Regulation of Calcium Uptake and Translocation in Plants

H. Yanga, Y. Jie and X. Shao

College of Horticulture
Shandong Agricultural University
State Key Laboratory of Crop Biology
Taian, Shandong 271018
China

Keywords: bio-regulator, Ca2+-ATPase, Ca uptake, energy supply, transport

Abstract
Calcium (Ca) is an essential plant nutrient and a second messenger in cell
signal transduction. Recently, most of the research on Ca in plants has been focused
on the role of Ca at the cellular level. But the uptake and transport are also very
important for Ca to accomplish its function at the whole plant level. The uptake of
Ca involves Ca entering one cell then exiting from this cell and entering another cell,
which is influenced by metabolism and temperature. The overexpression of Ca2+/H+
transporter can increase Ca levels of transgenic plants significantly. Ca2+ enter the
symplast from apoplastic pathways through Ca2+ channels. Ca2+-ATPase can drive
Ca2+ flux from symplast to apoplast. The uptake and transport of Ca are also
regulated by phytohormones, rootstock and genotype. There is a tight linkage of Ca
and auxin countercurrent fluxes.

INTRODUCTION
Ca is an essential element and a crucial regulator of growth and development in
plant. It plays an essential role in determining the structural rigidity of the cell wall and
controlling membrane structure and function (Hepler, 2005). The concentration of Ca
may be very high in soil, but Ca-deficiency disorders often occur in plants, such as bitter
pit of apple and fruit cracking of cherry (Shear, 1975). These disorders are mostly caused
by slow absorption and poor transport and distribution of Ca in the plant. Most of recent
research about Ca has been focused on the cellular or molecular levels and the role of Ca
in signaling (Hepler, 2005). The uptake of Ca2+ by roots is also very important to
understand.
The uptake of Ca2+ by roots is different than with single cell organisms because a
root is composed of many cell types. When moving into the xylem in roots for absorption,
Ca2+ is delivered to the endodermis via the apoplastic pathway, then it enters the symplast
through Ca2+ channels for the barrier of Casparian strip. When it reaches the stele, Ca2+ is
secreted into the apoplast from the symplast by the plasma membrane Ca2+-ATPase or
Ca2+/H+ antiporter. After being released to the xylem, Ca2+ is transported to the aerial part
through mass flow of water and ion exchange (Yang and Jie, 2005). White (2001) had
reviewed Ca movement of plants in general. This article provides an overview of work on
the regulation of Ca2+ uptake and delivery in plant.

REGULATION OF ENERGY SUPPLY ON CA UPTAKE

Temperature has no effect on uptake and translocation of Ca in intact plants
(Drew, 1971; Kuhn et al., 2000) and many inhibitors of respiration do not inhibit the
entering of Ca into cells (Shear and Faust, 1970), so it has been believed that the uptake
and transport of Ca2+ through the whole plant is a passive process via the apoplastic
pathway into the transpiration stream. But in decapitated plants, the water flux through
the roots is diminished even more than Ca2+ flux (Engels, 1999).
In fact, the uptake of Ca2+ in whole plants needs to pass through the apoplast and
the symplasm. The movement of Ca2+ from symplasm to apoplast against its
a
labft@sdau.edu.cn

Proc. IXth IS on Orchard Systems 1011

Ed.: T.L. Robinson
Acta Hort. 903, ISHS 2011
electrochemical gradient requires energy. In the presence of 2,4-DNP (one kind of
metabolic inhibitor), Ca2+ (45Ca) translocation is reduced in the intact plants in cucumber
while water translocation was unchanged (Bengtsson, 1982). In peanut, root and legumen,
2,4-DNP inhibits the transports of 45Ca and the curve for the relationship between Ca2+
uptake rate and Ca2+ concentration fits into Michaelis-Menten model (Zhou et al., 1996).
In apple roots, Ca2+ uptake rate is positively correlated to the activity of enzymes in
respiratory chain and the rate Ca2+ uptake is inhibited by 2,4-DNP under low Ca2+
concentrations (Yang et al., 2000).
The energy comes from active metabolism which is influenced by temperature.
Chung and Choi (1998) reported that the 45Ca2+ accumulation in leaves is doubled or
tripled by every 5°C increase from 15 to 25°C in grafted melon. In cucumber, Ca2+
accumulation increases gradually with temperature rising from 12-36°C (Daskalaki et al.,
1998). The rate of apple Ca2+ uptake was highest at 15-20°C under low concentrations of
Ca (Yang et al., 2003).

REGULATIONS OF CA2+ PASS THROUGH SYMPLASM

There are two protein-mediated steps for the delivery of solutes to the xylem, one
for uptake into the symplast and the other for release from stelar cells. The first step is the
Ca2+ influx to the symplast through Ca2+ channels. The second step is that Ca2+ effuses
from symplast and then is released to xylem from pericycle stelar parenchyma cells,
which requires ATPase to drive the process (Tester and Leigh, 2001).
When epidermal cells and root hairs contact the soil solution, Ca2+ can enter
directly to them through channels. It has been found that Ca2+ influx is highest at the tips
of root hairs (Gilroy and Jones, 2000), and many kinds of Ca2+ channels have been found
in root cells (White, 1998). These channels may play roles in Ca passing through the
endodermis. Ma et al. (2006) reported that seedlings of Arabidopsis lacking ion channel
of AtCNGC1 in the roots had lower Ca2+ in shoot. They conclude that AtCNGC1
contributed to Ca2+ uptake into plants.
There are Ca2+/H+ antiporters that remove Ca2+ from the cytosol to either the
apoplast or to intracellular organelles in the plasma membrane or tonoplast of plant.
Eleven genes encoding putative Ca2+/H+-antiporters (AtCAX) have been identified in the
genome of Arabidopsis, and the Ca levels increased significantly in carrots, tomato and
potato by overexpression of an Arabidopsis Ca2+/H+ transporter in transgenic plants (Park
et al., 2005; Han et al., 2005).
Zhou and He (1999) reported that the symplastic transport of Ca relied on Ca2+-
ATPase in fruit tissue. The inhibitor of Ca2+-ATPases, VO43- substantially reduced the
amount of Ca2+ delivered to the stele of roots (Cholewa and Peterson, 2004). This
suggests that Ca2+ fluxes to the xylem may be sustained by Ca2+-ATPases in exodermal
and endodermal cells (Hayter and Peterson, 2004). Yang et al. (2004) had found that there
was a positive correlation between the rate of Ca2+ uptake and Ca2+-ATPase activity in
roots under low Ca concentration in solution. The transportation and storage of Ca and
Ca2+-ATPase activity in tender shoots of apple was promoted by IBA (Li et al., 2006).
The distribution of Ca2+-ATPase is related to the direction Ca2+ transport. In apple root
cells, Ca2+-ATPase is distributed primarily in the plasmalemma, the inner margin of
vessels and the space between the plasmalemma and cell wall. Its distribution is not
uniform in the cell and plasmalemma. The activity of Ca2+-ATPases decreases gradually
in the radial direction from vessel to epidermis cells (Yang et al., 2004).

REGULATION OF CA TRANSPORT BY BIO-REGULATORS

Auxin applied two weeks after blooming may increase the amount of Ca in the
fruits (Basak, 1993). The movement of Ca from apple peel to fresh can be promoted by
IAA and NAA, but they enhance Ca2+ efflux from the cell and vacuole (Zhou et al., 1999,
2000). Auxin can increase Ca mobilization from old stub and root tissues to current
shoots and roots of apples (Kim, 1997). Auxin promotes the translocation and
accumulation of Ca in the grafted melon (Chung and Choi, 1998), and enhances Ca

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transport in eggplant and Chinese cabbage (Miao et al., 1998; Sun et al., 1999). The
accumulation of Ca was observed for the roots and mesocotyls of plants treated with
IAA + NaHSeO3 in zea mays (Pazurkiewicz-kocot et al., 2003). IBA (4-[3-indolyl]
butyric acid), another kind of auxin, increases the Ca content both in roots and leaves of
Malus hupehensis (Yang et al., 2002). Li et al. (2006) has observed that spraying of IBA
increased the percentage of active Ca (NaCl-Ca and H2O-Ca) in tender shoots, and
boosted the transportation of stored Ca in apple trees. The mechanism of auxin regulation
of Ca uptake in root is shown in Figure 1.
Lau and Yang (1975) reported that cytokinins greatly stimulated uptake of 45Ca2+
in mung bean hypocotyl segments. Elliott et al. (1989) found cytokinin have a small but
reproducible effect on increasing initial 45Ca2+ accumulation in Amaranthus protoplasts in
vitro. Application of cytokinin to tissues prior to protoplast isolation also increases Ca2+
transport capacity in vivo.
Saure (2002) suggested that high levels of endogenous gibberellins (GAs) may
result in the bitter pit caused by Ca deficiency in apple fruit. Varying levels of GAs could
be the cause of the differences in the Ca content of the fruit between years and regions
(Saure, 2005). Blanco et al. (2002) reported that Ca accumulation increases after
application of paclobutrazol, the inhibitor of gibberellin biosynthesis, in peach leaves. But
Basak (1993) observed that GA3 applied on long shoots of ‘Double Red McIntosh’ apple,
increased the percentage of Ca in fruits, though decreased the Ca uptake by whole plant
segments. Foliar applied GA3, promoted the translocation and accumulation of Ca2+ in
grafted melons (Chung and Choi, 1998). Zhou et al. (1999) reported that GA3 can
enhance the movement of Ca from apple peel to flesh. In tomato, the application of GA3
to either of these leaves resulted in twice the accumulation of 45Ca2+ in treated plants as in
plants which were sprayed with distilled water (Chung and Choi, 2001).

REGULATION OF OTHER FACTORS ON CA UPTAKE

Apple trees sprayed with daminozide had relatively more 45Ca in fruits and short
shoots (Basak, 1993). Chung and Choi (2001) reported that the 45Ca2+ accumulation
increased when 2-(3-chlorophenoxy) propanoic acid was applied onto upper tomato leaf.
Chitosan stimulated Ca uptake of young plants in Chinese cabbage (Jang et al., 2002) and
Vitamin D3 stimulated Ca2+ uptake in Phaseolas vulgaris root segments (Boland et al.,
2003).
The uptake and transport of Ca is related to scion genotype and rootstock. The
Ca2+ concentration in xylem sap was higher in most grafted melon than that in own-
rooted plants (Kim et al., 1999). ‘BC-2 Fuji’ apple trees grafted on Budagovsky 9
rootstock had higher Ca in the shoots and spur leaves and had higher fruit Ca than on
other rootstocks (M.9 NAKBT337, Ottawa 3, M.26 EMLA and M.7 EMLA) in two years
(Chun et al., 2002).

CONCLUSIONS
The absorption of Ca by whole plant requires that Ca2+ pass through symplastic
and apoplastic pathways, which is not solely a passive process drawn by transpiration. It
needs the support of energy and can be influenced by temperature. Ca2+-ATPases have
been found in roots. The rate of Ca2+ uptake in apple root increases with an increase in
Ca2+-ATPase activity. Inhibitors of Ca2+-ATPases substantially reduced the amount of
Ca2+ delivered to the stele (Cholewa and Peterson, 2004). Ca2+/H+ antiporters have been
found in roots too. They play an important role in transport of Ca to vacuoles and
catalyzing Ca2+ flux from symplast to apoplast. But there have been few reports on the
function of Ca2+/H+ antiporter in the loading of Ca2+ into the xylem.
When Ca2+ is released to the xylem it is transported to the aerial part with the
xylem stream via mass flow of water and ion exchange. The water flow rate is a key
factor for Ca2+ transport in the xylem. But Ca uptake is not always proportional to water
movement in the xylem. In going into and out of xylem, Ca2+ may pass through either an
apoplastic or symplastic pathway, or both. But the relative contribution of them is not

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known yet. The mechanism of Ca2+ release to the xylem vessel from xylem parenchyma
cells is not clear.
The uptake and transport of Ca is also regulated by phytohormones. Auxin
promotes Ca2+ uptake evidently at the cell level and plays a role in the allocation of Ca in
plants. There is a tight linkage of Ca and auxin countercurrent fluxes. Ca2+ translocation
and accumulation are promoted by cytokinins. There are different results concerning the
role of gibberellins in Ca2+ translocation and accumulation. The uptake and transport of
Ca also is related to rootstock and plant genotype. This means that the cultivars and
species with high efficiency of Ca uptake and transport can be selected, which eventually
can supply more Ca to the human body.

Literature Cited
Basak, A. 1993. Influence of retardant and auxin treatment of apple shoots and fruits on
Ca uptake and distribution. J. Fruit Orn. Plant Res. 1:103-114.
Bengtsson, B. 1982. Uptake and translocation of Ca in cucumber. Physiol. Plant. 54(2):
107-113.
Blanco, A., Monge, E. and Val, J. 2002. Effects of paclobutrazol on dry weight and
mineral element distribution among fruits and shoots of ‘Catherine’ peach trees. J
Plant Nutr. 25:1685-1699.
Boland, R., Skliar, M., Curino, A. and Ilanesi, L. 2003. Vitamin D compounds in plants.
Plant Sci. 164(3):357-369.
Chun, I.J., Colt, F.E., Shafii, W.M. and Tripepi, R.R. 2002. Effects of rootstocks and
microsprinkler fertigation on mineral concentrations, yield, and fruit color of ‘BC-2
Fuji’ apple. J. Amer. Pomol. Soc. 56(1):4-13.
Chung, H.D. and Choi, Y.J. 1998. Effects of temperature and foliar application of NAA
and GA3 on 45Ca translocation and accumulation in the grafted melon (Cucumis melo
var. makuwa) plants. J. Kor. Soc. Hort. Sci. 39:491-496.
Chung, H.D. and Choi, Y.J. 2001. Foliar application of plant growth regulators affects
distribution and accumulation of Ca (45CaCl2) in tomato leaves. J. Kor. Soc. Hort. Sci.
42(6):656-660.
Cholewa, E. and Peterson, C.A. 2004. Evidence for symplastic involvement in the radial
movement of Ca in onion roots. Plant Physiol. 134:1793-1802.
Daskalaki, A., Barrage, S.W. and Munnoz, C.R. 1998. Solution temperature and the
uptake of water and nutrients by cucumber (Cucumis sativus L.) in hydroponics. Acta
Hort. 458:317-322.
Drew, M.C. 1971. Effect of metabolic inhibitors and temperature on uptake and
translocation of 45Ca and 42K by intact bean plants. Plant Physiol. 48:426-432.
Elliott, D.C. and Yao, Y.G. 1989. Cytokinin and fusicoccin effects on Ca transport in
Amaranthus protoplasts. Plant Sci. 65:243-252.
Engels, C. 1999. Regulation of xylem transport of Ca from roots to shoot of maize by
growth-related demand. J. Plant Nutr. Soil Sci.162(3):287-294.
Jang, E.J., Lee, C. and Kim, J.K. 2002. Chitosan stimulate Ca uptake and enhances the
capability of young chinese cabbage plants to resist soft rot disease. Kor. J. Hort. Sci.
Techn. 20(5):32-32.
Gilroy, S. and Jones, D.L. 2000. Through form to function: root hair development and
nutrient uptake. Trend in Plant Sci. 5(2):56-60.
Hayter, M.L. and Peterson, C.A. 2004. Can Ca2+ fluxes to the root xylem be sustained by
Ca2+-ATPases in exodermal and endodermal plasma membranes? Plant Physiol. 136:
4318-4325.
Hepler, P.K. 2005. Ca: A central regulator of plant growth and development. Plant Cell
17:2142-2155.
Hirschi, K.D. 2001. Vacuolar H+/Ca2+ transport: who’s directing the traffic? Trends in
Plant Sci. 6:100-104.
Han, J.S., Chung, M.Y., Joung, Y.O. and Kim, C.K. 2005. Increased Ca in potato
(Solanum tuberosum cv. Daejiree) tuber by overexpression of Arabidopsis CAX1

1014
 gene. Hort. Environ. Biotech. 46(2):108-112.
Kim, W.S. 1997. Ca remobilization in ‘Golden Delicious’ apples and the seedlings of
during spring season. J. Kor. Soc. Hort. Sci. 38 (2):142-146.
Kim, S.E., Jung, K.H. and Lee, J.M. 1999. Content of mineral elements and cytokinins in
xylem sap of two oriental melon cultivars affected by rootstocks. Kor. J. Hort. Sci.
Techn. 17:742-746.
Kuhn, A.J., Schroder, W.H. and Bauch, J. 2000. The kinetics of Ca and magnesium entry
into mycorrhizal spruce roots. Planta 210:488-496.
Lau, O.L. and Yang, S.F. 1975. Interaction of kinetin and Ca in relation to their effect on
stimulation of ethylene production. Plant Physiol. 55:738-740.
Li, J., Yang, H.Q. and Shu, H.R. 2004. Indole butyric acid (IBA) activate Ca2+-ATPase
activity of Malus hupehensis Rehd. roots through protein phosphorylation. J. Plant
Physiol. Molecul. Biol. 30(4):449-454.
Li, J., Yang, H.Q., Shu, H.R. and Yan, T.L. 2006. Effect of Indole Butyric Acid on the
transportation of stored Ca in Malus hupehensis Rhed. seedling. Agri. Sci. China
5(11):834-838.
Ma, W., Rand, A. and Berkowitz, G.A. 2006. Characterization of plant phenotypes
associated with loss-of-function of AtCNGC1, a plant cyclic nucleotide gated cation
channel. Plant Physiol. Biochem. 44(7-9):494-505.
Miao, Y., Cao, J.S. and Jiang, Y.T. 1998. Effect of NAA on the uptake and accumulation
of 45Ca in Chinese cabbage. Acta Agri. Nucleatae Sinica 25(2):83-88.
Park, S.H., Kang, T.S., Kim, C.K., Han, J.S., Kim, S., Smith, R.H., Pike, L.M. and
Hirschi, K.D. 2005. Genetic manipulation for enhancing Ca content in potato tuber. J.
Agri. Food Chem. 53:5598-5603.
Saure, M.C. 2002. New views of the prerequisites for an occurrence of bitter pit in apple
and its control by Ca sprays. Acta Hort. 594:421-425.
Saure, M.C. 2005. Ca translocation to fleshy fruit: its mechanism and endogenous
control. Sci. Hort. 105(1):65-89.
Shear, C.B. 1975. Ca-related disorders of fruits and vegetables. HortScience 10:361-365.
Shear, R.L. and Faust, M. 1970. Ca transport in apple trees. Plant Physiol. 15:670-674.
Sun, D.L., Wen, F.Y., Shu, Y.M. and An, Z.X. 1999. Effect of NAA on Ca uptake and
transport in eggplant. Acta Agri. Boreali-Sinica 14(1):89-92.
Tester, M. and Leigh, R.A. 2001. Partitioning of nutrient transport processes in roots. J.
Exp. Bot. 52:445-457.
White, P.J. 1998. Ca channels in the plasma membrane of root cells. Ann. Bot. 81:173-
183.
White, P.J. 2001. The pathways of Ca movement to the xylem. J. Exp. Bot. 52:891-899.
Yang, H.Q., Li, J., Zhang, J., Zhang, X.H. and Xiao, J. 2002. The Regulation of Ca
absorption by plant growth substance in apple roots. In: Chinese Agriculture
Academy, eds. Annals of Chinese Youth Agriculture Science. Beijing: Chinese
Agriculture Press p.306-308.
Yang, H.Q., Zhang, L.Z., Qi, J.L. and Jie, Y.L. 2003. The kinetics of Ca uptake in apple
rootstock roots. Acta Hort. Sinica 30(3):253-256.
Yang, H.Q. and Jie, Y.L. 2006. Uptake and transport of Ca in plants. J Plant Physiol. Mol.
Biol. 31(3):227-234.
Yang, H.Q., Jie, Y.L. and Zhang, L.Z. 2000. Effect of IBA on the Ca2+ uptake and root
activity in young apple trees. Adv. Hort. China 4:57-59.
Yang, H.Q., Jie, Y.L., Zhang, L.Z. and Cui, M.G. 2004. The effect of IBA on the Ca2+
absorption and Ca2+-ATPase activity and their ultracytochemical localization in apple
roots. Acta Hort. 636:211-219.
Zhou, W. and He, P. 1999. The characteristic of Ca2+-ATPase activated transport of Ca2+
in the plasmalemma of apple fresh. Acta Phytophysiol. Sinica 25(2):151-158.
Zhou, W. and Lin, P. 1996. Study on the characteristic of Ca absorption in peanut roots.
Plant Nutr. Fert. Sci. 2(3):226-231.
Zhou, W. and Lin, P. 2000. Study on pathways of Ca2+ movement in young fruit tissue of

1015
 apple and its regulation by hormones. Plant Nutr. Ferti. Sci. 6(2):214-219.
Zhou, W., Lin, P. and He, P. 1995. Study on the mechanism of Ca absorption in peanut
pod. Plant Nutr. Fertilizer Sci. 1(1):40-45.
Zhou, W., Lin, P. and He, P. 1999. Characteristic of Ca absorption and its regulation by
hormones in apple fruit. Chinese Agri. Sci. 32(3):52-58.

Figures

Fig. 1. The scheme of auxin regulating Ca uptake in the root. After signal transduction,
auxin activates H+-ATPase and Ca2+-ATPase and Ca2+ channels for Ca
transporting cells, which could promote the movement of Ca to xylem vessels
through the symplastic pathway. At the same time, root activity increases (Yang et
al., 2002), which could provide energy for Ca uptake through the symplastic
pathway and transport via the apoplastic pathway. On the other hand, auxin can
promote cell division for root thickening and lateral root formation. During root
secondary growth and lateral root emergence, the Casparin band loses its function
as an apoplastic barrier (Peterson and Leterson, 1990) and apoplastic space
increases in the epidermis as some new crack appear and newly-formed
endodermal cell walls lack a Capsparian band (Weerdenburg and Peterson, 1984),
which is convenient for Ca moving to the xylem vessel via the apolastic pathway.
Furthermore, the growth and formation of lateral roots provides a large surface for
absorbing more Ca.

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