Elm., Sci., Vol. 30, No.3, 1984, pp. 705-714
Copyriahl 1984. by \be Society of American Formen
Growth and Physiology ofLoblolly Pine Roots
Under Various Water'Table Level and
Phosphorus Treatments
D.
S. DEBELL
D. D.
HOOK
W. H. MCKEE, JR.
J. L. AsKEW
ABsTRACT.
Weight, morphology, phosphorus and starch content, and anaerobic and nitrogen
metabolism of root s of loblolly pines grown from seed for 2 years in drained (D), seasonally
flooded (SF) and continuously flooded (CF) soils, with and without phosphorus fertilizer (PI and
Po, respectively) were compared. Root development was best in SF and poorest in CF, and was
improved by PI in all water table treatments. Rates of anaerobic metabolism were greatest in root
tips from seedlings grown in CF, and root tips of CF-PI had higher rates of ethanol and malate
production than those of Cr-Po. Relative contents of glutamic acid, 'Y-aminobutyric acid, aspar­
agine, and alanine in xylem sap increased with flooding. Based on these findings and other existing
knowledge, we suggest that loblolly pine root s are capable of accelerated glycolysis under anaerobic
or waterlogged soil conditions and that some carbon breakdown processes are shunted from ethanol
production to synthesis of nontoxic products. Enhancement of the energy status of pine roots by
phosphorus may be a factor in the fertilizer responses commonly obtained on wet or poorly
drained soils of the southeastern United States coastal plains. FOREST Sci. 30:705-714.
AnomONAL
KEY
WORDS.
Pinus taeda. ftooding, anaerobiosis, metabolism, nutrition.
KNOWLEDGE of adaptive mechanisms which enable some higher plants to survive
and grow in waterlogged and anaerobic soil environments has increased greatly
during the past decade (Hook and Crawford 1978, Armstrong 1979, Davies 1980,
Drew and Lynch 1980). Specific adaptations and growth responses to periodic
inundation and hypoxia by species only moderately tolerant of waterlogged soil
conditions, however, remain poorly understood. Information about the nutrition
of these species under such conditions is especially limited, and may have im­
portant implications in the management of wet lowland forest areas.
Excess soil water limits growth of pine on many lowland -sites in the southeastern
coastal plain of the United States, and water level control by ditching and/or
The authors
are,
respectively, Principal Silviculturist, Pacific Northwest Forest and Range Exper­
iment Station, USDA Forest Service; Professor of Forestry, Oemson University; Principal Soil Sci·
entist, Southeastern Forest Experiment Station, USDA Forest Service; Biological Technician, Oemson
University. This work was conducted while the first author was Visiting Professor at the Belle W.
Baruch Forest Science Institute of Oemson University at Georgetown, South Carolina. It was funded
in part through a Cooperative Research Agreement with the Southeastern Forest Experiment Station.
Charleston, South Carolina. The authors gratefully acknowledge the work of Robert W. Rose and M.
Monica McGregor of the Forest Science Laboratory, Westvaco Corporation, Summerville, S.c., in
analyses of starch content; Foster B. Wardlaw, Food Science Department, Clemson University, Oem­
son, S. C., in amino acid analyses; and Martha R. McKevlin, Southeastern Forest Experiment Station,
Charleston, S. C., in phosphorus analyses. Manuscript received 6 May 1983.
VOLUME 30, NUMBER 3,
1984 / 705
bedding is commonly practiced. Application of phosphorus fertilizer to wet farest
soils has frequently resulted in good growth responses by loblolly pine (Pinus
taeda L.) and slash pine (P. elliott;; Engelm. var. elliottil) (Pritchett 1979). In
some instances, fertilizer has produced growth increases comparable to those
obtained with improved drainage (Pritchett and Smith 1974).
Solubility of native mineral soil phosphorus is substantially greater under fo
l od­
ed or highly reduced conditions than under drained, aerobic conditions (Ponnam­
peruma 1972, Gambrell and Patrick 1978). Moreover, factors other than phos­
phorus are more likely to be limiting to growth under poorly drained conditions.
Response to applied phosphorus, in such situations, therefore, might be expected
to be less than on well-drained sites. The opposite is often true, however: the
greatest growth responses of loblolly and slash pines to phosphorus fertilizers are
frequently obtained in the wetter environments and on the more poorly drained
soils (Pritchett and Smith 1972).
One reason for these somewhat paradoxical relationships is that poor root
aeration may reduce the ability of southern pines to absorb nutrients (Shoulders
and Ralston 1975) and therefore higher soil concentrations are needed to attain
the same tree nutrient status (Shoulders 1976). Responses to applied phosphorus
may also be effected through specific mechanisms which enable pine to cope more
effecti:vely with hypoxia and other problems associated with excess soil water.
Exploratory research on several aspects of the growth and physiology of loblolly
pine roots was therefore superimposed on portions of a study designed to test
effects of water table depth and phosphorus additions on biomass production and
nutrient accumulation by loblolly pine (McKee and others 1984). This paper
presents our findings and discusses their possible significance to survival and
growth of loblolly pine on wet sites.
METHODS
Experimental Layout.- The study was conducted on loblolly pines grown from
seed for 2 years under three water table treatments and two fertilizer treatments
in soil tanks (hydroedaphytron, cf. Hook and others 1970 for description) in
coastal South Carolina. The tanks were filled to a depth of about 1.5 m with a
sandy loam soil from the B2 horizon of the Goldsboro series (aquic Paleudult,
fine-loamy, siliceous, thermic); this material was covered with about 0. 3 m of
sandy clay soil from the AI horizon of the Bethera series (typic Paleaquult, clayey,
mixed, thermic). Both sedimentary soils were collected from a Pleistocene terrace
on the FI1lncis Marion National Forest in Berkeley County, South Carolina. Lob­
lolly pines had responded to phosphorus fertilizer on an adjacent similar site, thus
indicating the soils used were deficient in available phosphorus.
Treatments of the tanks, which were exposed to normal precipitation, consisted
of three water table regimes: (1) maintained 61 cm below the soil surface (hereafter
called drained), (2) maintained at the soil surface (continuously flooded), and (3)
a variable water table where water was maintained at the soil surface during the
dormant season (November I to March 31) and then lowered 15 cm every 2
weeks until a depth of 61 cm was reached; this level was maintained to the end
of October (seasonally flooded). Phosphorus fertilizer as a monocalcium phosphate
was applied to one-half of each tank, and mixed throughout the surface soil (0.3
m) at a level of 100 parts per million phosphorus (the fertilized or PI treatment).
An equal amount of calcium was applied as calcium sulfate to the other one-half
of each tank (hereafter referred to as the unfertilized or Po treatment) to ensure
that calcium was not a variable in the study.
706 / FOREST ScIENCE
In each tank, the two fertilizer treatments (PI and Po) were separated by a
plywood barrier. Two replications of each water table level-phosphorus treatment
were established, and each replicate consisted of 18 seedlings spaced 30 cm apart.
One replication was harvested in late fall 1980, and the other was harvested in
spring 198 1. Shoot weight per tree (average of both harvests) was affected by both
water table level and phosphorus applications as follows: drained- 1 10 g (Po),
1 14 g (PI); continuously flooded-5 g (Po), 26 g (PI); seasonally flooded- 153 g
(Po), I 72 g (P.).1
Harvesting Proced ures -Root systems were washed from the soil using garden
hoses equipped with spray nozzles. Lateral roots were so intertwined in all but
the continuously flooded treatment that removal of intact root systems was not
feasible. The terminal 10-cm sections of new roots (i.e., roots with actively growing
tips) were therefore cut off, wrapped in moist paper towels, and refrigerated at
2"C for 4 to 6 hours until used in studies of anaerobic metabolism. The tap and
most of the lateral roots of each seedling were extracted intact; remaining lateral
and fine roots were washed from the soil and kept separate by treatment.
.
Weight and Morphology of Roots.-Weights of root systems were obtained from
fresh material, with dry weights estimated from fresh weight: dry weight rela­
tionships determined on subsamples dried at 70°C. Taproot lengths were measured
to the point where diameter was less than 0.3 cm. The positions (distance from
root collar) of all primary lateral roots were recorded; these data were summarized
as number of laterals at 0-6 cm and at 6 + cm below the soil surface.
Phosphorus and Starch Concentrations in Roots. -Analyses were performed on
composite samples made up of roots from all trees in each treatment (i.e., one
sample per treatment). Samples of dried root material were ground to 40 mesh
in a Wiley mill. One portion was dry ashed at 450°C for 2 hours, taken up in 0. 3
N nitric acid, and analyzed for phosphorus by the molybdovanadate procedure
(Jackson 1958). Starch was determined on another portion by a method using
enzymatic hydrolysis (Haissig and Dickson 1979).
Anaerobic Metabolism of Root Tips.- The terminal 10 cm of new roots were
surface sterilized by dipping in 0.02-percent mercuric chloride and rinsed three
times with sterile distilled water. The terminal l -cm portions of these roots were
then excised, and 10 to 20 root tips from each treatment were placed in individual
Warburg flasks with I ml distilled water. flasks were then attached to a dife
f rential
respirometer and incubated in N2 atmosphere at 25°C as per Hook and Brown
( 1973). Carbon dioxide (C02) evolution was measured at one-half hour intervals
for 4 hours. After incubation, the root tips and bathing solution were analyzed
for ethanol (Hook and Brown 1973) and malate (Gutmann and Wahlefeld 1974).
Previous work indicated tQat amounts of ethanol and malate in the excised root
tips prior to incubation were negligible. Data on CO2, ethanol, and malate were
summarized as micromoles or nanomoles produced per mg root tissue per hour.
Nitrogenous Compounds in Xylem Sap.-Xylem sap was extracted from freshly
cut stems by the vacuum flask method (Bollard 1953) and composited by treat­
ment. The composite samples were filtered and frozen at - 15°C until analyzed.
The sap was evaporated to dryness in a flash evaporator, the residue was dissolved
in 0.9 ml distilled water, and 0. 1 ml of 36-percent sulfosalicylic acid was added
I The study reported herein was conducted on roots of seedlings harvested in spring 1981 (seedlings
harvested in fall were used to develop and refine the analytical procedures).
VOLUME 30, NUMBER 3, 1984 / 707
to precipitate proteins and peptides. After centrifuging at 12,000 rpm, free amino
acids and amides in the supernatant were detennined on an amino acid/peptide
analyzer for all but one treatment. Sap extracted from the small trees of the
nonfertilized, continuously flooded treatment was of insufficient quantity for such
analyses.
RESUL TS AND DISCUSSION .
Weight and Morphology of Roots.- Ovendry weights of roots were affected by
both water table level and phosphorus fertilization (Table I). Weights were highest
in the seasonally flooded treatment and those of the drained treatment were
somewhat lower. Root weights were drastically reduced under continuously flood­
ed conditions, averaging only about 15 percent of those in the seasonally flooded
treatment. Such differences are in concert with those detennined for shoot pro­
duction in various water table level treatments. The effect of applied phosphorus
varied with water table level. Root weights in the drained treatment were increased
100 percent by phosphorus application; in .the seasonally flooded treatment, root
weight of fertilized trees was 60 percent greater than that of unfertilized trees.
Much greater relative differences occurred under continuously flooded conditions;
root systems in soil receiving added phosphorus were nearly three and one-half
times larger than those in unfertilized soil. Substantial increases in root biomass
of slash pine due to phosphorus fertilization were also reported in a controlled
water level study by White and others ( 197 1).
Length of taproots and number of lateral roots also varied with water table
level and phosphorus fertilization (Table 1). Taproot lengths for pines grown in
drained and seasonally flooded treatments without phosphorus were similar (27
cm) and were increased 22 to 30 percent by phosphorus applications. Taproots
of the continuously flooded trees were much shorter, only 5 cm without added
phosphorus, but were tripled in length with phosphorus. Numbers of lateral roots
in the 0 to 6-cm soil horizon tended to increase with flooding; at soil depths
greater than 6 cm, however, lateral root fonnation was strongly inhibited in the
continuously flooded treatment. Application of phosphorus fertilizer increased
the average number of lateral roots for all drainage treatments by 23 percent.
Continuously flooded pines treated with phosphorus had 54 percent more lateral
roots in total, and nearly three times as many roots below 6 cm than their coun­
terparts without fertilizer.
Mycorrhizae were observed on roots of seedlings in all treatments.
Phosphorus and Starch Concentrations in Roots. - Concentration of phosphorus
appeared higher in the continuously flooded treatment than in the other water
treatments (Table 1). Moreover, phosphorus concentrations were markedly in­
creased (7 1 to 125 percent) by phosphorus fertilization in all water level treat­
ments. Starch concentrations may provide a general index of shoot and root system
vigor. Highest starch levels occurred in the vigorous roots of the seasonally flooded
treatment whereas the lowest concentrations were found in the continuously flood­
ed treatment. Phosphorus fertilization enhanced starch levels slightly in the drained
(8 percent) and seasonally flooded ( 13 percent) treatments, but the increase in
starch content was pronounced (72 percent) in the continuously flooded treatment.
As a result, root starch concentration in the continuously flooded; phosphorus
treatment was similar to concentrations in the fertilized and unfertilized drained
treatment.
Anaerobic Metabolism of Root Tips. -Carbon dioxide production of root tips
from drained and seasonally flooded root systems appeared similar (Table 2).
Rates of CO2 production of tips from the continuously flooded treatment, how­
708 / FOREST SCIENCE
TABLE 1. Root characteristics of loblolly pine seedlings grown under different
water table level and phosphorus treatments.·
Lateral roots
Treatment2
Taproot
length
Root dry
weight
0-6cm
depth
Phosphorus
concentration)
>6cm
depth
number
.. ..._. ..
Starch
concentration)
. . .. . .. ... . percent ..................
g
cm
Po
27±10
27±2
8± I
7± I
0.05
11.9
PI
54±8
33± 2
8 ±1
9± I
.09
12.8
30
8
8
.07
12.4
Drained
40
Average
_______._
.__.
.
.
. _...
.
. .
_
. ..
Seasonal flooding
Po
PI
47±8
27± 2
10± I
10± I
.04
14.8
75± 15
35±3
10± I
12± I
.09
16.8
61
31
10
11
.06
15.8
4±2
5± I
10± I
3± I
.07
7.5
14±3
16± I
12± 1
8 ±1
.12
12.9
10
11
6
.10
10.2
Average
Continuous flooding
Po
PI
9
Average
I Mean values are accompanied by standard error based on 12 to 18 subsamples.
2P
phosphorus fertilizer mixed throughout surface soil at level of
o no phosphorus added; PI
100 ppm.
=
=
) Concentrations
are
based on tissue dry weights.
ever, averaged three to four times higher than those of tips from the drained and
seasonally flooded treatments. There w re no apparent effects of prior applications
of phosphorus on CO2 evolution.
Amounts of ethanol produced by root tips increased with degree of prior flooding
(Table 2). In addition, ethanol production appeared to be related to prior phos­
phorus treatments. Root tips of the drained, phosphorus treatment produced 75
percent more ethanol than those of the unfertilized, drained treatment, and the
TABLE 2. Some products of anaerobic metabolism by loblolly pine root tips
excised from seedlings grown under different flooding and phosphorus treatments.·
Carbon dioxide (C02)
Treatment
Drained
.._._. __
_.___
Ethanol
,,-mole mg--Ih-I
____._ ...._._ .._.
Malate
nanomoles mg--I h-I
Po
0.05±om
0.24±0.05
6.0 ±0.5 PI .06±.02
.42±.10
6.3±1.0
Average
.06
.33
6.2
Seasonal flooding
Po
.09±.03
1.03±.31
9.5±2.2 PI
.06±.02
.40± .08
15.7±9.7 Average
.08
.72
12.6 Continuous flooding
Po
PI
Average
I
.20
.26±.06
.23
.53±.39
28.3±22.1 1.70±.23
119.6±72.9 1.12
74.0 Mean production is accompanied by the standard error based on four subsamples; CO2 data
available for only one subsample of the unfertilized (Po), continuously flooded treatment and malate
data for only two subsamples of the fertilized (PI), continuously flooded treatment.
VOLUME 30, NUMBER 3, 1984 / 709
A
ADP
(j'I
V
NADH 2
ATP
A
Phoaphoonol_ V
y
NA
Glucose --..x _Fructose -6...p PlFruct08e-1,6-P--X -lI.-X-x-pyruvate - Pyruvate
ADP\.
ATP
CO 2 2
LEO]
. Atp
CO
\ -L2.I
A
NADH2
UlQIIIIID
Blocks:
Indicate metabolites Influenced by treatments in our
study.
Clrel•• :
Indicate points where explanation for pathway is
available as follows·
1. Rate·llmltlng step In glycolysis; stimulated by high ratio of Inorganic P and ADP to ATP(Davies 1980).
2. CO, acts as both metabolite and physiological activator (Zemlianukhln and Ivanov 1978). 3. CO, activates reaction sequence from pyruvate to form 1·amlnobutyrate and alanine vlao·ketoglutarate and glutamate (Zemlianukhln and Ivanov 1978). •. Glulamlne synthesis Is Inhibited by high lev ls of alanine (Lehninger 1975) and probably by low energy levels. FIGURE 1.
Oxaloacetate
Aspartate
ATP
DP
N D
l
2
Acetaldehyde
2
(Ethanoll
Postulated pathways for metabolites influenced by flooding or phosphorus.
phosphorus-related stimulation of ethanol in tips of the continuously flooded
treatment was 221 percent or about three times greater than the unfertilized
treatment. Response to applied phosphorus in the seasonally flooded treatment,
however, was reversed; more ethanol was produced in roots from the nonfertilized
treatment.
The relative effect of prior flooding on production of malate in excised root tips
was, in general, more pronounced than effects of flooding on carbon dioxide and
ethanol production (Table 2). Prior application of phosphorus had no effect on
malate production in root tips from the drained treatment, and variation was too
great in the seasonally flooded treatment to attribute average differences to phos­
phorus. There was, however, an apparent stimulation of malate synthesis in root
tips from the continuously flooded seedlings by applied phosphorus.
The higher levels of CO2, ethanol, and malate production by excised root tips
from the continuously flooded treatments suggest an inductive mechanism. Al­
though prior flooding is unlikely to have resulted in complete anaerobiosis as did
the incubation conditions, it may have induced synthesis of enzymes related to
these products. The inductive nature of alcohol and malic dehydrogenases in plant
roots has been established (Crawford and McManmon 1968). In a similar exper­
iment with swamp tupelo, Hook and others ( 197 1) showed that CO2 and ethanol
production were nearly five times greater in roots from flooded soils than from
aerated soils.
Effects of phosphorus nutrition on anaerobic or hypoxic metabolism of tree
roots has not, to our knowledge, been studied. Acceleration of anaerobic break­
down of glucose (glycolysis) in root tips with higher phosphorus content is con­
sistent, however, with current knowledge of carbohydrate metabolism (Vartape­
tian 1978). The phosphorylation reaction between fructose-6-phosphate and ATP
to give fructose 1-6-diphosphate is a non equilibrium reaction (Fig. 1) and is
believed to be the rate-limiting step in glycolysis (Davies 1980). Phosphofruc­
tokinase catalyzes the reaction, and studies of both plant and animal tissues
indicate that this enzyme is stimulated by inorganic phosphorus (Turner and
Turner 1975). Such relationships, however, do not explain our results regarding
effects (or lack thereof) of phosphorus fertilizer on CO2 and ethanol production
of excised root tips from seasonally flooded root systems.
7 10 I FOREST ScIENCE
TABLE 3. Free amino acids and amides in xylem sap o/loblolly pine seedlings
grown under different water table level and phosphorus treatments.
Free amino acids and amides (AAS)I
Treatment
GLU-NH2
GLU
GABA
Drained
_. ____.___.____. ____
ASP-NH2
ASP
ALA
Total
concen­
tration
mgMs per
Percent of total freeMs
_____.___...__._.. _..__
100 ml sap
Po
PI
71
7
3
7
2
Tr.
57
14
3
7
3
Tr.
8.8
Average
64
10
3
7
2
Tr.
10.4
Po
32
18
7
13
3
3.5
PI
29
17
7
16
2
2.9
Average
30
18
7
14
2
J
3.2
17
10
12
2
2
7.2
12.0
Seasonal flooding
Continuous flooding
PI
I GLU-NH2
45
=
2
glutamine, GLU
=
glutamic acid, GABA
=
'Y-aminobutyric acid, ASP
=
aspartic
acid, ASP-NH2
asparagine, ALA
alanine.
2
Xylem sap extracted from Po stems in continuously flooded treatment was insufficient for amino
=
=
acid analysis.
In anaerobic incubation studies with swamp tupelo roots, Hook and others
( 197 1) found that ethanol and CO2 were produced in nearly equimolar quantities;
thus, the substantially greater ratio found in our study was unanticipated. Synthesis
of malate (Fig. 1) will fix some CO2 (via carboxylation of phosphoenolpyruvate
to form oxaloacetate and the reduction of the latter to malate) and thus may
account for a minor portion of this disparity. Similar increases in malate pro­
duction have been observed in other species under flooded or waterlogged soil
conditions (Crawford 1978, Keeley 1979, Mendelssohn and others 1981).
Although malate production in anaerobically incubated, excised root tips was
little affected by added phosphorus in the drained and seasonally flooded treat­
ment, it appeared to be stimulated by phosphorus in root tips of the continuously
flooded treatment. This difference may be related to the much higher rates of
glycolysis (as evidenced by ethanol production) in the root tips of the fertilized,
continuously flooded treatment, and consequent effects of elevated CO2 concen­
trations.
Nitrogenous Compounds in Xylem Sap. 'total concentrations of free amino acids
and amides were lower in xylem sap of seedlings grown in seasonally and con­
tinuously flooded treatments than in sap of seedlings in the drained treatment
(Table 3). Because concentration at any time is affected by rates of absorption
and transpiration of water, data on relative composition of amino acid and amide
contents probably provide a more informative indication of differences or alter­
ations in nitrogen metabolism of root systems among the various water table level
and phosphorus treatments. The amino acids and amides listed in Table 3 account
for 72 to 90 percent of total free amino acid and amide contents; they also are
the nitrogenous compounds that appeared to be most affected by treatment.
Glutamine was the principal nitrogenous compound in all treatments, but its
relative quantity decreased from an average of 64 percent in the drained treatment
to 30 and 4S percent, respectively, in the seasonally and continuously flooded
treatments. Correspondingly, relative amounts of glutamic acid and asparagine
-
VOLUME 30, NUMBER 3, 1984 / 7 1 1
were about 80 percent higher in the two flooded treatments. Compared with the
drained treatment, the percentage of -y-aminobutyric acid was more than twice
as great in the seasonally flooded treatment and more than three times as great
in the continuously flooded treatment. Aspartic acid did not appear to be affected
by treatment. Alanine was present in only trace amounts in sap of the drained
treatment, but comprised 1 to 2 percent of total free amino acid and amide content
in the two flooded treatments.
The coupling of altered pathways of carbohydrate and amino acid metabolism
is believed to occur as an adaptive mechanism in facultative anaerobic and aerobic
organisms (Zemlianukhin and Ivanov 1978). Because our information on changes
in amino acid composition was obtained from xylem sap collected from the
harvested seedlings, it cannot be compared directly with CO2, ethanol, and malate
data from anaerobic incubation of excised root tips. Our findings, however, do
indicate effects of flooding on nitrogen metabolism within the loblolly pine sys­
tems; i.e., proportions of glutamine are reduced and relative amounts of -y-ami­
nobutyric acid, alanine, glutamic acid, and asparagine are substantially increased.
Glutamine may account for more than 70 percent of the total nitrogen trans­
located in xylem sap of pine species (Barnes 1963). Decreased glutamine synthesis
and increased alanine under hypoxic conditions have been reported in studies
with other species and tissues (Kohl and others 1978), and are believed to be
associated with a low energy charge (hence, low amination of glutamic acid to
glutamine) and high pyruvate levels (a precursor of alanine). Glutamine synthetase
is inhibited by high levels of alanine (Lehninger 1975). Similarly, accumulation
of-y-aminobutyric acid under hypoxic or high CO2 environments is characteristic
of many organisms and appears to be of general biological significance. Zemli­
anukhin and Ivanov ( 1978) suggest that a-ketoglutaric acid is synthesized from
pyruvate via a roundabout reaction chain which is activated by high CO2 (Fig.
1); a-ketoglutaric acid is aminated to form glutamic acid which in tum is converted
to -y-aminobutyric acid. Increased -y-aminobutyric acid and glutamic acid levels
have also been reported in roots of willow (Salix spp.) under anaerobiosis (Du­
binina 196 1). The increased glutamic acid probably results in part from the re­
duction in glutamine synthesis as mentioned above. Reasons for the increase in
asparagine content are less clear; although oxaloacetate formed via carboxylation
of phosphoenolpyruvate would serve as a substrate for aspartate synthesis, energy
(adenosine triphosphate) would be required for amination of aspartate to form
asparagine. Our findings, however, correspond to those of Kohl and others
( 1978) for meristematic root tissue of maize incubated anaerobically with a
NH4 +-nitrogen source.
Phosphorus application had no apparent influence on amino acid composition
of xylem sap, except in the drained treatment where relative amounts of glutamine
and glutamic acid were lower and higher, respectively, in sap of fertilized seedlings.
Earlier work by Carter and Larsen ( 1965) with N, P, and K fertilizers on loblolly
pine supports these observations. The possibilities remain that applied phosphorus
did influence amino acid composition of sap in the continuously flooded treat­
ment, and that it may influence amino acid composition of xylem sap in seasons
other than spring.
OVERVIEW AND IMPLICATIONS
The largest root systems were developed in the seasonally flooded treatment.
Seasonal flooding represents, to some degree, both a "drainage" and flooding
treatment with attendant positive and negative implications for tree growth pro­
cesses. The unexplained differences between seasonally flooded and continuously
flooded trees with regard to effects of phosphorus on some aspects of root phys­
7 12 / FOREST SCIENCE
iology may be due, at least in part, to such "drainage" effects. Additional phys­
iological research is needed to fully understand the effects of phosphorus fertilizers
on sites with variable water tables.
Roots of continuously flooded seedlings were by far the smallest and obviously
were growing under much stress. Because the conditions of this treatment were
severe and uniform during the entire experimental period, data from these seed­
lings probably provide the most informative clues as to potential effects of phos­
phorus fertilizer on root physiology in wet and poorly drained soils. Our results
indicate that phosphorus applications greatly improve the ability of loblolly pine
roots to grow under anaerobic or hypoxic conditions. It appears that loblolly pine
roots have the capacity to accelerate rates of glycolysis in waterlogged soils. The
addition of phosphorus in such situations may result in even greater increases in
glycolytic rates, as evidenced by increased ethanol and malate production in
excised root tips from the continuously flooded treatment. Furthermore, accel­
erated anaerobic respiration in loblolly pine apparently leads to altered metabolic
pathways (Fig. 1) such that some carbon breakdown processes are shunted from
production of ethanol to production of malate and certain amino acids (e.g.,
glutamic acid, 'Y-aminobutyric acid, asparagine, and alanine). These products are
nontoxic, and reactions involved in their syntheses provide a means of regener­
ating reduced nicotinamide nucleotides. Translocation of these reduced com­
pounds to the shoots (where they can be oxidized in an aerobic environment)
may serve as a mechanism for transferring the oxygen debt from roots to tops
(Crawford 1978).
The improved energy status of phosphorus-fertilized roots no doubt has some
direct and immediate benefits for survival and growth of roots in such adverse
soil conditions. Presumably, such improvement also leads to more favorable
nutrient balances (Hook and others 1983) and increased synthesis of growth
substances which are translocated to shoots. Consequent enhancement of top
growth and photosynthate production should ultimately be reflected in better
development of both roots and shoots of loblolly pines planted in waterlogged
soils.
LITERATURE OTED
ARMSTRONG, W.
1979.
Aeration in higher plants. In Advances in botanical research (H. W. W.
Woolhouse, ed), p 225-332. Vol 7. Academic Press, London. 697 p.
BARNES, R. L. 1963. Organic nitrogen compounds in tree xylem sap. Forest Sci 9:98-102.
BollARD, E. G. 1953. The use of tracheaJ sap in the study of apple tree nutrition. J Exp Bot 4:363368.
CARTER, M. C., and H. S. LARsEN. 1965. Soil nutrients and loblolly pine sap composition. Forest
Sci 11:216-220.
CRAWFORD, R. M. M. 1978. Metabolic adaptations to anoxia. In Plant life in anaerobic environments
(D. D. Hook and R. M. M. Crawford, eds), p 119-136. Ann Arbor Sci Publ, Inc, Ann Arbor,
Mich. 564 p.
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