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Bio-fortification of potato tubers using foliar zinc-fertiliser

Article  in  Journal of Horticultural Science and Biotechnology · March 2012

DOI: 10.1080/14620316.2012.11512842

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Journal of Horticultural Science & Biotechnology (2012) 87 (2) 123–129

Bio-fortification of potato tubers using foliar zinc-fertiliser

By PHILIP J. WHITE1*, MARTIN R. BROADLEY2, JOHN P. HAMMOND2, GAVIN RAMSAY1,

NITHYA K. SUBRAMANIAN1, JACQUELINE THOMPSON1 and GLADYS WRIGHT1
1
The James Hutton Institute, Invergowrie, Dundee DD2 5DA, UK
2
Plant and Crop Sciences Division, University of Nottingham, Sutton Bonington Campus,
Loughborough LE12 5RD, UK
(e-mail: [email protected]) (Accepted 29 November 2011)

SUMMARY
Worldwide, many people are zinc (Zn)-deficient. Dietary Zn intake can be increased by producing crops with higher
concentrations of Zn in their edible portions. This can be achieved by applying Zn-fertilisers to varieties with an
increased ability to acquire Zn and to accumulate Zn in their edible portions. Potato (Solanum tuberosum L.) is an
important food crop and is, therefore, a target for bio-fortification with Zn. Field trials incorporating a core collection
of 23 potato genotypes, performed over 4 years (2006 – 2009), indicated significant genotypic effects on tuber Zn
concentration and suggested that tuber Zn concentration was influenced by environmental effects, but also found that
genotype
environment (G
E) interactions were not significant. Tuber Zn concentrations averaged 10.8 mg kg–1
dry matter (DM), and the ratio between the lowest and the highest varietal tuber Zn-concentration averaged 1.76.
Tuber Zn concentrations could be increased by foliar Zn-fertilisation. Tuber yields of ‘Maris Piper’ were unaffected by
foliar applications of < 1.08 g Zn plant–1. The relationship between tuber Zn concentration and foliar Zn application
followed a saturation curve, reaching a maximum at approx. 30 mg Zn kg–1 DM at a foliar Zn application rate of 1.08 g
plant–1. Despite a 40-fold increase in shoot Zn concentration compared to the unfertilised controls following foliar Zn-
fertilisation with 2.16 g Zn plant–1, only a doubling in tuber Zn concentration was observed. This suggests that the bio-
fortification of tubers with Zn was restricted by the limited mobility of Zn in the phloem. A significant positive linear
relationship between tuber Zn concentration and tuber N concentration supported the hypothesis of co-transport of
Zn and N-compounds in the phloem.

I t has been estimated that over one-third of the World’s

population are zinc (Zn)-deficient (Cakmak, 2008;
White and Broadley, 2009; Cakmak et al., 2010; Stein,
2011). It has been estimated that 200 g fresh weight (FW)
of unpeeled potato tubers can supply 5.5% of the total
daily requirement of male human adults (i.e., approx. 11
2010 and references therein). This situation can be mg Zn; White et al., 2009). Furthermore, since potato
addressed through dietary diversification, mineral tubers contain relatively high concentrations of organic
supplementation, and/or food fortification, although compounds that stimulate the absorption of Zn, and low
these strategies have not always been successful (White concentrations of compounds that limit Zn absorption,
and Broadley, 2005; 2009; Cakmak, 2008; Meenakshi the bio-availability of Zn in potato tubers is potentially
et al., 2010; Stein, 2010). An alternative strategy is to high (Burlingame et al., 2009; Kärenlampi and White,
increase the concentrations of Zn in the edible portions 2009; White et al., 2009). The use of Zn-fertilisers to
of crops through the use of Zn-fertilisers on plant increase tuber Zn concentrations could provide a simple
varieties that are able to acquire Zn and to accumulate strategy to increase the amount of bio-available Zn in
Zn in their edible portions (White and Broadley, 2005; diets dominated by potatoes. This paper describes the
2009; Graham et al., 2007; Pfeiffer and McClafferty, 2007; effects of foliar applications of Zn-fertiliser on tuber yields
Cakmak, 2008; Cakmak et al., 2010; Bouis and Welch, and on Zn concentrations in a Zn-sufficient potato crop.
2010; Meenakshi et al., 2010; Stein, 2010; White and
Brown, 2010). This strategy is termed bio-fortification,
and it promises not only to increase Zn concentrations in MATERIALS AND METHODS
food and feed, but also to increase crop yields on infertile Quantifying variation in tuber Zn concentration among
soils. Zinc is commonly applied to crops as ZnSO4, ZnO, potato genotypes
or as synthetic chelates (Broadley et al., 2007; Cakmak, Field trials incorporating a core collection of
2008; White and Broadley, 2009). 23 tetraploid (S. tuberosum Group tuberosum) potato
Potato (Solanum tuberosum L.) is one of World’s most genotypes were conducted at Gourdie Farm, Dundee
important food crops (FAO, 2009). It is of increasing (56°28'N, 03°07'W), in 2006, 2007, and 2008, and at
importance in developing countries because of its price Balruddery Farm, Dundee (56°28'N, 03°03'W), in 2009,
stability, its high yield potential, and its nutritional following standard UK agronomic practices. The
qualities (Andre et al., 2007; Storey, 2007; Prakash, 2008; genotypes used were: 12601ab1, ‘Ailsa’, ‘Anya’, ‘Brodick’,
Burlingame et al., 2009; White et al., 2009; Fageria et al., ‘Cara’, ‘Desiree’, ‘Estima’, ‘Golden Millennium’,
‘Hermes’, ‘Home Guard’, ‘Home Harvest’, ‘Maris Piper’,
*Author for correspondence. ‘Montrose’, ‘Nadine’, ‘Pentland Dell’, ‘Pentland Squire’,
124 Bio-fortification of potato with zinc

‘Record’, ‘Saxon’, ‘Scarborough’, ‘Stirling’, ‘Tay’, ‘Vales grade from each plot, comprising four diagonally-
Everest’, and ‘Wilja’. Plants were grown in randomised opposite eighths of three or more representative tubers
block designs, with five-to-eight plants per plot, was freeze-dried. A sub-sample of each freeze-dried
depending on the year of the field trial, with two shoot and tuber material was milled separately to
replicate plots per genotype. Seed potatoes were planted powder (C+N Laboratory Mill; Christy and Norris Ltd.,
in late April, and tubers were harvested at commercial Chelmsford, UK). Zinc concentrations in the powdered
maturity in September. samples were determined essentially as described by
Three representative tubers from each plot were Subramanian et al. (2011). Accurately weighed powdered
washed and cut into eighths by first slicing horizontally samples (each approx. 50 mg DM) were digested with 3.0
from rose-to-heel, then vertically from rose-to-heel, and ml concentrated nitric acid and 1.0 ml of 30% (v/v)
finally vertically midway between rose and heel. Sub- hydrogen peroxide in closed vessels using a microwave
samples from each plot, comprising four diagonally digester (MARS Xpress; CEM Microwave Technology,
opposite eighths of all representative tubers sampled Buckingham, UK) with the following programme: 2 min
from that plot, were freeze-dried (Millitorr S3921 at 100°C, 1 min at 120°C, 2 min at 160°C, 20 min at 180°C,
Vacuum Freeze-Drying Unit; Millitorr Engineering Ltd., and 20 min cooling time. Each digested sample was
Manchester, UK). Sub-samples of freeze-dried tuber diluted to 50 ml with sterile MilliQ water (18.2 M cm)
material were milled to a powder using a ball-mill. prior to elemental analyses. Blank digestions were also
Accurately weighed sub-samples [approx. 100 mg dry performed and the National Institute of Standards and
matter (DM)] of each milled material were digested by Technology (NIST, Gaithersburg, MD, USA) tomato leaf
the micro-Kjeldahl method and their Zn concentrations standard (Reference Number 1573a) was used as an
were determined using inductively-coupled plasma internal control. Zinc concentrations in the digested
emission spectrometry (ICP-AES; JY Ultima 2; Jobin plant material samples were determined using
Yvon Ltd., Stanmore, UK), as described by Broadley inductively-coupled plasma mass spectrometry (ICP-
et al. (2010). Total nitrogen (N) concentrations were MS; ELAN DRCe; PerkinElmer, Waltham, MA, USA).
quantified directly on accurately weighed sub-samples
(approx. 0.5 g DM) of each milled material using a C:N Statistical analysis
analyser (CN2000; LECO, Stockport, UK), as described Data were expressed as means ± standard deviations
by Broadley et al. (2004). from n determinations. The significance of the difference
between two sets of data was attributed through the
Increasing tuber Zn concentration by foliar fertilisation Student’s t-test. Analysis of variance (ANOVA) was
The variety ‘Maris Piper’ was used to determine the performed using Microsoft Office Excel (Microsoft
effects of foliar Zn-fertilisation on tuber Zn Corporation, Redmond, WA, USA).
concentration. Plants were grown in Quarry Field at the
former SCRI, Dundee (56°27'N, 03°04'W). Seed
potatoes were planted late, on 15 July 2010, and grown in RESULTS AND DISCUSSION
a randomised block design with five plants per plot and Significant differences in tuber Zn concentration were
two replicates for each of ten treatments. The plot size observed among the core collection of 23 common
was 1.84 m2. potato genotypes in field trials performed on SCRI
In addition to a control treatment without the
application of foliar Zn, nine foliar Zn-fertiliser
Mean tuber Zn concentration (mg kg–1 DM)

treatments were applied. These were based on a “full-

dose” of 1.8 g Zn plot–1. The treatments were: half the
full-dose applied once (Half X1), half the full-dose
applied twice (Half X2), half the full-dose applied three
times (Half X3), the full-dose applied once (Full X1), the
full-dose applied twice (Full X2), the full-dose applied
three times (Full X3), double the full-dose applied once
(Double X1), double the full-dose applied twice (Double
X2), and double the full-dose applied three times
(Double X3). In each case, the first application was made
as zinc sulphate heptahydrate in July. The second and
third applications, where appropriate, were made as
Zintrac 700 (zinc oxide; Yara, Grimsby, UK) on 4 August
and 19 August.
Shoots were excised from plants on 14 September, and
tubers were harvested on 28 September. The total FWs
of shoots and tubers were determined for each plot. FIG. 1
Variation in mean tuber Zn concentration in a core collection of 23
Shoot material from a representative plant from each commercial potato genotypes. Data are expressed as means of the
plot was freeze-dried, then weighed to determine its DM. annual mean ± standard error of the mean for four field trials performed
on SCRI farms in 2006, 2007, 2008, and 2009. The genotypes used were:
All tubers from each plot were separated by size (< 30, (1) ‘Home Harvest’, (2) ‘Home Guard’, (3) ‘Record’, (4) 12601ab1, (5)
30 – 45, 45 – 60, 60 – 75, and > 75 mm in diameter) and ‘Pentland Dell’, (6) ‘Vales Everest’, (7) ‘Scarborough’, (8) ‘Estima’, (9)
the contribution of each tuber size to the total FW of the ‘Maris Piper’, (10) ‘Desiree’, (11) ‘Pentland Squire’, (12) ‘Cara’, (13)
‘Tay’, (14) ‘Montrose’, (15) ‘Wilja’, (16) ‘Hermes’, (17) ‘Nadine’, (18)
plot was determined. Tubers were washed and cut into ‘Brodick’, (19) ‘Golden Millennium’, (20) ‘Stirling’, (21) ‘Ailsa’, (22)
eighths, as described above. A sub-sample of each size ‘Anya’, and (23) ‘Saxon’.
 P. J. WHITE, M. R. BROADLEY, J. P. HAMMOND, G. RAMSAY, N. K. SUBRAMANIAN, J. THOMPSON 125
and G. WRIGHT
farms between 2006 and 2009 (Figure 1). These results (Figure 2C). A two-factor ANOVA with replication
were consistent with previous observations that potato indicated that foliar Zn-fertiliser treatments had no
genotypes have different Zn concentrations in their significant effect on the yields of tubers of different sizes
tubers (e.g., Randhawa et al., 1984; Ereifej et al., 1998; (data not shown).
Tekalign and Hammes, 2005; Bethke and Jansky, 2008; When foliar Zn-fertilisers were applied to Zn-
White et al., 2009; De Haan et al., 2010). In addition to sufficient potato plants, shoot Zn concentrations
significant genotypic effects on tuber Zn concentrations
(P = 0.0004), the SCRI field trials suggested that tuber
Zn concentration was also influenced by environmental
effects attributed to the year in which the plants were A
grown (P = 0.0174), but found that genotype

environment interactions were not significant (P = 0.361;
two-factor ANOVA with replication). The ratio of the
highest to the lowest varietal tuber Zn-concentration
averaged 1.76 (n = 4 years). Both the means and standard
deviations of tuber Zn concentrations in the core
collection were remarkably similar across the four
annual field trials. Tuber Zn concentrations were 11.01 ±
1.97 mg kg–1 DM in 2006, 10.09 ± 1.45 mg kg–1 DM in
2007, 11.14 ± 1.75 mg kg–1 DM in 2008, and 11.14 ± 1.43
mg kg–1 DM in 2009 (mean ± SD; n = 23 genotypes). In
addition, the rankings of the tuber Zn concentrations of
these 23 potato genotypes were relatively consistent
between years. However, although the tissue Zn-
concentrations measured in the plants grown in these
field trials would be considered sufficient for maximal B
tuber yield (Figure 2), a 200 g FW portion of their tubers
would deliver only approx. 4% of the daily Zn
requirement for male human adults.
Shoot Zn concentrations can be increased by
Zn-fertilisation of the soil in plants growing on most, but
not all, soils, and/or by foliar applications of Zn-fertiliser
(Rengel et al., 1999; Cakmak, 2008; White and Broadley,
2009; Bouis and Welch, 2010). However, Zn
concentrations in fruits, grains, and tubers are often only
increased significantly in plants with adequate
Zn mobility in the phloem, unless Zn-fertilisers are
applied directly to these edible tissues or they have
functional xylem continuity (Rengel et al., 1999; White
and Broadley, 2005; 2009; Stomph et al., 2009; Cakmak
et al., 2010). To determine the limits to the bio-
fortification of potato tubers with Zn, foliar applications
C
of Zn-fertiliser were made to Zn-sufficient plants. In
addition to a control treatment without foliar Zn
application, nine foliar Zn-fertiliser treatments were
applied (see Materials and Methods).
There were no significant differences in shoot biomass
between those plots that had received foliar Zn-fertiliser
and the unfertilised control plot. However, there was a
trend of decreasing shoot biomass with increasing foliar
Zn application (Figure 2A). The mean shoot biomass
from plots that had received < 5.4 g Zn plot–1 (i.e., 18.35
± 1.90 kg FW plot–1; n = 14) was significantly greater (P
= 0.0015) than the mean shoot biomass from plots that
had received ≥ 5.4 g Zn plot–1 (14.65 ± 2.32 kg FW plot–1;
n = 6). Similarly, lower tuber yields occurred in plots that FIG. 2
had received the foliar applications ≥ 5.4 g Zn plot–1 Relationships between (Panel A) shoot biomass and foliar Zn
application, (Panel B) tuber yield and foliar Zn application, and (Panel
(Figure 2B). Mean tuber yields from plots that had C) tuber yield and shoot biomass for ‘Maris Piper’ potato. Data are from
received < 5.4 g Zn plot–1 (i.e., 26.52 ± 1.31 kg FW plot–1; individual plots. In addition to a control treatment without foliar Zn
application (closed circles), nine foliar Zn-fertiliser treatments were
n = 14) were significantly greater (P = 3.04
10–1) than applied. These were based on a “full-dose” of 1.8 g Zn plot–1. The
mean tuber yields from plots that had received ≥ 5.4 g Zn treatments applied were: half the full-dose applied once, twice, or three
plot–1 (21.72 ± 2.63 kg FW plot–1; n = 6). The relationship times (closed squares in Panels A and B), the full-dose applied once,
twice, or three times (open squares in Panels A and B), and double the
between tuber FW yield and shoot FW biomass full-dose applied once, twice or three times (closed triangles in Panels A
appeared to be unaffected by the foliar application of Zn and B).
126 Bio-fortification of potato with zinc

FIG. 3
The effect of foliar Zn-fertiliser application on tuber Zn concentration
in ‘Maris Piper’ potato. Data are from individual plots. In addition to a
control treatment without foliar Zn application (closed circles), nine FIG. 4
foliar Zn-fertiliser treatments were applied. These were based on a “full- The effect of foliar Zn-fertiliser application on Zn concentrations in
dose” of 1.8 g Zn plot–1. The treatments were: half the full-dose applied tubers of ‘Maris Piper’ of different size. In addition to a control
once, twice, or three times (closed squares), the full-dose applied once, treatment without foliar Zn application, nine foliar Zn-fertiliser
twice, or three times (open squares), and double the full-dose applied treatments were applied. These were based on a “full-dose” of 1.8 g Zn
once, twice or three times (closed triangles). plot–1. The treatments were: half the full-dose applied once, twice, or
three times, the full-dose applied once, twice, or three times, and double
the full-dose applied once, twice or three times.
increased greatly, as also observed by Fontes et al. (1999).
Across all treatments, the shoot retained 30.4 ± 9.1% (n = Zn-fertiliser to the plot (Figure 3). Again, this might be
18) of the foliar Zn-fertiliser applied to the crop. The attributed to the timing of the application(s) of
mean shoot Zn concentration of plants that received a Zn-fertiliser, or to the use of different forms of
foliar application of 3.6 g Zn plot–1 was 368 mg Zn kg–1 Zn-fertiliser in the first and subsequent applications. The
DM (Double X1 treatment) or 792 mg Zn kg–1 DM (Full tubers of plants that received 3.6 g Zn plot–1 (Full X2 and
X2 treatment). These concentrations exceed the whole- Double X1 treatments) had 1.7-fold higher tuber Zn
leaf Zn concentration thought to be toxic in potato (> 150 concentrations than plants that had received no
mg Zn kg–1 DM; Walworth and Muniz, 1993), but no Zn-fertiliser (Figure 3). When the Zn concentrations in
toxicity symptoms were apparent. It is possible that the tubers of different sizes were considered (Figure 4), in
higher shoot Zn concentrations in plants that had addition to the significant effects of foliar
received multiple smaller applications rather than a Zn-fertilisation on tuber Zn concentrations (P = 2.57

single large application of the same amount of 10–11), it was observed that tuber Zn concentrations also
Zn-fertiliser might be attributed to the timing of the differed significantly between tubers of different size
applications of Zn-fertiliser, or to the type of Zn-fertiliser (P = 1.18
10–6), which is consistent with a decrease in
applied. Zinc was applied as ZnSO4 in the first tuber Zn concentration during tuber bulking (P. J. White
application, but as ZnO in subsequent applications. The and M. A. Taylor, unpublished observations), but there
shoots of plants that received 10.8 g Zn plot–1 had a mean were no interactions between foliar Zn-fertilisation and
Zn concentration of 2,160 mg Zn kg–1 DM (Double X3 tuber size on tuber Zn concentrations (P = 0.621;
treatment), which was 40-fold greater than the mean Zn two-factor ANOVA with replication for tuber sizes < 30,
concentration in the shoots of plants that had received no 30 – 45, 45 – 60, and 60 – 75 mm in diameter).
Zn-fertiliser.The location of the Zn in the shoots of plants The observations that (a) tuber Zn concentrations
to which Zn-fertiliser had been applied was not were far lower than shoot Zn concentrations, and (b)
determined. It is possible that some of the Zn measured that there was a maximum tuber Zn concentration that
in the shoot was still present on the surface of the plant or could be achieved, suggest that tuber Zn concentration
in the shoot apoplast, rather than within cells. was limited by the translocation of Zn in the phloem
Although the concentration of Zn in tubers also from the shoots to the tubers. This is consistent with
increased with increasing foliar Zn-fertilisation, this previous observations that Zn has a measurable, but
increase was not as great as in shoots, and tuber Zn limited, mobility in the phloem of potato plants
concentrations were far lower than shoot Zn (Westermann, 2005; Kärenlampi and White, 2009). A
concentrations (Figure 3). The relationship between similar phenomenon has been observed in cereals. Zn is
tuber Zn concentration and foliar Zn application thought to be transported either as Zn-nicotianamide or
followed a saturation curve, reaching a maximum value complexed with small proteins in the phloem (White and
of approx. 30 mg kg–1 DM (Figure 3). It is possible that Broadley, 2009). In cereals, Zn concentrations in the
restricted entry of Zn into leaf cells, or restricted loading grain were correlated with grain protein concentration
of Zn into the phloem in the shoot could be responsible (e.g., Zhao et al., 2009; Cakmak et al., 2010; Chatzav et al.,
for the inability to increase tuber Zn concentrations. 2010; Gomez-Becerra et al., 2010), and the limit to grain
Below this maximum value, tuber Zn concentrations Zn concentration could be increased by higher
were greater in crops that had received multiple smaller applications of N-fertiliser (Kutman et al., 2010; 2011a,b;
applications than a single large foliar application of Shi et al., 2010). However, increasing the N-fertilisation
 P. J. WHITE, M. R. BROADLEY, J. P. HAMMOND, G. RAMSAY, N. K. SUBRAMANIAN, J. THOMPSON 127
and G. WRIGHT

FIG. 5
The relationships between tuber Zn concentration and tuber N concentration in a core collection of 23 commercial potato genotypes grown in field
trials performed on SCRI farms in 2006, 2007, 2008, and 2009. Genotypes were grown in two replicate plots and data points represent individual
replicates (n = 46).

of potatoes increases vegetative growth and delays et al., 2009; Luis et al., 2011). Potato genotypes grown on
maturity, which can reduce tuber yields (e.g., Neeteson SCRI farms without the application of Zn-fertiliser
and Wadman, 1987; Zebarth and Rosen, 2007; McPharlin generally have mean Zn concentrations of 7 – 16 mg kg–1
and Lancaster, 2010; Šrek et al., 2010). Nevertheless, if Zn DM in commercial-grade tubers (Figure 5; White et al.,
bio-fortification was the principal concern, then this 2009; Subramanian et al., 2011). Assuming a DM:FW
strategy might be pursued. Increased N-fertilisation has ratio of 0.21 (USDA, 2010) this would supply 2.7 – 6.1%
been shown to increase tuber Zn concentration (Hlusek of the daily Zn requirement of adult human males in a
et al., 1997). It is noteworthy that there were significant 200 g FW portion, provided both the flesh and the skin
positive relationships between tuber Zn concentration were consumed. The application of foliar Zn-fertiliser
and tuber N concentration in all SCRI field trials increased tuber Zn concentrations to approx. 25 – 30 mg
incorporating the core collection of 23 commercial kg–1 DM (Figure 3; Figure 4), which would supply
potato genotypes (Figure 5). The latter observation between 9.5 – 11.5% of the daily Zn requirement of adult
supports the hypothesis of co-transport of Zn and N- human males in a 200 g FW portion. Since the
compounds in the phloem of potato plants. Furthermore, bio-availability of Zn in potato tubers is potentially high
tuber N concentrations can be increased rapidly by foliar (White et al., 2009), foliar Zn-fertilisation could provide
applications of urea, which minimises N losses to the a simple strategy to increase Zn levels in diets dominated
environment (e.g., Witte et al., 2002). It is also possible by potato.
that potato genotypes that have higher tuber Zn
concentrations in the absence of Zn-fertilisation This work was supported by the Scottish Government.
(Randhawa et al., 1984; Hlusek et al., 1997; Ereifej et al., Nithya K. Subramanian acknowledges financial support
1998; Tekalign and Hammes 2005; Bethke and Jansky from the International Office, University of Nottingham
2008; White et al., 2009) might also have even higher for a Research Scholarship, and SCRI for an SCRI -
tuber Zn-concentrations following foliar Zn-fertilisation. Universities Ph.D. Scholarship. We thank Professor John
It has previously been estimated that 200 g FW of H. Beattie (Rowett Institute of Nutrition and Health,
UK-grown potato tubers can supply 5.5% of the daily Zn University of Aberdeen) for the challenge of bio-
requirement of adult human males (White et al., 2009). A fortifying potato tubers with zinc, Ralph Wilson and
similar percentage contribution can be calculated for Euan Caldwell for help with field trials, and Mark Tucker
potato tubers produced in other countries (e.g., White (Yara, Grimsby, UK) for supplying Zintrac 700.
128 Bio-fortification of potato with zinc

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