Xylem and Phloem Transport of Mineral Nutrients from Solanum tuberosum Roots

Author(s): D. P. NELSON, W. L. PAN and V. R. FRANCESCHI

Source: Journal of Experimental Botany, Vol. 41, No. 230 (September 1990), pp. 1143-1148
Published by: Oxford University Press
Stable URL: http://www.jstor.org/stable/23695117
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Journal of Experimental Botany, Vol. 41, No. 230, pp. 1143-1148, September 1990

Xylem and Phloem Transport of Mineral

Nutrients from Solanum tuberosum Roots

D. P. NELSON1-3, W. L. PAN1 and V. R. FRANCESCHI2

1 Department of Agronomy and Soils, Washington State University, Pullman, Washington 99164-6420, USA

2 Department of Botany, Washington State University, Pullman, Washington 99164-4230, USA

Received 24 January 1990

ABSTRACT
The xylem and phloem transport of mineral elements from stem nodal roots to the stem and stolon of growing potato
(Solarium tuberosum L. cv. 'Russet Burbank') plants was investigated. Adventitious roots, originating from below-ground nodes of
the stem of potato seedlings, were exposed to solutions of SrCl2 or MnS04. Relative elemental concentrations were measured in
the conductive tissues using energy dispersive X-ray analysis. After a 5 h daylight uptake period, Sr (a Ca-transport analogue)
levels were elevated in the stem xylem tissue, but Sr did not increase in the stem phloem, nor was it present in either of the
conductive tissues of stolons located 1-2 nodes above the treated roots. In contrast, elevated levels of Cl, S, and Mn were found
in stolon xylem and phloem tissue during the same period. The absence of Sr in the stolon after 5 h suggests that no xylem flow
into the stolon occurred during the uptake period and, furthermore, phloem flow is responsible for the transport of the Cl, S, and
Mn into the stolon. Elevated levels of these mobile nutrients in the xylem of the stolon were attributed to xylem-to-phloem
transfer in the stem or leaves, transport to the stolon in the phloem, and phloem-to-xylem transfer in the stolon. During a 19 h
uptake period, some Sr was observed in the phloem tissue of the stem, demonstrating slow exchange of Sr with sieve elements or
proximal phloem parenchyma and companion cells.

Key words: Calcium, manganese, X-ray analysis.

INTRODUCTION

The mobility of an element in the phloem affects its of tomatoes and lettuce leaves, which are phloem-fed
delivery to plant organs exhibiting low transpiration rates. organs, even when the plants are cultured in a medium
Nutrient mobility in the phloem is directly related to its containing adequate Ca for otherwise normal plant
concentration in the phloem sap (Raven, 1977). While Ca, growth (Marschner, 1983; Scaife and Clarkson, 1978).
B, and Sr are found in low concentrations in phloem sap, Calcium deficiency during potato tuber growth can
other elements such as K, CI, and S are found in relatively decrease the quality of the tuber (Simmons and Kelling,
high concentrations in the phloem. Elements generally 1987; Tzeng, Kelman, Simmons, and Kelling, 1986; Ar
considered to be intermediate in phloem mobility include teca, Poovaiah, and Hiller, 1980). Therefore, knowledge
Mn, Zn, Fe, and Cu (Ziegler, 1975). While these elements of the pathway of Ca movement to the tuber is important
can be transported by the xylem along the transpiration to the development of practical strategies to prevent Ca
stream, many organs such as fruits and underground deficiency-related disorders. Several transport pathways
storage organs exhibit very low transpiration rates. Con- have been suggested. Davies and Millard (1985) have
sequently, these tissues receive their nutrient elements calculated, based on the Ca : sucrose ratio in phloem sap,
primarily through the phloem (Marschner, 1983). Com- that although the concentration of Ca is quite low,
pared to other plant tissues, organs that are primarily phloem flow is sufficient to account from 12% up to 100%
phloem-fed tend to contain similar concentrations of K of the total Ca found in the tuber. The tuber is generally
and Mg, but substantially lower concentrations of Ca. considered a non-transpiring organ and would, therefore,
This may be related to the observations that physiological receive nutrient elements primarily via phloem flow,
disorders related to Ca deficiency may develop in the fruit Kratzke and Palta (1985) used dyes to demonstrate a

3 Present address: Soiltest Farm Consultants, 2925, Wapato Drive, Moses Lake, WA 98828, USA.

Oxford University Press 1990

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1144 Nelson et al.Xylem-Phloem Transport in Potato
marked absence of xylem flow to the tuber. Subsequent of Sr as a Ca analogue should enhance the sensitivity of the
split-root experiments indicated that Ca added to the procedure due to the low background levels of Sr in most plants
stolon and tuber region increased Ca concentration in the an(J s0ll,s- Stem nocal r,00ts originating from 1-2 nodes below a
. t i j i .i i i , , , , stolon bearing a developing tuber were placed m test tubes
tuber, while Ca supplied to the basal root section had no containing eifher SrCl2 r 5MnSC,4. After the uptake period,
effect on Ca accumulation in the tuber (Kratzke and sections of root from 2-0 cm above the solution, stem 1-3 cm
Palta, 1986). Baker and Moorby (1969) have shown that above the node of the treated root, and tuber-bearing stolon
small amounts of radiolabelled Sr supplied at high con- located 1-2 nodes above the treated root, were cut from the
centration to the root system can enter the tuber. The Plant and immediately frozen in a 1: 9 (v:v) solution of methyl
a ^ * i . . . cyclohexane and 2-methyl butane chilled in a liquid nitrogen
influx mostly occurred at night when the transpiration th Because of the solJble nature of the elemen4ts of inter*st>
demand of the shoot is minimal. They concluded that no fixative solutions were employed. Without thawing, the tissue
xylem flow at night provides an important pathway for samples were freeze-cleaved, and lyophilized. It was assumed
transport of phloem immobile elements to the tuber. In that the rapid freezing and lyophilization prevented the leakage
addition, Kraus and Marschner (1971) gathered evidence of io,ns from tissue during preparation They were then mounted
. , . , , , , on aluminium stubs and carbon coated for X-ray analysis, using
suggesting that much of the tuber Ca is absorbed directly an ETEC Autoscan SEM equipped with a Keex 7f/0o energy
through the periderm. dispersive X-ray analysis unit. The accelerating voltage was
The present study was conducted to obtain direct 20 kV. The detector and specimen were oriented in the same
evidence regarding the transport pathway of elements of manner for each analysis. Deadtime was adjusted to approxi
varying phloem mobility from the root to the tuber. A nialel>'40%; Magnification was kept constant at 500 x for each
, . . /or-TkiTx i j specimen, the stage was tilted 45 towards the detector, the
scanning electron microscope (SEM) coupled with energy ^.orklng distance *was kept at the 12 mm scttlngi and scans
dispersive X-ray analysis (EDXA) was used to identify were generated over an equal area (approximately 35 j.m square)
xylem and phloem tissues of roots, stems, and stolons, and each time using the reduced area mode and a 50 s acquisition
to measure relative elemental concentrations in each type time.
of conductive tissue Two uptake experiments were conducted. In experiment I,
roots of three plants were placed in 50 mM solutions of either
uateriaic a xrn ucTHnnc MnS04 or SrCl2 for 19 h, beginning in mid-afternoon (15.00 h)
MA1ER1ALS AND METHODS and endng the ngxt morning (10.00 h). In experiment II, three
Potato {Solanum tuberosum L. cv. 'Russet Burbank') plants used replicate plants were exposed to 10 mM MnS04 or SrCl2
in this study were cultured in a greenhouse from cores 10 mm in solutions for a daytime uptake period of 5 h. X-ray spectra
diameter by 10 mm long containing one 'eye' cut from certified integrations at energy level windows for Sr, Mn, CI, and S were
Russet Burbank seed tubers. The cores were rinsed in a dilute collected for at least three locations within each vascular tissue
hypochlorite solution, dusted with Captan fungicide, and type (xylem and phloem) for each organ (stem, root, and
planted in vermiculite. The plants were kept at 25 C for the 14 h stolon). In potato stems and stolons, phloem is located both
daylight period and 18 C for the 10 h dark period. Lamps interior and exterior to the xylem. Phloem tissue samples were
producing approximately 70 /E m 2s 1 PAR at leaf level were randomly examined without regard to its proximal location to
used to supplement the winter daylight. Five to seven weeks after the xylem. Peak integrations for the same treatment, vascular
emergence, plants were selected for use in the experiments. tissue, and organ were averaged. For experiment I, counts from
Preliminary microscopic studies were conducted to become tissues from a plant which received only distilled water in the
acquainted with the appearance, relative location, and distribu- uptake solution were subtracted from the counts obtained from
tin of the xylem and phloem tissues in the various regions of the analogous tissues from plants which received the salt solution
plant. A gold coating procedure was used to prepare tissues treatments. In the second experiment, counts from Sr and CI
which could retain the distinctive characteristics of the various windows collected from the MnS04-treated tissues were sub
cell types during prolonged periods of study without destruction traded from the counts from the Sr and CI windows in the
of the cellular integrity. Small specimens from the root, stem, SrCl2-treated tissues. Similarly, Mn and S counts from the
and stolon of a potato plant were fixed in a solution of 3% SrCl2-treated plants were subtracted from the Mn and S counts
glutaraldehyde and 2% paraformaldehyde in 50 mM cacodylate collected from the MnS04-treated plants. In experiment I, little
buffer (pH 7 0) for 18 h at 4 C. They were then post-fixed in 1 % difference in background counts were obtained by using dis
osmium tetroxide in the cacodylate buffer overnight at 4 C. The tilled water or the opposite salt in the uptake solution. There
samples were dehydrated with an ethanol series, freeze-cleaved forc, the distilled water control was omitted from experiment
in liquid nitrogen, critical-point dried, and sputter-coated with n, and the opposite ion solutions were used for determining
gold. Microscopic examination was conducted on an ETEC background counts.
Autoscan SEM at 20 keV accelerating voltage. Photographs of
the tissues of interest were taken to help identify the same tissues RESULTS

The uptake of elements was studied on young plants with Xylem tissue was easily identified regardless of the fixation
small tubers just forming. Phloem mobile elements, S and Cl, a procedure employed. The characteristic patterns pro
phloem immobile element, Sr, and an element of intermediate duced by the secondary cell wall thickenings were easily
phloem mobility, Mn were used for comparison. Sr has been identified (Plate 1A, B, C). With the cacodylate and
used to model Ca in numerous studies (Baker and Moorby, tt,
i t.- j c , ,o osmium fixing procedure, the cellular contents were quite
1969; Drew and Fourcy, 1986; Franceschi and Schueren, 1986) ^ . , ... . ... .
and is assumed to behave similarly to Ca in transport processes. apparent; appearing as web-like or spongy material within
Although differences in Ca levels in the tuber have been the cell (Fig. 1a). Properly lyophilized frozen tissue
measured with the EDXA method (Arteca et al., 1980), the use samples (Plate 1C) appeared very similar to the chemically

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 Nelson et al.Xylem-Phloem Transport in Potato 1145

:-$

Pifeg;"

safe
SBrjj

Plate 1. (A) Scanning electron micrograph of a longitudinal section of chemically fixed, gold-coated potato (Solarium tuberosum L. cv. 'Russet
Burbank') stem at a stolon node. Note the characteristic secondary cell wall patterns of xylem tissue (X) and the phloem parenchyma cells (P) rich in
cytoplasmic contents. (B) Scanning electron micrograph of a transverse section of freeze-dried, carbon-coated vascular tissue of a potato root at the
same settings used to obtain X-ray data. Counts were collected over an area approximately 35 /m2. (C) Scanning electron micrograph of a transverse
section of freeze-dried, carbon-coated vascular tissue of potato stem at a root node. Note close proximity and intermingling of xylem (X) and phloem
(P) tissues. (D and E) Typical X-ray spectra photographed directly from Kevex monitor. The abscissa represents wave energy, ranging from
approximately 5 to 10 kEV. The ordinate represents the relative quantity of X-rays of each energy. The uneven baseline is a result of bremsstrahlung.
(D) Spectrum of xylem tissue from a root approximately 2 0 cm above MnS04 solution. (E) Spectrum of xylem tissue from a root approximately 2-0 cm
above SrCl2 solution. Note the peaks associated with wave energies characteristic of Mn, Sr, S, and CI.

fixed samples; however, resolution at higher magnifica- xylem vessels. Phloem parenchyma and companion cells
tions was poorer due to sample charging. contain much cytoplasmic material. In potato stems,
Phloem tissue was more difficult to identify, especially phloem is located both interior and exterior to the xylem
as no sieve plates were observed. Sieve elements do not as well as intermingled with the xylem. Phloem tissue
have the secondary wall thickenings characteristic of frequently developed a slight charge and would appear as

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1146 Nelson et al.Xylem Phloem Transport in Potato

COUNTS (xlO3)
(xIO3) In reviewing these figures, it must be pointed out that the
10 | ordinate values of one element cannot be directly com
root tissue M stem tissue 19 hr. 19uptake
ROOT TISSUE M STEM TISSUE
hr. uptake
pared to those of another element. The ordinate values
indicate the amount of element present relative to the
rh
background level of a similar plant tissue which did not
[+1
rh rln receive experimentally an additional supply of the element
of interest.
Experiment I included a 19 h uptake period and collec
tion of tissue samples from the root directly above the
treatment solution as well as from the stem above the
root-bearing node. Figure 1 shows the change in relative
element content from the root to the stem after the 19 h
uptake period for the solutions of SrCl2 and MnS04.
Sr Cl
CI Mn S Sr Cl
CI Mn S Other than CI in the stem tissue, the relative amounts of
XYLEM PHLOEM each element in the xylem tissue are similar to those found
Fig. 1. Relative concentrations of Sr, CI, Mn and S in root and stem in the phloem. The S concentration is the same in the
vascular tissues of potato after 19 h exposure of a single potato root to xylem tissue of the root and the stem. On the other hand,
50 mM SrCl2 and MnS04 solutions. Counts were collected and corrected
Sr, CI, and Mn levels were markedly lower in the stem
for background as described in the text. The height of the bar graphs
represent the corrected mean values with error bars indicating standard
vascular tissue relative to the root.
error of the differences between treated plants and control plants. In experiment II, lower concentrations of the solutions
were allowed to be taken up for 5 h during the daytime. Sr
very bright areas on the video screen and photographs levels in the xylem and phloem of the root were about the
(Plate IB). A few cells, probably sieve tubes, can be seen same, but the Sr concentration in the phloem dropped
which have very little cytoplasm. Plate ID is a photograph well below that in the xylem of the stem (Fig. 2). In the
of the Kevex monitor representing a typical X-ray spec stolon, Sr concentrations in the xylem and phloem were
trum obtained from a SrCl2 treatment and Plate IE is not significantly different from background. Chloride
from a MnS04 treatment. Data presented in this study are levels in the xylem and phloem were very similar, and CI
based on peak integrations collected from 'windows' or was similarly elevated in both the root and stem tissues by
energy ranges characteristic of the four elements of in the SrCl2 treatment. The CI level in the vascular tissues of
terest; Plates ID and IE are included as examples of the the stolon was approximately double that of the root
relative peak heights and background levels. tissues. Manganese followed a pattern very similar to that
X-ray counts of each of the elements give an indication of Sr, except that Mn levels in both the xylem and phloem
of relative mobility among tissues and organs (Figs 1, 2). of the stolon were slightly elevated above background.
Sulphur levels in both the xylem and phloem were below
background in the roots and slightly above background in
COUNTS (x103)
the stolon. In the stem sections, S levels in the phloem
were above background while S levels in the xylem were
well below background.

DISCUSSION

The elevated levels of Sr in the xylem tissues of the root

and stem but not in the stolon in experiment II (Fig. 2)
indicate that little xylem flow to the tuber occurred during
the 5 h uptake period. As this experiment was conducted
during daylight hours, it is likely that leaf transpiration
provided the dominant driving force for xylem flow.
Baker and Moorby (1969) were unable to detect the
Sr Cl
CI Mn S Sr Cl
CI Mn S entrance of radiolabelled Sr into the stolon during day
XYLEM PHLOEM light hours. In the present experiment, phloem transport
of Sr was insignificant as Sr levels were not above the
Fig. 2. Relative concentrations of Sr, CI, Mn, and S in root, stem, and
stolon (rhizome) vascular tissues of potato after 5 h exposure of a stem background in the phloem in any of the tissues examined
nodal root to 10 mM SrCl2 and MnS04 solutions. Counts were collected except in the root immediately above the SrCl2 solution.
and corrected for background as described in the text. The height of the The latter may have been due to root injury or apoplastic
bar graphs represent the corrected mean values with error bars indicat
flow.
ing standard error of the differences between treated plants and control
plants. Based upon these observations, nutrient elements sup

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 Nelson et al.Xylem-Phloem Transport in Potato 1147

plied to the tuber during daylight hours must be delivered parently, a considerable amount of sulphate was trans
in the phloem. Manganese, in contrast to Sr, was found in ported to the leaves via the xylem, reduced in the leaves,
concentrations elevated above background in both the loaded into the phloem and retranslocated to the expand
xylem and phloem of the stolon (Fig. 2). Chloride was ing stolon. As the tuber is a storage organ for protein as
found at greatly elevated levels in both the xylem and well as starch this proposed rapid assimilation of
phloem of the stolon. Phloem-to-xylem transfer is a absorbed sulphate is not unreasonable,
possible explanation for the observation that Mn and CI Stark and Halderson (1987) measured diurnal tuber
were found in stolon xylem tissue but not Sr. These more volume changes on the order of 20% of the tuber
phloem-mobile elements could be transferred to the volume. Similarly, Baker and Moorby (1969) measured
phloem, translocated to the stolon, then transferred back weight increases at night of approximately 10% of tuber
to the xylem. Pate (1986) demonstrated the frequency and fresh weight. The Ca concentration of potato tubers
importance of xylem-to-phloem transfer in the N budget ranges from 0-5 to 2-0 mg g"1 dry weight (using Bret
of Lupinus alhus L. It follows that opportunity may exist zloff, 1971, fresh weight data and 20% dry matter),
for phloem-to-xylem transfer to occur for other mineral Kunkel, Holstad, and Russell (1973) measured 21% dry
nutrients as well. The intimate spatial association of xylem matter in mature tubers and a corresponding Ca concen
and phloem tissues (Plate IB, C) lends support to the tration of approximately 1-6 mgg"1 dry weight. Kirkby
possibility for this transfer to occur. (1979) listed a potato tuber Ca level of 0-8 mg g"1. Our
After 19 h, Sr was found well above background in measurements of internal tuber Ca levels of field-grown
both the xylem and phloem of the stem tissue. It can be plants (unpublished) are similar to this latter value,
seen from Plate 1C that even the reduced area from which Calcium concentrations in xylem sap have been
the counts were collected was not limited to only one sieve measured to be 40 mg dm"3 for Triticum aestivum L.
element, but overlapped adjacent phloem parenchyma (Gartner, LeFaucheur, Roinel, and Paris-Pireyre, 1984),
and companion cells. Indeed it was by the appearance of 150 to over 350 mg dm"3 for Brassica olercea L. cv.
these cells that phloem tissue was identified. As a conse- italica (Shelp, 1987), 47 mg dm"3 for Spartium junceum
quence, sieve elements could not be separated from these L., and 95 mg dm"3 for Lupinus albus L. (Pate, Sharkey,
surrounding types of phloem cells. As pointed out by and Lewis, 1975). The above values can be used to
Raven (1977) the immobility of Ca (and Sr) in the phloem calculate potential contributions of xylem flow to Ca
is due to its active export from the cytoplasm, binding or delivery to developing tubers. If it is assumed that a
chelation to immobile cell structures, and precipitation as 300 g tuber develops at a linear growth rate over 75 d
phosphates or carbonates in the cell wall. Thus, over the and 10% fresh weight increases occur nightly as a result
longer time of this part of the experiment, Sr would be of xylem sap influx, then a calculated 1140 cm3 of xylem
expected to accumulate, or at least to equilibrate between fluid enters the tuber over the entire growth period. If
the importing xylem tissue and the cells surrounding the this were the sole source of Ca delivered to the tuber, Ca
sieve elements. These results do not preclude the possible concentrations in the xylem would need to be on the
movement of Sr transport in the sieve elements during the order of 210 mg Ca dm"3, well within the range of
19 h exposure. xylem Ca concentration measured in other species. If a
The accumulation of Mn and CI in the root tissue similar range exists in potato, then it appears that xylem
relative to the stem after 19 h may indicate that these flow may potentially supply up to 100% of the Ca
elements accumulate in the apoplast of the root but are requirements of a typical potato tuber. These calcula
not translocated into the xylem vessels as readily as S. tions were based on the assumptions that (1) all noctur
Sulphur levels in the xylem as well as the phloem were nal weight gain or volume increase was due to xylem
somewhat above background levels in both the root and inflow, and (2) all Ca carried into the tuber at night
stem. This indicates that S, in contrast to Mn and CI, was remained in the tuber when leaf transpiration resumed
readily exported in the xylem from the root and also the next day. If either of these assumptions are compro
readily moved to the phloem tissue. These results may also mised, higher Ca concentrations in the xylem would be
reflect plant uptake responses to the elevated salt concen- required to maintain adequate tuber Ca levels via this
tration (50 mM). pathway.
The appearance of elevated levels of S in the phloem
tissue of the stolon after only 5 h is unlikely to be ACKNOWLEDGEMENTS
sulphate-S. Ziegler (1975) indicated that sulphate is not The SEM and EDXA work was conducted at the Electron
transported to any major extent in the phloem, rather Microscopy Centre, Washington State University. The
most S in the phloem is in organic forms. The Sr results authors would like to thank the staff at the Centre for
suggested that there was no xylem flow to the stolon and, their assistance. This research was partially funded by the
therefore, little sulphate was likely to have reached the Washington Potato Commission and the Washington
phloem parenchyma by transfer from xylem tissue. Ap- State Agricultural Research Centre.

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1148 Nelson et al.Xylem-Phloem Transport in Potato
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