Annals of Botany 88: 555±561, 2001
doi:10.1006/anbo.2001.1497, available online at http://www.idealibrary.com on
The Importance of Phellogen Cells and their Structural Characteristics in
Susceptibility and Resistance to Excoriation in Immature and Mature
Potato Tuber (Solanum tuberosum L.) Periderm
E D WA R D C . L U L A I * { and T H O M A S P. F R E E M A N {
{USDA-ARS, Northern Crop Science Laboratory, P.O. Box 5677, University Station, Fargo, ND 58105-5677, USA
and {North Dakota State University, Northern Crop Science Laboratory, P.O. Box 5677, University Station, Fargo,
ND 58105-5677, USA
Received: 10 April 2001
Returned for revision: 13 May 2001
Accepted: 13 June 2001
Published electronically: 17 August 2001
Potato tuber (Solanum tuberosum L.) periderm maturation is an important physiological process that directly a€ects
the susceptibility and development of resistance to costly excoriation (skinning-type wounds) at harvest. The objectives
of this research were to identify the speci®c types of cells and the cellular changes associated with susceptibility and
resistance to tuber excoriation in immature and mature tubers respectively. Epi¯uorescent microscopic examination of
immature tuber periderm ( phellem, phellogen and phelloderm cells) from several genetically diverse cultivars has
shown that the cellular damage resulting from excoriation occurs within the phellogen (cork cambium), a meristematic
layer of cells that gives rise to neighbouring phellem and phelloderm cells. Tuber excoriation is the result of the fracture
of radial phellogen cell walls linking the skin ( phellem) to the phelloderm. As the tuber periderm matures, phellogen
cells become inactive and the radial walls of these cells become more resistant to fracture; resistance to excoriation
develops. Ultrastructural studies of immature tuber periderm show that radial walls of active phellogen cells are thin
and fragile. During periderm maturation, both radial and tangential phellogen cell walls thicken as they strengthen and
become resistant to fracture, thereby providing resistance to excoriation. These results refute previous theories of the
physiological changes responsible for the onset of resistance to tuber skinning injury. The combined results establish a
paradigm whereby the thickening and strengthening of tuber phellogen cell walls upon periderm maturation are the
determinant for resistance to tuber excoriation.
Key words: Cambium, meristematic, periderm, phellem, phelloderm, phellogen, potato, skinning, Solanum
tuberosum L., 0tuber.
I N T RO D U C T I O N
Potato tuber periderm is of great agricultural importance
and scienti®c interest because of the protection a€orded by
the intact periderm to the tuber against pathogens and
dehydration (Soliday et al., 1979; Peterson et al., 1985; Lulai
and Orr, 1994, 1995; Lulai and Corsini, 1998). The periderm
covering immature tubers is very fragile and is susceptible to
wounding by excoriation (idiom ˆ skinning); this type of
wounding is a serious and costly problem at harvest (Lulai
and Orr, 1993). The term skinning is poorly and anecdotally
de®ned and has been used to imply that the entire periderm
is physically detached from the underlying tuber cells. The
term excoriation is interchangeable with the term skinning
in describing this type of wound, but without the
anecdotally derived implications and de®nitions. Maturation of the periderm, during and after potato vine
desiccation, is an important physiological process that is
directly related to the development of resistance to excoriation (Lulai and Orr, 1993). Although slow or hindered
* For correspondence. Fax 001 7012391349, e-mail [email protected].
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development of resistance to excoriation during periderm
maturation constitutes a serious problem, the anatomical
and physiological basis for susceptibility and resistance of
the potato tuber to skinning injury has not been addressed
scienti®cally.
Confusion and uncertainty concerning tuber periderm
physiology remains. Reeve et al. (1969) indicated that potato
tuber periderm is composed of: (1) phellem (suberized cells);
(2) phellogen (cork cambium); and (3) phelloderm tissues.
Lyshede's (1977) analysis of mature tuber periderm did not
produce de®nitive evidence for the presence of a phellogen
or phelloderm. The suberization processes involved in
phellem development are only partially characterized
(Kolattukudy, 1984; Lulai and Morgan, 1992; Thomson
et al., 1995; Bernards and Lewis, 1998; Lulai and Corsini,
1998). There are no published data identifying or relating
maturational changes in phellem, phellogen or phelloderm
to susceptibility and resistance to tuber excoriation. Perhaps
more importantly, there is no information on the changes
that occur in phellogen cell walls when the cork cambium
becomes inactive. The lack of information on the type of
periderm cells and cellular changes that are responsible for
susceptibility and resistance to excoriation has hampered the
development of e€ective, rational approaches to describe
556
Lulai and FreemanÐPotato Periderm Maturation
periderm maturation and to solve the costly problem of
tuber skinning injuries that occur during harvest.
The skin of the potato tuber is the protective part of the
tuber surface tissue that is easily excoriated from immature
tubers. Although the skin is an important part of the
periderm, it has not been clearly identi®ed or de®ned scienti®cally and it is often mistakenly referred to as constituting
the total tuber periderm. The confusion surrounding
excoriation and use of the terms `skin' and `skinning' has
been exacerbated because skin thickness and suberization
have been proposed to be responsible for susceptibility and
resistance to tuber excoriation in immature and mature
tubers (Hiller et al., 1985; de Haan, 1987; Hiller and
Thornton, 1993). However, these theories arose anecdotally
and have not been researched or con®rmed scienti®cally.
Controlled environment studies have shown that low
relative humidity hastens periderm maturation in freshly
harvested tubers (Lulai and Orr, 1993) and that periderm
maturation is more rapid in tubers from cultivars with
characteristically higher water vapour loss (Lulai and Orr,
1994). Consequently, the ®rst layer of fully hydrated cells
within the periderm, i.e. the phellogen, should play an
important role in tuber periderm maturation and excoriation. However, there is no published information on the
changes that occur within the cork cambium/phellogen of
potato tuber periderm as growth ceases and as the periderm
matures. Extensive studies have been conducted on the
structure, ultrastructure, cytology and biochemistry of the
vascular cambium of woody plants and taproots as plants
cycle through dormancy and growth. These are periods
when the vascular cambium correspondingly cycles from
inactive to active meristematic activity (Catesson, 1994;
Catesson et al., 1994; Cha€ey et al., 1997, 1998; Lachaud et
al., 1999). Similar information is not available for cell walls
of meristematically active and inactive cork cambium/
phellogen from potato tuber or other plants. However,
changes in cell wall architecture of the vascular cambium
from perennial plants may only serve as a partial model for
the cork cambium/phellogen from periderm tissues of
annual plants such as potato tubers.
We conducted a series of experiments with several potato
cultivars raised during three growing seasons to identify the
type of periderm cells and cellular characteristics that are
responsible for susceptibility to tuber excoriation, or skinning injury, and the changes responsible for the development of resistance to skinning injury. The terms `skin' and
`skinning' are rede®ned and a structural model for skinning
and resistance to skinning (skin-set) is presented. These
results are requisites to the identi®cation of the biochemical
processes and mechanisms that regulate the development of
resistance to tuber excoriation.
M AT E R I A L S A N D M E T H O D S
Potato cultivars
Potato tubers from cultivars with diverse genetic backgrounds were sampled from plants grown using standard
cultural practices in non-irrigated ®elds during three growing
seasons. The results presented were obtained from cultivars
with rapid (`Goldrush' and `Russet Norkotah') and slow
(`Red Ruby' and `Kennebec') periderm maturation (Lulai
and Orr, 1993, 1994). Tubers that were immature (susceptible to excoriation/skinning), maturing or approaching
periderm maturity (developing resistance to excoriation/
skinning) were sampled from growing plants, senescing
plants and plants whose vines were dead and desiccated,
respectively. Harvested tubers were stored in controlled
environment chambers (95 % relative humidity and 9 8C) to
allow postharvest sampling when the periderm was fully
mature (resistant to skinning). The periderms of the sampled
tubers were examined microscopically to identify the cellular
layers damaged during skinning and to determine the
structural characteristics of these cells before and after
development of resistance to skinning. The periderm
properties observed in this study were similar for all growing
seasons.
Determination of resistance to excoriation (skinning injury)
in relation to phellogen activity
The time course for development of resistance to
skinning injury in comparison to phellogen activity was
determined objectively using a mechanical skin-set (resistance to skinning/excoriation) measuring device described
by Lulai and Orr (1993). The device measured the amount
of torsional force (milliNewton meters) required to produce
skinning injury.
Phellogen activity was determined in a manner similar to
that described previously for vascular cambium activity, as
reviewed and described by Larson (1994b). Brie¯y, this
activity value was determined by counting the number of
active phellogen cells and nascent phellogen derivatives in a
segment of the cork cambial layer and dividing by the total
number of columns of adjoining phellem cells produced
from this phellogen. These calculations provided the
number of cell layers associated with active phellogen that
gave rise to a single column of phellem cells. The measured
changes in resistance to skinning injury and phellogen
activity occurred over the time course of periderm maturation during and after potato vine desiccation and autumn
harvest.
Tissue sampling, preparation and histochemical analysis for
¯uorescence microscopy
At each sampling time six tubers from each cultivar were
rinsed in distilled water. Tissue blocks (2 mm 3 mm 4 mm deep) of periderm and neighbouring cortical tissues
were excised from the equatorial region of each tuber surface
and ®xed in a solution of formalin : acetic acid : 95 %
ethanol : water (3 : 1 : 10 : 7, v/v/v/v). Excoriated samples
were obtained from tubers whose periderm had separated
naturally and from undamaged portions of the same tubers
which had the layer of skin gently pulled from the tuber with
a pair of forceps; these approaches produced identical tissue
injury. Fixed tissues were dehydrated in a tertiary-butyl
alcohol series, embedded in paran (Paraplast Plus, Sigma,
St. Louis, MO, USA), sectioned and deparanized as
described previously (Lulai and Morgan, 1992). The
Lulai and FreemanÐPotato Periderm Maturation
following histochemical treatments were employed as outlined previously (Lulai and Morgan, 1992): berberine and
ruthenium red were used to identify suberin polyphenolic
accumulations; neutral red and toluidine blue O were used
to identify suberin polyaliphatic accumulations; and Sudan
III/IV to stain polyaliphatic accumulations a faint pink
while maintaining pale yellow auto¯uorescence of the
polyphenolic accumulations. Light microscopy was performed as outlined previously (Lulai and Morgan, 1992)
using a Zeiss Axioskop 50 microscope con®gured for
epi¯uorescent illumination using the model 100 illuminator
equipped with an HBO 50 W/L2 mercury lamp. Blue-violet
excitation was employed for neutral red and berberine
induced ¯uorescence, and Sudan III/IV colouration and
auto¯uorescence (exciter ®lter BP 436/10, dichromatic
beam-splitter FT 460, barrier ®lter LP 470).
Tissue sampling and preparation for electron microscopy
Sampling for ultrastructural studies included: (1) immature tubers that were freshly harvested and susceptible to
skinning injury; and (2) mature tubers that had aged and
were resistant to skinning injury. For transmission electron
microscopy (TEM), samples from six tubers of each
cultivar were prepared by removing a small block
(8 mm 4 mm 4 mm deep) of the periderm and adjoining cortical tissue. Each of these samples was then placed in
0.1 M phosphate bu€er ( pH 7.4) and was subdivided into
approx. 2 mm cubes and ®xed for 20 h in bu€ered 2.5 %
glutaraldehyde, washed in phosphate bu€er, and post®xed
for 6 h at 22 8C in phosphate-bu€ered 2 % osmium
tetroxide. Samples were dehydrated in a graded acetone
series and stained en bloc with saturated uranyl acetate in
70 % acetone prior to being embedded in Spurr's resin.
Ultrathin sections (600 to 8008A) were cut with a diamond
knife. Obliquely cut sections do not give rise to the
appearance of symmetrical cell walls. Consequently, the
tissue blocks were aligned as closely as possible for
sectioning at right angles to the tuber surface. However,
slight obliqueness is unavoidable and these sections can
change the apparent cell wall symmetry. The sections were
stained with lead citrate and examined on a JEOL 100CX
transmission electron microscope.
For scanning electron microscopy (SEM), samples of
each cultivar containing the periderm were cut from the
tuber and placed in acidi®ed 2-2 dimethoxypropane (DMP)
for ®xation and rapid dehydration. Samples were removed
from DMP and were washed with several changes of
absolute ethanol and critical point dried in a Tousimis 810
critical point drier using CO2 as the transitional ¯uid. Dried
specimens were coated with Au/Pd in a Balzer SCD030
sputter coater and examined and photographed using a
JEOL 6300 scanning electron microscope.
R E S U LT S
Fluorescence microscopy of tuber periderm
Fluorescence microscopy of immature potato tuber periderm
shows that periderm damage incurred during excoriation
557
involves the separation of the phellem from the underlying
tissue, and that the phellem constitutes what has loosely
been referred to as the skin (Fig. 1A). At higher magni®cation (Fig. 1B), it is apparent that the separation occurred
within the phellogen and that there was no fracturing or
separation within the layer of suberized cells ( phellem). The
same results were obtained using berberine/ruthenium red
and neutral red/toluidine blue O (micrographs not shown)
to visualize the suberin polymers and thereby identify the
phellem cells. The phellogen interfaces the phellem and
phelloderm. The phelloderm, consisting of a loosely
organized rectangular matrix of cells, can be discerned in
Fig. 1D. The radial walls of the phellogen were susceptible
to fracture (Fig. 1A and B). Careful analysis of the
micrographs of the active phellogen at higher magni®cation
(Fig. 1B and C) shows that the radial and tangential cell
walls appear frail and wispy. The fragility of radial and
tangential cell walls of the active phellogen was also
evidenced by the ease with which they were damaged during
embedding and sectioning, particularly for TEM. Mature
tuber periderm (Fig. 1D) was resistant to skinning injury.
Phellogen cell walls from mature tuber periderm were not
fragile and were indistinguishable from the cell walls of the
adjoining phelloderm which were strong and resistant to
mechanical fracture. Higher magni®cation showed that the
phellogen cell walls of immature tuber periderm were weakly
auto¯uorescent (Fig. 1C). Phellogen cell walls did not
¯uoresce after tandem treatment with suberin ¯uorochromes and auto¯uorescent quenching agents (berberine/
ruthenium red or neutral red/toluidine blue O), indicating
that the walls did not contain suberin lignin-like polyphenolic or polyaliphatic material. Since no ¯uorescent signals
were obtained, these micrographs are not shown.
Electron microscopy of tuber periderm
Results from SEM analysis (Fig. 2A) show the contrasting morphology and integration of the three types of cells
that constitute the periderm: phellem, phellogen, and
phelloderm. The TEM micrographs in Fig. 2B±G reveal
more ultrastructural details relevant to the susceptibility or
resistance of phellogen cell walls to fracture and tuber
skinning injury. In immature periderm, the radial cell walls
of the phellogen were thin compared to the adjoining
tangential phellem cell walls (Fig. 2B). Phellogen radial cell
walls were sometimes folded (Fig. 2C), unlike the rigid
radial walls of the phellem or phelloderm. Folding of these
¯exible walls may have been due to changes in turgor in situ
or may have occurred upon dehydration for tissue
embedding. The fragility of radial phellogen cell walls of
immature periderm was evidenced by their ease of fracture
upon tuber excoriation and during embedding and sectioning (Fig. 2D). Two months after the tubers were harvested
and the periderm was no longer susceptible to excoriation,
i.e. after the periderm had matured, the radial walls of the
inactive phellogen were noticeably thickened and were no
longer prone to fracture (Fig. 2E). Similarly, phellogen
tangential cell walls from mature tubers (Fig. 2F) were
thicker than those from tubers with immature periderm
(Fig. 2G). Plasmodesmata were observed in the cell walls of
558
Lulai and FreemanÐPotato Periderm Maturation
F I G . 1. Periderm tissues: phellem (PM), phellogen (PG) and phelloderm (PD) and neighbouring cortical (C) cells from `Kennebec' tubers. Tissues
were treated with Sudan III/IV to stain phellem cells for identi®cation. The tuber surface is oriented to the top of each micrograph resulting in
tangential walls running horizontally and radial walls running vertically. The Sudan treatment retains intense auto¯uorescence of phellem cell
walls and a low intensity auto¯uorescence of non-suberized cell walls, which facilitates detection of phellogen and phelloderm cell walls.
Figure 1A±C shows immature periderm with active phellogen. Note the separation of the phellem from neighbouring tissues and the fracturing of
phellogen cell walls in Fig. 1A and B (arrowheads). The fragile appearance and the dim auto¯uorescence of the nascent phellogen cell walls is
noticeable in Fig. 1C (arrows). The enhanced contrast of the black and white inset in Fig. 1B helps in the detection of phellogen cell walls and
their fracture (arrowhead). Figure 1D shows cell walls from mature periderm. The cell walls of inactive phellogen in mature periderm (Fig. 1D)
appear more clearly de®ned than the characteristically fragile cell walls of active phellogen (Fig. 1A±C).
inactive phellogen (mature periderm), but were not detected
in the walls of the active phellogen cells (immature
periderm) that we examined.
Resistance to excoriation in relation to phellogen activity
In addition to the changes noted above, our results show
that an inverse relationship exists between the development
of resistance to tuber skinning injury, and the combined
number of layers of active phellogen and immediate/nascent
phellogen derivatives (Fig. 3). As phellogen activity
decreased, the resistance to skinning injury increased.
Results for all experiments were similar for all growing
seasons.
DISCUSSION
In immature tuber periderm, the phellogen is the speci®c
layer of cells that is labile and prone to fracture and allows
separation to occur within the periderm causing excoriation/skinning injury (Fig. 1A and B). Although potato
tuber excoriation during harvest has been a costly and
persistent problem (Murphy, 1968; Hiller et al., 1985; Lulai
and Orr, 1993), this study is the ®rst to identify and describe
the type of tuber periderm cells and cell wall changes
responsible for susceptibility and resistance to tuber
skinning injury. Previous theories incorrectly held that
periderm thickening, skin thickening, or suberization cause
the development of resistance to excoriation during
periderm maturation (Hiller et al., 1985; de Haan, 1987;
Hiller and Thornton, 1993). Our results show that the
phellem constitutes what has loosely been referred to as the
skin, and that periderm or skin thickening and suberization
are not involved in resistance to excoriation because there is
no separation within the phellem upon skinning injury.
Excoriation results in tissue separation that is speci®c to the
layer of phellogen cells.
These microscopical studies of excoriation and periderm
architecture also show the presence of a loosely structured
phelloderm which may be slightly easier to identify in
periderm possessing a meristematically active phellogen,
but can also be detected in mature periderm (Fig. 1A and
Lulai and FreemanÐPotato Periderm Maturation
559
F I G . 2. SEM and TEM micrographs of potato tuber periderm showing phellem (PM), phellogen (PG) and phelloderm (PD) and neighbouring
cortical (C) cells. Tangential walls are arranged horizontally and radial walls vertically. Figure 2A illustrates the contrasting morphology of the
periderm cells and neighbouring cortical cells. The TEM micrographs illustrate the following: Fig. 2B, a radial (R) phellogen cell wall connecting
to a lower tangential (LT) phellem cell wall in immature tuber periderm; Fig. 2C, a radial (R) phellogen cell wall connecting to a lower tangential
(LT) phellem cell wall in maturing tuber periderm; Fig. 2D, a fractured radial (R) phellogen cell wall connecting to an intact lower tangential (LT)
phellogen cell wall in immature periderm; Fig. 2E, a thickened phellogen radial (R) cell wall from mature periderm; Fig. 2F, a thickened lower
tangential (LT) phellogen cell wall from mature periderm; and Fig. 2G, a thin lower tangential (LT) phellogen cell wall from immature periderm.
D). The few cell layers which constitute the phelloderm
show typical phelloderm architecture in that they are
characterized by loosely organized layers of starch-depleted
cells between the phellogen and cortex (Fig. 2A). Earlier
results, which indicated that there was no easily discernable
phelloderm present in potato tuber (Lyshede, 1977), were
Lulai and FreemanÐPotato Periderm Maturation
2.2
‘Norkotah’ phellogen
‘Norkotah’ resistance
‘Kennebec’ phellogen
‘Kennebec’ resistance
2.0
1.8
1.6
450
400
350
1.4
1.2
300
0.0
0.8
250
0.6
0.4
(Torque mN.M)
Resistance to skinning
Phellogen activity
(layers of active phellogen and derivatives)
560
200
0.2
150
0.0
8/31
9/7
9/14 9/21 9/28 10/5 10/12 10/19 10/26 11/2
*
Calendar date
F I G . 3. Relationship between phellogen activity (number of layers of phellogen cells and immediate derivatives) and resistance to excoriation/
skinning injury (torque in mN m ÿ1) for tubers of `Norkotah' and `Kennebec' during the ®nal stages of growth and periderm maturation. Note
that as phellogen activity decreases during periderm maturation, the resistance to skinning injury increases. The arrows pointing diagonally
upward indicate that the resistance to skinning had increased beyond the measurable range of the technique and that the tubers were becoming
very resistant to skinning injury. *, Tubers were harvested late, 28 September, to allow for periderm maturation in the ®eld and were then placed
into a controlled environment chamber (95 % RH and 9 8C) to allow the periderm to mature further until sampled for analysis on 2 November.
obtained with mature tubers, and consequently there was
no active phellogen present for easy anatomical reference.
The fragile, nascent walls of active phellogen of immature
periderm can be distinguished from the walls of inactive
phellogen in mature periderm. Walls of inactive phellogen
were not easily distinguished from walls of adjoining
phelloderm and cortical cells. The walls of inactive
phellogen, adjoining phelloderm and cortical cells were
commonly observed to possess plasmodesmata, but these
were not apparent in the sections of active phellogen that
we examined, suggesting that they are dicult to detect or
are rare in the cell walls of active phellogen. These results
may be considered consistent with the concept of secondary
formation of plasmodesmata proposed for vascular cambial
cells (Larson, 1994a).
Phellogen cell walls change morphologically as the
periderm matures and the phellogen becomes inactive.
The thicker cell walls present in inactive phellogen of
mature periderm (Fig. 2E and F) are apparently stronger
and more resistant to fracture than the noticeably thinner
cell walls of active phellogen cells from immature periderm
(Fig. 2B, D and G). Susceptibility to skinning decreases
during phellogen inactivation. Skinning does not occur in
mature periderm (Lulai and Orr, 1993) which we have
found to be characterized by thickened phellogen cell walls.
The thickening of phellogen walls, especially radial walls,
upon periderm maturation, appears to be a primary
physiological and structural basis for the development of
resistance to tuber skinning. Like the walls of tuber
parenchyma cells, the strong, thickened walls of the inactive
phellogen do not accumulate lignin or lignin-like material
upon periderm maturation.
The nascent radial and tangential cell walls of active
phellogen, unlike the thickened cell walls of inactive
phellogen which resemble phelloderm, did not display a
readily recognizable middle lamella or other morphological
characteristics found in neighbouring phelloderm cell walls
which are thickened and resistant to fracture. A portion of a
middle lamella and stained, electron-dense suberin from a
fully formed neighbouring phellem cell could sometimes be
detected extending a short distance into the thin, nonlamellar adjoining radial wall of meristematically active
phellogen (Fig. 2B). The walls of meristematic cells are not
rigid, but must be elastic to withstand changes in turgor
pressures associated with growth (Iiyama et al., 1994).
Previous results showing a relationship between rapid tuber
water vapour transpiration and rapid periderm maturation
(Lulai and Orr, 1994) are consistent with the completion of
cell growth and may play a role in cell wall sti€ening or
thickening. Cell wall asymmetry was commonly observed in
non-meristematic cells (Fig 2E and F). These di€erences
may be due to the angle of section, physiological activity or
stage of maturation.
The absence of a recognizable middle lamella in the cell
walls of meristematically active phellogen is consistent with
that of tangential walls of meristematically active vascular
cambium (Roland, 1978; Catesson and Roland, 1981).
However, unlike cell walls in the active cambial zone of
hardwood taproots, and shoots which have radial walls that
are noticeably thicker than the adjoining tangential cell
walls (Cha€ey et al., 1997; Lachaud et al., 1999), we found
that radial and tangential cell walls from active tuber
phellogen are equally thin. These di€erences in radial wall
thicknesses are consistent with the patterns of growth for
trees, where the annual growth in height is much greater
Lulai and FreemanÐPotato Periderm Maturation
than that in girth, vs. potato tuber, where vigorous growth is
expressed laterally and longitudinally. Another major
di€erence is that the meristematic activity of the vascular
cambium of these woody plants cycles annually from
dormancy to growth with the vascular cambial cell walls
thickening during dormancy and then becoming thin as
meristematic activity resumes during the growing season
(Lachaud et al., 1999). This reactivation and cycling of
meristematic activity does not occur in the phellogen/cork
cambium of tuber periderm because of di€erences in
biology, including the fact that potato is not a perennial
plant. The biological changes and biochemical processes
associated with phellogen cell wall thickening during
phellogen inactivation are currently being investigated.
In summary, these results de®ne the tuber skin as the
phellem layer of the periderm. The phellogen is clearly
identi®ed as the speci®c layer of periderm tissues directly
involved in tuber excoriation/skinning injury. The cell wall
characteristics that are responsible for susceptibility and the
onset of resistance to tuber excoriation upon potato tuber
periderm maturation are synonymous with active and
inactive phellogen. Excoriation is related to a prototypal
description of the ultrastructural di€erences between active
and inactive tuber phellogen cells. The results provide a
useful model that is the ®rst description of the structural
physiology of immature vs. mature periderm in relation to
potato tuber skinning injury.
AC K N OW L E D GE M E N T S
We thank Thomas J. Wirta, Kathy L. Iverson, Scott A.
Payne and Je€rey L. Miller for their technical assistance.
# 2001 US Government
L I T E R AT U R E C I T E D
Bernards MA, Lewis NG. 1998. The macromolecular aromatic domain
in suberized tissue: a changing paradigm. Phytochemistry 47:
915±933.
Catesson AM. 1994. Cambial ultrastructure and biochemistry: changes
in relation to vascular tissue di€erentiation and the seasonal cycle.
International Journal of Plant Science 155: 251±261.
Catesson AM, Roland JC. 1981. Sequential changes associated with cell
wall formation and fusion in the vascular cambium. IAWA
Bulletin 2: 151±162.
Catesson AM, Funada R, Robert-Baby D, Quinet-Szely M, Chu-Ba J,
Goldberg R. 1994. Biochemical and cytochemical cell wall changes
across the cambial zone. IAWA Journal 15: 91±101.
Cha€ey N, Barnett J, Barlow P. 1997. Endomembranes, cytoskeleton,
and cell walls: aspects of the ultrastructure of the vascular
cambium of taproots of Aesculus hippocastanum L. (Hippocastanaceae). International Journal of Plant Science 158: 97±109.
Cha€ey NJ, Barlow PW, Barnett JR. 1998. A seasonal cycle of cell wall
structure is accompanied by a cyclical rearrangement of cortical
microtubules in fusiform cambial cells within taproots of Aesculus
561
hippocastanum (Hippocastanaceae). New Phytologist 139:
623±635.
de Haan PH. 1987. Damage to potatoes. In: Rastovski A, van Es A et
al, eds. Storage of potatoes: post-harvest behavior, store design,
storage practice, handling. Wageningen, The Netherlands: Pudoc,
371±380.
Hiller LK, Thornton RE. 1993. Management of physiological disorders.
In: Rowe RC, ed. Potato health management. St. Paul, Minnesota,
USA: APS Press, 87±94.
Hiller LK, Koller DC, Thornton RE. 1985. Physiological disorders of
potato tubers. In: Li PH, ed. Potato physiology. New York:
Academic Press Inc, 389±455.
Iiyama K, Lam TBT, Stone BA. 1994. Covalent cross-links in the cell
wall. Plant Physiology 104: 315±320.
Kolattukudy PE. 1984. Biochemistry and function of cutin and suberin.
Canadian Journal of Botany 62: 2918±2933.
Lachaud S, Catesson AM, Bonnemain JL. 1999. Structure and
functions of the vascular cambium. Comptes Rendus de l'Academie
des Sciences, Paris 322: 633±650.
Larson PR. 1994a. Anticlinal cambial divisions. In: Larson PR, ed. The
vascular cambium, development and structure. Berlin, Heidelberg:
Springer-Verlag, 155±318.
Larson PR. 1994b. Cambial zone characteristics. In: Larson PR, ed.
The vascular cambium, development and structure. Berlin, Heidelberg: Springer-Verlag, 587±637.
Lulai EC, Corsini DL. 1998. Di€erential deposition of suberin phenolic
and aliphatic domains and their roles in resistance to infection
during potato tuber (Solanum tuberosum L.) wound-healing.
Physiological and Molecular Plant Pathology 53: 209±222.
Lulai EC, Morgan WC. 1992. Histochemical probing of potato
periderm with neutral red: a sensitive cyto¯uorochrome for the
hydrophobic domain of suberin. Biotechnic and Histochemistry 67:
185±195.
Lulai EC, Orr PH. 1993. Determining the feasibility of measuring
genotypic di€erences in skin-set. American Potato Journal 70:
599±609.
Lulai EC, Orr PH. 1994. Techniques for detecting and measuring
developmental and maturational changes in tuber native periderm.
American Potato Journal 71: 489±505.
Lulai EC, Orr PH. 1995. Porometric measurements indicate wound
severity and tuber maturity a€ect the early stages of woundhealing. American Potato Journal 72: 225±241.
Lyshede OB. 1977. Studies on the periderm and epidermis of the
potato tuber Solanum tuberosum L. cv. Bintje. In: Yearbook of the
Royal Veterinary and Agricultural University. Copenhagen,
Denmark, 68±74.
Murphy HJ. 1968. Potato vine killing. American Potato Journal 45:
472±477.
Peterson RL, Barker WG, Howarth MJ. 1985. Development and
structure of tubers. In: Li PH, ed. Potato physiology. New York:
Academic Press Inc, 123±152.
Reeve RM, Hautala E, Weaver ML. 1969. Anatomy and compositional
variation with potatoes. I. Developmental histology of the tuber.
American Potato Journal 46: 361±373.
Roland JC. 1978. Early di€erences between radial walls and tangential
walls of actively growing cambial zone. IAWA Bulletin 1: 7±10.
Soliday CL, Kolattukudy PE, Davis RW. 1979. Chemical evidence that
waxes associated with the suberin polymer constitute the major
di€usion barrier to water vapor. Planta 146: 607±614.
Thomson N, Ray FE, Kelman A. 1995. Wound healing in whole potato
tubers: a cytochemical, ¯uorescence, and ultrastructural analysis
of cut and bruise wounds. Canadian Journal of Botany 73:
1436±1450.