidized to
chlorophyll b by chlorophyllide a oxygenase, but chloro-
phyll b can be reduced back to chlorophyll a. For chloro-
phyll degradation, chlorophyll b must be first converted
to chlorophyll a as chlorophyll b derivatives are not cat-
alyzed in the subsequent pathway. Thus, the ratio of
both pigments is tightly regulated by the interconversion
of chlorophyll a and b (chlorophyll cycle) (Blankenship
2014, Sato et al. 2014). Chlorophyll a and b are related
to the stability of the light harvesting complex II (LHCII)
and chlorophyll b is crucial for LHCII accumulation (Sato
et al. 2015). Degradation of chlorophyll b triggers degra-
dation of LHCII and thus participates in the regulation of
the plant light-harvesting capacity and the suppression of
photodamage. It also promotes nutrient remobilization
as LHCII is a highly abundant protein in the chloroplast
and serves as a reservoir of nutrients under deficiency
(Sato et al. 2015). Thus, chlorophyll degradation under
Mg deficiency can function to release Mg and to protect
cells from photodamage by triggering LHCII degradation.
Similarly, the total concentration of chlorophyll has
been frequently reported to decrease under K deficiency
(Longstreth and Nobel 1980, Bednarz and Oosterhuis
1999, Zhao et al. 2001, Lu et al. 2016b). It has been
suggested, however, that chlorophyll degeneration is not
a primary effect of K deficiency, but is rather attributed
to an excessive production of ROS (Cakmak 2005) that
will be referred to later in the text.
Rubisco activation and activity
Magnesium is crucial for CO2 fixation as it is directly
involved in the activation and activity of Rubisco.
419
Furthermore, Mg is crucial for protein synthesis, which
affects Rubisco protein abundance and thereby, indi-
rectly influences CO2 fixation. Under Mg deficiency,
protein concentrations were shown to be reduced in
sugar beet (Faust and Schubert 2016), wheat (Mengutay
et al. 2013) and maize (Mengutay et al. 2013). Lower
protein concentrations under Mg deficiency might be
due to the involvement of Mg ions in ribosomal sub-
unit association and activity (Yamamoto et al. 2010).
Furthermore, Mg is suggested to control the structural
flexibility of numerous ribosomal proteins (Yamamoto
et al. 2010). More than 100 magnesium ions are associ-
ated with the large ribosomal subunit (Petrov et al. 2012)
and part of the Mg ions form magnesium microcluster,
which contain two tightly associated Mg ions. Magne-
sium microclusters are suggested to provide structural
integrity to the large ribosomal subunit and assist in
maintaining the compact native structure of the assem-
bly (Petrov et al. 2012). The most abundant protein on
earth is Rubisco, and about 30% of the total protein
in a plant leaf (Jensen 2000) and approximately 40%
of all stromal proteins is Rubisco (Hazra et al. 2015).
By proteomic analysis, Peng et al. (2015) showed that
the protein abundance of Rubisco and Rubisco activase
(Rca) was decreased under Mg deficiency in Citrus
sinensis, indicating that Rubisco quantity and activity
are affected which agreed with an 88% reduction of
assimilation rates in Mg-deficient leaves. However, the
CO2 fixation is rather controlled by the amount of active
Rubisco, than by the total amount of Rubisco protein
(Taylor and Andersson 1996).
Rubisco activity is commonly measured in in vitro
assays, whereas in vivo determination of CO2 assimi-
lation rates can serve as a measure for Rubisco activ-
ity. Numerous studies show decreased Rubisco activity
or CO2 assimilation rates under Mg deficiency in vari-
ous plant species such as spinach (Yuguan et al. 2009),
citrus (Tang et al. 2012, Li et al. 2017), maize (Jezek
et al. 2015), sunflower (Lasa et al. 2000) and P. radi-
ata (Laing et al. 2000, Sun et al. 2001). The Rubisco
activity is sensitive to the Mg status as observed by
a decline in CO2 assimilation rates in Mg-deficient
sugar beet and barley already 7 and 8 days, respectively,
after onset of Mg deficiency in nutrient solution trials
(Terry and Ulrich 1974, Tränkner et al. 2016). Rubisco
catalyzes the carboxylation and/or the oxygenation of
ribulose-1,5-bisphosphate (RuBP) and thereby initiates
the sugar producing or photorespiratory pathway. To
exhibit catalytic activity, a lysine residue in the active
site of the enzyme has to be carbamylated by an acti-
vator, non-substrate CO2 molecule and the labile carba-
mate group is subsequently stabilized by an Mg ion prior
to binding of the substrate RuBP (Taylor and Andersson
420
1997, Portis 2003). However, the loss of the activator
CO2 and Mg ion can lead to tight binding of the sub-
strate RuBP or other sugar phosphates without prior car-
bamylation, inhibiting its activity (Taylor and Andersson
1997). Kim and Portis (2006) show that low Mg con-
centrations increased dramatically the rate of deactiva-
tion of Rubisco and relate this to decarbamylation of
active sites and stronger binding of RuBP to the uncar-
bamylated form of Rubisco. The release of the bound
RuBP and other sugar phosphates is achieved by the
catalytic chaperone Rca (Kuriata et al. 2014). Rca has
a hydrolytic ATPase activity, which is required for the
Rubisco activating activity. When Mg was absent from
the assay medium, enzymatic turnover was abolished
in isolated tobacco Rca (Hazra et al. 2015). Similarly,
the Rca activity was decreased in Mg deficient spinach
(Yuguan et al. 2009). Hazra et al. (2015) suggest that
a second protein-based magnesium-binding site exists
which serves as a co-activator by mediating contact
between the subunits. Thus, both Mg coordinated with
ATP and Mg for promoting subunit assembly is required
and the fully activated complex is best represented by
Rca•Mg•ATP•Mg (Hazra et al. 2015). The catalytic acti-
vation of Rca is Mg specific, as a replacement of Mg2+
by Mn2+ resulted in a 32-fold decrease in turnover rates.
High-cytosolic sucrose concentrations in Mg deficient
leaves, which is a common phenomenon under Mg
deficiency, resulting from reduced rates of phloem export
(Cakmak et al. 1994a), are also supposed to repress the
expression of genes involved in photosynthesis (Neales
and Incoll 1968, Jang and Sheen 1994, Sheen 1994).
Likewise, K deficiency reduces Rubisco carboxylation
activity in chloroplasts. This was shown by in-vitro mea-
surements (Weng et al. 2007, Hu et al. 2015, Zahoor
et al. 2017) as well as by estimations of the maximum
Rubisco carboxylation velocity, Vc,max , from combined
measurements of leaf gas exchange and chlorophyll flu-
orescence (Jin et al. 2011, Battie-Laclau et al. 2014, Erel
et al. 2015, Jákli et al. 2017). It is sometimes stated that
K deficiency inhibits the activation of Rubisco (Oost-
erhuis et al. 2013), resulting in reduced rates of RuBP
carboxylation. In an early report on the subject, Peo-
ples and Koch (1979) clearly state that, in a purified
Rubisco extract of K-deficient and K-sufficient alfalfa, the
‘specific activity of RuBPc (=RuBP-carboxylase) isolated
from severely K-deficient and K-sufficient leaflets was not
significantly different, suggesting that K does not function
in RuBPc activity’. In contrast, when measuring carboxy-
lation activity in a crude extract, the authors found sig-
nificantly increased activity of Rubisco extracted from K
sufficient leaves. They came to the conclusion that the
biosynthesis of Rubisco was markedly suppressed under
deficient K supply. This was again shown in cucumber
Physiol. Plant. 163, 2018
cotyledons (Ohya et al. 1986). Generally, protein syn-
thesis appears to be sensitive not only to Mg but also
to K deficiency, because K+ is involved in ribosomal
translation (Nissen 2000, Austin and First 2002). Hence,
the concentration of soluble proteins in plant tissues is
reduced under K deficiency, whereas the concentration
of free amino acids increases (Besford 1975, Cakmak
et al. 1994a, Li et al. 1997, Faust and Schubert 2016).
As a consequence, the quantity of Rubisco is reduced
in K-deficient leaves. Lower Rubisco content (on a leaf
area basis) was also shown in K-deficient soybean leaves
(Wang et al. 2015), but neither total soluble protein
nor Rubisco content was affected by K status in citrus
leaves (Lavon et al. 1999). The authors, however, report
higher total amino acid content and Rubisco carboxy-
lation activity. Nonetheless, the effect of K on quantita-
tive Rubisco characteristics appears to be dependent on
the species under study and the respective growth stage
(Osaki et al. 1993).
Apart from Rubisco quantity, K supply can indirectly
affect Rubisco activity. Optimum chloroplastic K+ con-
centrations (i.e. in the range of cytosolic K+ concentra-
tions around 100 mM) induce a broader range of pH opti-
mum for Rubisco functioning than under K deficiency
(Mengel and Kirkby 2001). Furthermore, downregula-
tion of Rubisco activity may occur under low chloro-
plastic CO2 concentrations (Galmés et al. 2011), which
is a result of reduced CO2 transfer rates in K-deficient
mesophyll tissues (Jákli et al. 2017). Comparable to
Mg deficiency, reduced rates of phloem export result
in high-cytosolic sucrose concentrations (Cakmak et al.
1994a) that can cause feedback inhibition of Rubisco
activity (Goldschmidt and Huber 1992).
Additionally, Jin et al. (2011), Battie-Laclau et al.
(2014) and Erel et al. (2015) report reduced maximum
electron transport rates (Jmax ) through PSs of K-deficient
hickory, eucalyptus and olive leaves, respectively. Jmax
is associated with the ATP- and NADPH-consuming
RuBP regeneration (Farquhar et al. 1980), implying less
acceptor molecules for CO2 fixation.
To summarize, there is no evidence that K+ is involved
in Rubisco activation, but rather regulates Rubisco activ-
ity by affecting its quantity, its pH-optimum and substrate
(CO2 and possibly RuBP) availability.
K and Mg involvement
in photoassimilate translocation
Plant growth and metabolism require the translocation
of carbohydrates from photosynthetically active tissues
into sink organs such as roots, flowers and seeds. Load-
ing of sucrose − the major transport form of carbo-
hydrates in plants − into the phloem is substantially
Physiol. Plant. 163, 2018
affected by K and Mg nutrition (Fig. 1E) and a shortage
of either of these elements may substantially affect the
efficiency of the long-distance carbon transport within
plants. According to the pressure flow hypothesis ini-
tially developed by Münch (1930), the movement of
solutes in the phloem follows a hydrostatic pressure gra-
dient that originates from differences in solute concen-
trations. K+ is the most abundant cation in the phloem
and, together with sucrose and amino-N compounds, is
the most important osmotic compound of the phloem
sap. It therefore contributes to the rate of phloem trans-
port (Lalonde et al. 2003), and K+ concentration within
the phloem sap of Ricinus communis was positively cor-
related with the level of external K supply (Mengel and
Haeder 1977).
In apoplastic phloem loading, sucrose has to be
actively transported against its concentration gradient
across the plasma membranes of phloem companion
cells and sieve elements by sucrose transporters. The
necessary energy is generated by H+ -ATPases, which
create a proton gradient across the plasma membrane
(Michelet and Boutry 1995). Low cellular Mg concen-
trations can result in dissociation of the Mg•ATP com-
plex and in a decreased activity of plasma membrane
H+ -ATPases (Hanstein et al. 2011). As a consequence,
the transmembrane proton gradient cannot be estab-
lished, the rate of phloem export declines and sucrose
accumulates in the leaf tissue.
Besides Mg, K is crucially involved in sucrose load-
ing. A study on Arabidopsis akt2/3-1 knockout mutants
revealed that the transmembrane potential established
by H+ -ATPases is regulated by the inward-rectifying
AKT2/3 potassium channel (Deeken et al. 2002). AKT2/3
therefore contributes to the basic loading and unload-
ing of sucrose into and from the phloem. By multiple
post-translational modification steps it can be converted
to a non-rectifying channel, which facilitates a rapid
efflux of K+ from the sieve element/companion cells
complex (Gajdanowicz et al. 2011, Sandmann et al.
2011). The established K+ gradient provides energy that
is used by other transporters for phloem loading. This
mechanism, the so-called ‘potassium battery’, serves as
a mobile energy source to overcome local ATP-shortages
and maintain the efficiency of the long-distance transport
system (Gajdanowicz et al. 2011, Dreyer et al. 2017).
An impaired source-to-sink carbon allocation under
Mg deficiency was shown in numerous plants such as
sugar beet (Hermans et al. 2005), maize (Mengutay et al.
2013), bean (Cakmak et al. 1994a) and soybean (Yang
et al. 2017). Besides sucrose, starch can accumulate in
the chloroplast under Mg deficiency (Lavon et al. 1995,
Ceylan et al. 2016, Yang et al. 2017). The molecular
regulation underlying carbon acumulation under Mg
421
deficiency is still ambiguous. In sugar beet, the transcript
abundance of the specific H+ /sucrose symporter BvSUT1
was higher in Mg-deficient leaves, but sucrose contents
were increased (Hermans et al. 2005). In V. faba, the
transcript abundance of plasma membrane H+ -ATPase
isoforms was decreased when plants were gown under
Mg-deficient conditions (Neuhaus et al. 2013). How-
ever, this was not the case for all examined isoforms.
One isoform showed slightly increased transcript abun-
dance under Mg deficiency and another isoform could
only be found in the Mg-deficient treatment and was
absent under control Mg supply (Neuhaus et al. 2013).
Similar to Mg, a shift in the partitioning of assimilates
–with increased concentrations of carbohydrates in pri-
mary leaves and reduced concentrations in roots – as
well as reduced rate of phloem export of sucrose were
observed in K-deficient Phaseolus vulgaris (Cakmak et al.
1994a, 1994b). Likewise, sucrose concentration was
increased in functional leaves of K-deficient cotton (Bed-
narz and Oosterhuis 1999, Hu et al. 2015, Zahoor et al.
2017).
These studies clearly show the strong influence of Mg
and K on carbon assimilation and allocation. However, it
remains ambiguous how Mg and K status, carbohydrate
accumulation and carbohydrate-triggered feedback on
photosynthesis in physiological and molecular aspects
are linked.
K and Mg involvement in photoprotection
As outlined in the previous paragraphs, K and Mg affect
the photosynthetic capacity and a deficiency of either
one of the two nutrients decreases CO2 assimilation
(Fig. 2). Under this limitation of photosynthetic capacity,
the absorbed light energy is in excess to what can be used
in photosynthesis processes, leading to an enhanced
production of ROS and plants suffer oxidative stress
(Nishiyama et al. 2006, Takahashi and Badger 2011).
ROS inhibit the repair of photodamaged PSII, predom-
inantly the D1 protein in the reaction center of PSII,
causing photoinhibition (Takahashi and Badger 2011,
Järvi et al. 2013). Photoinhibition can be indicated by the
chlorophyll fluorescence parameter Fv /Fm (Niyogi 1999),
which describes the maximum efficiency at which light
absorbed by PSII is used for the reduction of QA , the
primary quinone electron acceptor in PSII (Baker 2008).
Mg- and K-deficiency induce non-uniform responses in
Fv /Fm . In Mg-deficient Citrus and sugar beet, Fv /Fm was
decreased (Hermans et al. 2004, Tang et al. 2012, Yang
et al. 2012) whereas in Mg-deficient sunflower and Sulla
carnosa, Fv /Fm was unaffected (Lasa et al. 2000, Farhat
et al. 2015). Changes in Fv /Fm under Mg-deficiency were
related to damage of the oxygen-evolving complex on
422
PSII or to an accumulation of reduced QA (Yang et al.
2012). K deficiency induced a decrease of Fv /Fm in
two cotton cultivars (Wang et al. 2012), in rice (Jia
et al. 2008), olive (Erel et al. 2015) and in maize (Qu
et al. 2013), whereas in Norway spruce and sunflower a
decrease in Fv /Fm was not observed (Barnes et al. 1995,
Jákli et al. 2017). Two soybean cultivars being tolerant
and sensitive to K deficiency, respectively, responded
differently to K deficiency: the tolerant cultivar did not
show altered Fv /Fm values, whereas the sensitive culti-
var showed a significant decrease of Fv /Fm (Wang et al.
2015). In conclusion, Mg- and K-deficiency do not com-
monly induce photoinhibition, which might depend on
the magnitude of deficiency of Mg and K in the leaf tis-
sue, cultivar specific responses and environmental and
experimental conditions.
ROS scavenging
The ROS species that are produced in the thylakoid have
to be immediately detoxified before they diffuse from
their generation site and damage targeted molecules
(Asada 2006). Detoxification in the chloroplast is
achieved by antioxidants such as ascorbate peroxidase
(APX), Fe- and CuZn-superoxide dismutase (SOD) and
glutathione reductase (GR). The interplay between ROS
formation and ROS detoxification is strictly controlled
and necessary for unrestricted photochemistry. Mg- and
K-deficiency induce commonly elevated ROS levels and
enhanced ROS-detoxifying enzyme activity. Under low
K and Mg supply, increased H2 O2 or O2 − concentra-
tions have been reported on numerous plants species
such as Arabidopsis, maize, rice, cotton and coffee
(Shin and Schachtman 2004, Weng et al. 2007, Hu
et al. 2016, Da Silva et al. 2017). A K-inefficient cotton
cultivar increased O2 − and H2 O2 leaf concentrations,
and increased activities of SOD and APX, whereas a
K-efficient cotton cultivar only increased APX, but not
SOD activity, and neither H2 O2 nor O2 − concentrations
were affected (Wang et al. 2012). Özgür Uzİlday et al.
(2017) showed the clear impact of the Mg status on
ROS generation. When Mg was absent from the nutrient
solution or supplied only with 75 μM, the H2 O2 con-
centration in cotton leaves was increased by 29 and
33%, respectively, but when the Mg supply was raised to
150 μM, the H2 O2 concentration was increased by 13%.
Similarly, barley leaves suffering severe Mg deficiency
had up to 55% higher H2 O2 concentration compared
to control, though the activity of APX, GR and SOD
were substantially increased. Under mild deficiency, the
activity of APX, GR and SOD were still increased, but
the concentration of H2 O2 was decreased to the same
level as the control, indicating that under severe Mg
Physiol. Plant. 163, 2018
Fig. 2. Effects of potassium and magnesium deficiencies on processes related to photosynthesis, photoassimilate translocation and photoprotection.
Primary effects are direct anatomical, physiological or biochemical responses to K and/or Mg deficiency. Secondary effects are immediate consequences
following primary effects and eventually inhibit photosynthetic CO2 assimilation. Tertiary effects result from the inhibition of CO2 assimilation and are
only indirectly related to K and/or Mg deficiencies. Complex feedback loops and interactions exist. Leaf anatomy, photoassimilate translocation,
protein synthesis, Rubisco activity, chloroplast ultrastructure and chlorophyll synthesis and abundance are directly affected by Mg and/or K deficiency.
Altered leaf anatomy impedes CO2 diffusion through mesophyll, and thereby decreases the chloroplastic CO2 concentration, which in turn limits CO2
assimilation either directly, or indirectly by affecting Rubisco activity. Impaired photoassimilate translocation results in an accumulation of sucrose,
which directly affects Rubisco activity via feedback inhibition, and indirectly affects mesophyll CO2 diffusion. A decreased Rubisco activity eventually
limits CO2 assimilation. Disrupted chloroplast ultrastructure and low-chlorophyll abundance reduce the overall photosynthetic capacity, again inhibiting
assimilation. As a consequence, stomatal conductance is actively adjusted to low rates of CO2 assimilation in order to enhance photosynthetic water-use
efficiency. Low-photosynthetic capacity causes excessive ROS production and photo-oxidation of, e.g. chlorophyll. As a consequence, photoprotective
mechanisms are up-regulated.

deficiency the extent of H2 O2 production exceeded the Non-photochemical quenching

scavenging capacity (Tränkner et al. 2016).
In conclusion, K and Mg deficiencies induce oxidative
stress indicated by increased H2 O2 and O2 − levels, but
in response the antioxidant enzyme activity is enhanced,
which detoxifies part of the ROS. However, ROS cannot
always be decreased to levels comparable to levels in
unstressed plants, depending on the stress level induced
by K- and Mg-deficiency.
The non-photochemical dissipation of excess absorbed
light energy as heat, commonly determined as NPQ
which is located in LHCII antenna, is an important pho-
toprotective mechanism (Ruban 2016). Thermal energy
dissipation as a photoprotective mechanism can dissi-
pate up to 75% of absorbed light energy (Niyogi 1999).
Plants increase the dissipation of energy as heat in
response to Mg and K deficiency in order to protect

Physiol. Plant. 163, 2018 423

the PS from damage and to maintain photosynthetic
performance. In three Citrus cultivars subjected to Mg
deficiency (Tang et al. 2012, Yang et al. 2012), and two
rice cultivars (Jia et al. 2008) and sunflower subjected
to K deficiency (Jákli et al. 2017), NPQ was increased.
In contrast, in S. carnosa, NPQ was not affected even
when Mg was omitted from the nutrient solution (Farhat
et al. 2015). As Mg- and K-deficient plants have a lim-
ited capacity to convert light energy to chemical energy,
high-light intensities augment the formation of NPQ, as
shown in Mg-deficient P. radiata (Laing et al. 2000).
Photorespiration
Besides carboxylation, Rubisco catalyzes the oxygena-
tion of RuBP, resulting in photorespiration. Photorespira-
tion is considered an important photoprotective mech-
anism that can alleviate over-reduction of the electron
transport chain and thus helps to prevent photoinhi-
bition and excessive ROS formation (Lima Neto et al.
2017). In cotton, the response of photorespiration to
K deficiency was variety-specific and resulted in an
increase of photorespiration in the K-efficient var. Liao-
mian18, and a contrasting reduction of photorespiration
in the K-inefficient var. NuCOTN99 (Wang et al. 2012).
Absolute values of photorespiration also decreased in
K-deficient leaves of alfalfa (Peoples and Koch 1979).
Interestingly, photorespiration relatively increased from
26 to 34% of net assimilation, indicating a shift in the car-
boxylation/oxygenation specificity of Rubisco. A direct
involvement of K in photorespiration is questionable,
and alterations under K deficiency are most likely the
result of non-specific photoprotective reactions. How-
ever, photorespiration did not respond to light intensities
above 400 μmol m2 s−1 photosynthetic photon flux den-
sity (PPFD) in K-deficient olive, whereas it increased with
increasing PPFD in sufficiently supplied plants (Erel et al.
2015).
Chloroplast movement
Light harvesting complexes and PSs are located
in chloroplasts of mesophyll cells. Changes in the
arrangement and structure of chloroplasts affect light
harvesting and photosynthesis. The arrangement of
chloroplast in response to light intensities was suggested
by Kasahara et al. (2002) to function as a photoprotec-
tive mean, which was accepted in a review by Takahashi
and Badger (2011). At weak light intensities, chloro-
plasts accumulate at the cell wall in vertical direction
to the light in order to absorb weak light efficiently. At
strong light intensities, chloroplasts arrange at cell walls
in parallel direction to the light in order to minimize
the absorption of excessive light and to maximize the
424
absorption of CO2 from intercellular airspaces (Taka-
hashi and Badger 2011). In B. napus leaves, chloroplasts
responded to K deficiency by increasing their distance
from the cell wall (Lu et al. 2016b). Usually, chloroplasts
are allocated at the cell surface to absorb CO2 and
light. However, the study of Lu et al. (2016b) focuses on
CO2 diffusion conductance in the mesophyll and does
not consider light absorption. Nevertheless, it revealed
altered chloroplast organization under K deficiency, but
further studies are needed to describe this effect with
regard to photoprotection. The same applies for Mg,
where studies of chloroplastic movement in response to
Mg deficiency are completely absent from the present
literature.
Leaf movement
Paraheliotropic leaf movement is a mechanism by which
absorption of excess light and a resulting excessive exci-
tation pressure to the reaction centers is avoided. In
Robinia pseudoacacia, paraheliotropic leaf movement
resulted in an effective mean to alleviate high-light stress
on PSII (Arena et al. 2008). The level of Fv /Fm mea-
sured in the late afternoon was comparable to those in
the morning, whereas in leaves in which the rachis was
fixed to prevent leaf and leaflet movement, Fv /Fm was
reduced in the late afternoon. The authors suggest that
the absence of recovery indicate a PSII damage assuming
that Fv /Fm is a good indicator for photoinhibition (Arena
et al. 2008). Similarly, in young soybean leaves, changes
in the petiole and midrib angle reduced the light intensity
on the leaf surface and helped to protect leaves against
high irradiance (Jiang et al. 2006). Paraheliotropism was
shown to be a protection strategy against photoinhibition
in water-stressed bean cultivars (Pastenes et al. 2004) and
Vitis california (Gamon and Pearcy 1989). We observed
strong heliotropic leaf movements in sunflower grown
under K deficiency (unpublished data). We suggest that
beside the above-mentionned effects of leaf movement
on microclimate, paraheliotropism might play a role in
protecting sunflower leaves from excessive light. An indi-
cation is that leaf areas showing K deficiency symptoms,
are almost shaded from any light incidence. However,
in sunflower this phenomenon seems to be K-specific
as Mg-deficient plants did not show such behavior. To
our knowledge, no study on paraheliotropism under K
deficiency and its contribution to photoprotection exists.
Further research should be conducted to reveal whether
paraheliotropic leaf movement is an active strategy of
photoprotection or whether it is a reaction to reduced
turgor under K deficiency. In case it is an active strat-
egy under low-cellular K+ status, leaf movement might
be a preferred strategy as it is a turgor-driven and thus
Physiol. Plant. 163, 2018
a K requiring process (Oosterhuis et al. 2014), hence K+
ions preferentially need to be allocated to the sites where
leaf angle is controlled.
Summary
Mg and K are directly and indirectly involved in numer-
ous physiological processes associated to photosynthe-
sis (Fig. 2). A decline in the rate of net carbon assim-
ilation is observed when either of the nutrients can-
not be absorbed by plants in sufficient quantity, and its
leaf tissue concentration drops under a critical value.
Primary effects of K deficiency, that can be associated
with a reduction of the photosynthetic capacity or CO2
assimilation, are (1) decreased protein synthesis, and
therefore Rubisco quantity, (2) anatomical alterations
in leaf structure reducing mesophyll conductance and
thus chloroplastic CO2 concentration and (3) chloroplast
ultrastructure. Although K is involved in the osmoreg-
ulation of stomatal guard cells, K deficiency does not
impede stomatal functioning and the optimization of
photosynthetic water-use efficiency. Primary effects of
Mg deficiency also include protein and Rubisco syn-
thesis as well as chloroplast ultrastructure. In contrast
to K, Mg directly functions in chlorophyll synthesis and
Rubisco activation, but no effect of Mg deficiency on
leaf anatomy or mesophyll conductance is reported.
Both K and Mg directly affect the phloem loading of
sucrose, and a deficiency in those nutrients results in
an accumulation of sucrose in source tissues, causing
further down-regulation of Rubisco activity. Photoprotec-
tive mechanisms respond to both K and Mg deficiency,
with the potential of decreased Fv /Fm and enhanced
NPQ, antioxidant enzyme activity and photorespiration.
The manifold effects of plant anatomy, physiology and
biochemistry on photosynthesis, photosynthate translo-
cation and photoprotection under conditions of K and
Mg deficiency are characterized by complex interactions
and inter-regulatory mechanisms, and many questions
still remain to be answered.
Author contributions
M.T. and B.J. conceived, proofread and formatted the
manuscript in equal contributions. M.T. wrote the
sections related to Mg deficiency. E.T. wrote the sections
related to ROS and antioxidants. B.J. wrote the sections
related to K deficiency.
Acknowledgements – We thank Klaus Dittert, Andreas
Gransee and Ismail Cakmak for their continuous support
and creative input to our scientific work. We acknowledge
Dipl.-Ing. agr. Henrik Kierbaum of k1 mediendesign for
customized development and production of graphics.
Physiol. Plant. 163, 2018
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