Plant Physiol. (1984) 74, 1055-1058
0032-0889/84/74/1055/04/$01.00/0
Short Communication
Role of Seagrass Photosynthesis in Root Aerobic Processes'
Received for publication December 7, 1983 and in revised form January 6, 1984
ROBERT D. SMITH, WILLIAM C. DENNISON, AND RANDALL S. ALBERTE*
Barnes Laboratory, Department of Biology, The University of Chicago, Chicago, Illinois 60637
ABSTRACT
The role of shoot photosynthesis as a means of supporting aerobic
respiration in the roots of the seagrass Zostera marina was examined.
O2 was transported rapidly (10-15 minutes) from the shoots to the rootrhizome tissues upon shoot illumination. The highest rates of transport
were in shoots possessing the greatest biomass and leaf area. The rates
of 02 transport do not support a simple gas phase diffusion mechanism.
02 transport to the root-rhizome system supported aerobic root respiration and in many cases exceeded respiratory requirements leading to 02
release from the subterranean tissue. Release of 02 can support aerobic
processes in reducing sediments typical of Z. marina habitats. Since the
root-rhizome respiration is supported primarily under shoot photosynthetic conditions, then the daily period of photosynthesis determines the
diurnal period of root aerobiosis.
The inundation of soils or sediment with water can lead to 02
deficiency due to the low solubility of 02 in water and its low
rate of diffusion in the aqueous phase compared to that in the
gas phase (12). Under such conditions, whether caused by episodic, periodic, prolonged, or indefinite floodings as in natural
wetland conditions, lake bottoms, or coastal marine areas, soil
anoxia can develop and persist (2, 3). As a consequence, the
portions of vascular plants growing in such soils can become
anaerobic resulting in fermentative metabolism in these tissues
(1, 5). The predominance of glycolysis over mitochondrial activities of the Krebs cycle and electron transport can lead to
dramatic reductions in ATP levels, reduced protein synthesis
and plant growth, inhibition ofion uptake, and the accumulation
of toxic metabolic end products (1-3, 5, 12). If such conditions
persist, tissue death usually occurs; a response characteristic of
flood-intolerant species (2, 3).
Many species, however, have evolved physiological or morphological means by which tissue anoxia is avoided or minimized. These species, termed flood-tolerant species (2, 3), often
possess aerial roots (3), have extensive aerenchymous tissue (8,
12, 16, 20), show pressurized ventilation (4), have 02 transport
from aerated tissue to anoxic tissues (10, 1 1, 15, 16, 19), or have
metabolic means to minimize the harmful consequences of
anoxia (1-3, 5). In the latter situation, carbon skeletons from
glycolysis are most often shunted away from ethanol to less toxic
compounds, such as organic or amino acids, which may be
oxidized subsequently for energy or used for other metabolic
activities (see Refs. 1, 5).
Though there have been numerous investigations of flood
tolerance in terrestrial species (2, 3), there have been few studies
examining this phenomena in submerged angiosperms which
grow in anoxic and/or reducing sediments. In the present study,
we sought to examine the flood tolerance of the submerged
marine angiosperm Zostera marina (eelgrass). This temperate
seagrass inhabits coastal areas of the Northern Hemisphere which
are characterized, for the most part, by the presence of reducing
sediments (9) and light limitation for growth (7). Despite this
apparently inhospitable environment, Z. marina is one of the
most productive marine primary producers known (14). Previous
investigations have shown that seagrass plants can release 02 into
the sediments under photosynthetic conditions (14, 15) and in
doing so support the activity of oxygenic nitrifying bacteria (10,
16). Therefore, we examined the extent of photosynthesis-dependent 02 transport from shoots to roots-rhizomes and considered the importance of growth light environment and shoot
biomass on these processes.
MATERIALS AND METHODS
Plant Materials. Zostera marina plants were collected at 1 to
2 m depth at Great Harbor, Woods Hole, MA (40° 31.5'; 70°
40.5'). Cores, 10 to 12 cm in depth and 20 cm diameter,
containing 8 to 15 shoots were extracted from the sediment with
plexiglass corers. The cores were transferred promptly to the
laboratory and placed in running seawater aquaria.
Root, rhizome, and shoot (aerial stem and leaves) biomass
were determined from dry weight measurements of tissues
washed thoroughly in distilled H20 prior to drying. Leaf areas
per shoot were determined from conversion factors of dry weight
to leaf area derived from Dennison and Alberte (7) on plants
collected at the same time.
0° Exchange Measurements. The 02 exchange from the rootrhizome systems of intact Z. marina plants was measured polarographically in a two-chambered apparatus (Fig. 1) fitted to a
Clark-type 02 electrode (Rank Bros, England) following the
procedures of Delieu and Walker (6). This apparatus allowed for
the separation of the root-rhizome system (lower chamber) from
the shoot (upper chamber), and prevented shoot to root gas
exchange except through living tissue. A syringe needle was
inserted through the chamber separation stopper to maintain a
continuous pressure gradient between both chambers. The temperature of both the shoot and root chambers were maintained
at ambient seawater levels (20 ± 1C). Mixing in the electrode
chamber was rapid and uniform as determined from dye studies.
Intact shoots were carefully removed from the cores prior to
experimentation and the root-rhizome system washed thoroughly with seawater. The older portions of the rhizome were
excised and the cut ends sealed with silicone grease. Seedlings
were also used in which rhizomes and roots were kept fully
' Robert Smith and William Dennison were supported by a National
Institute of Health Training Grant (GM 07183). A portion ofthis research
was conducted as a part of the Marine Ecology Course, Marine Biological
Laboratory, Woods Hole, MA. Research support from National Science
Foundation Grant OCE 8214914 is acknowledged.
1055- Published by www.plantphysiol.org
Downloaded from on June 15, 2017
Copyright © 1984 American Society of Plant Biologists. All rights reserved.
1056
SMITH ETAL.
Plant Physiol. Vol. 74, 1984
GAS
INLET
8X
O60
:40
2 -Dark----Light--WATER
7 BATH
3
4
5
1-Dark6
7
8
HOURS
ROOT
CHAMBER
5cm
FIG. 1. Two chambered apparatus for measurement of 02 evolution
and uptake in the root-rhizome system of Zostera marina L. (eelgrass).
A, Shoot chamber; B, 25-gauge syringe needle maintains pressure gradient with minimal 02 exchange between chambers; C, magnetic stirring
bar allows rapid and uniform mixing throughout the electrode chamber,
D, water bath (20°C); E, silicone grease; F, electrode; G, lead to recorder.
intact. The root-rhizome system was placed in the electrode
chamber containing ultrafiltered (0.22 Am) seawater (33 %0
salinity) under reduced 02 tension (10-15% of air saturation).
The electrode chamber was kept in total darkness during measurement, while the shoot chamber was illuminated with photosynthetically saturating light (150 ME m 2 s-' PAR; see Ref. 7)
or kept in darkness. The 02 exchange rates (uptake and release)
were recorded continuously for up to 8 h during shoot illumination and darkness. The 02 transport rates were calculated by
subtracting root-rhizome respiration from 02 release rates (10).
RESULTS AND DISCUSSION
When Z. marina plants were maintained in total darkness,
root-rhizome 02 uptake from the electrode chamber seawater
occurs (21 ± 7.1 nmol 2 h-' mg-' dry weight of root-rhizome)
(Fig. 2). Upon illumination of only the shoots, photosynthetically
produced 02 was transported rapidly from shoots to the rootrhizome system as seen in a typical trace of the 02 exchange
rates of the root-rhizome system in Figure 2. The use of the term
transport does not imply an active process, but merely a directional movement of 02 (see further discussion below).
In every case (n = 9), the highest rates of 02 uptake from the
electrode chamber seawater were observed when the shoots were
kept in darkness. Upon illumination of the shoots with photosynthetically saturating light however, 02 uptake by the rootrhizome system begins to decrease within 15 to 30 min and, in
many cases, results in the release of 02 from the roots (positive
slope, Fig. 2) presumably from 02 availability in excess of respiratory demand. The reduced root-rhizome demand for external
02 (electrode chamber seawater) reflects the increasing availability of an internal source of
02
resulting from transport of 02
FIG. 2. The effects of illumination of Zostera shoots on 02 exchange
rate in the root-rhizome tissue. Plants were maintained in either total
darkness or the shoots were illuminated with photosynthetically saturating light (150 ,E m-2 s-'). The 02 exchange was monitored continuously
between the root tissue and the 02 electrode solution. A negative slope
indicates 02 uptake by the root-rhizome system (respiration during dark
periods) while a positive slope indicates 02 release. The time period
between a change in illumination state and a significant change in slope
is indicated as the lag period.
from net shoot photosynthesis. The 02 exchange rates during
shoot illumination ranged from -6.2 (uptake) to +7.4 (release)
nmol 2 h-' mg-' dry weight of root-rhizome or -1.92 to +0.46
nmol 02 h-' mg-' dry weight (shoot).
The transport of 02 from shoot to roots can be demonstrated
simply by separating the base of the meristem from the rhizome,
which results in an increased 02 uptake from the rhizosphere
(electrode chamber seawater) (data not shown). Previous studies
have demonstrated that Z. marina possesses a system of air-filled
lacunae (16, 20) which are continuous from shoots through the
meristematic region to the root tips ( 16; see also Ref. 1 1; Smith,
unpublished). These channels provide a system for gas phase
movement of 02.
The precise mechanism of 02 transport in Z. marina is unknown. However, based on the rates of transport, the diameters
of typical lacunae and the distances over which transport must
occur (approximately 20 cm), rates of gas phase diffusion are
simply too slow (approximately 105 times slower than the transport rates measured here assuming that 50% of the root-shoot
volume is lacunal volume and the distance for transport is 20
cm) to account for the observed transport rates. Therefore, it
seems unlikely that only a gas phase diffusion mechanism functions in the movement of 02 from shoots to roots in eelgrass.
The amount of 02 transported and the potential for 02 release
to the sediment is determined in part by the total amount of
active photosynthetic tissue in Z. marina. Plants with greater
shoot biomass transport proportionately more 02 to the rootrhizome system than plants with low shoot biomass (Fig. 3).
Since Z. marina leaf biomass is directly proportional to leaf area
(7), a minimum leaf area (based on the 02 exchange data) of
about 4 x 10-3 m2/shoot is required for 02 release. A typical
mature eelgrass shoot has a leaf area of about 5 x 10-3 m2 when
the canopy is at its seasonal maximum (7).
Larger, fully developed shoots with greater biomass (Fig. 4)
and leaf areas are capable of transporting 02 in excess of respiratory demand to their roots which can be released into the
sediments or support oxygenic activities in older portions of the
Downloaded from on June 15, 2017 - Published by www.plantphysiol.org
Copyright © 1984 American Society of Plant Biologists. All rights reserved.
SEAGRASS OXYGEN TRANSPORT
S
0
0.2k
x
0
.o 0.1-
1057
illumination with lag times of only 15 to 30 min. In a similar
manner, the cessation of 02 transport brought about by darkening the shoot chamber leads to an equally rapid cessation in 02
transport from the shoot to the roots (see Fig. 2). Such rapid
responses to illumination would ensure a maximum daily period
of 02 transport to underground tissues, thereby maximizing the
daily period of root aerobic respiration. Furthermore, it would
also ensure maximum oxygenation of the typically highly reducing sediments and consequently support the metabolic activities
of the many facultative aerobic bacteria present in the sediments
(see Ref. 17).
Since most Z. marina communities are distributed along a
depth gradient, the portions ofthe population at depth are subject
Ito greatly reduced light intensities due to the attenuation of light
by the water column. Accompanying the reduced light intensities
400
lo& are reductions in the daily period of saturating photosynthesis
200
600
800
(7), termed Hat2. Plants growing at depth can experience H.t
SHOOT DRY WT (mg)
periods 3 h shorter than plants growing in shallow water (7).
FIG. 3. Relationship between 02 transport rates and shoot dry weight Since aerobic respiration in the underground tissues is supported
in Zostera marina (r = 0.78). Each data point represents 02 transport primarily during shoot photosynthetic periods, then H,1.t period
rate of individual plants for which dry weights were determined at the will determine the daily period of aerobic respiration in the rootend of the experiment.
rhizome. Consequently, the roots of plants growing at depth in
reducing sediment must endure longer periods of anoxia or
hypoxia. Prolonged root-rhizome anoxia or hypoxia due to short
0.2
H,,t regimes should reduce growth and biomass production.
Preliminary results (W. C. Dennison, unpublished data) show
that plants subjected to in situ shortened H,11 regimes (<5 h) have
I
about a 4% reduction in root and shoot production compared
0.1
with control plants (H,t,= 8 h).
The results of this study have important implications with
respect to the adaptive physiology and distribution of Z. marina.
Since this species inhabits coastal marine waters along a signifi(.C
0/ release
0
cant
depth gradient of a few meters to 30 m or more, then plants
a
O2uptake
growing at depth experience lower light intensities, shorter periods of photosynthetic saturation (H.,,) (7), and consequently,
0.=0.86
longer periods of 02 limitation for root-rhizome growth and
x
metabolism. Therefore, it appears that the period of root anoxia,
which is directly related to the daily period of saturating photo-0.
synthesis (H,.), could dramatically influence the depth distribution of this ecologically important species.
r-0.78
0
z
-
-
-
-
z
D)
200
400
600
8100
SHOOT DRY WT (mg)
FIG. 4. The relationship between Zostera root-rhizome 02 exchange
= 0.86). The 02 exchange rates were
recorded as described in Figure 1.
rates and shoot dry weight (r
rhizome. It is also likely that this excess 02 is utilized by roots of
small developing shoots branching off the main rhizome which
probably do not carry out net photosynthesis as light levels are
well below photosynthetic saturation (approximately 20-30 4E
m s-') at the bottom of dense eelgrass canopies (7, 13).
Lacunal diameter may also influence the 02 transport in Z.
marina plants. Increased root lacunal size in response to lower
sediment redox potential has been observed (16). Reduced lacunal diameter may mechanically restrict exchange of gases
within the root-rhizome system. We have observed that the
lacunal system in shoots, basal meristems, and root-rhizome
tissues are well developed in older plants from strongly reducing
sediments which have high 02 transport rates (R. D. Smith,
unpublished observations). However, young plants and seedlings,
characterized by low shoot dry weights and leaf areas and poorly
developed lacunae, have reduced 02 transport and generally do
not release 02 during shoot illumination (Fig. 4). These findings
suggest that a combination of low leaf biomass and area, and
small and few lacunae can account for reduced 02 transport in
eelgrass.
02 transport to the root-rhizome system is rapid upon shoot
2
Acknowledgments-We would like to thank Drs. J. Dacey and R. Aller for
helpful discussions and Dr. I. Valiela for laboratory space.
LITERATURE CITED
1. APREEs T, AM SMITH 1979 Pathways of carbohydrate fermentation in the
roots of marsh plants. Planta 146: 327-334
2. ARMSTRONG W 1978 Root aeration in the wetland conditions. In DD Hook,
RRM Crawford, eds, Plant Life in Anaerobic Environments. Ann Arbor
Science Publishers Inc, Ann Arbor, MI, pp 269-297
3. CRAWFORD RMM 1978 Metabolic adaptations to anoxia. In DD Hook, RMM
Crawford, eds, Plant Life in Anaerobic Environments. Ann Arbor Science
Publishers Inc, Ann Arbor, MI, pp 119-136
4. DACEY JWH 1981 Pressurized ventilation in the yellow waterlily. Ecology 62:
1137-1147
5. DAVIEs DD 1980 Anaerobic metabolism and the production of organic acids.
In PK Stumpf, EE Conn, eds, The Biochemistry of Plants. Academic Press,
London, pp 581 -607
6. DELIEU T, DA WALKER 1972 An improved cathode for the measurement of
photosynthetic oxygen evolution by isolated chloroplasts. New Phytol 71:
201-225
7. DENNISON WC, RS ALBERTE 1982 Photosynthetic responses of Zostera marina
L. (eelgrass) to in situ manipulations of light intensity. Oecologia 55: 137144
8. DREW EA 1979 Physiological aspects of primary production in seagrasses.
Aquat Bot 7: 139-150
9. FENCHEL T 1977 Aspects of the decomposition of seagrasses. In CP McRoy, C
Helfferich, eds, Serass Ecosystems: A Scientific Perspective. Dekker, New
York, pp 123-146
10. IIZUMI H, A HArroRI, CP McRoy 1980 Nitrate and nitrite in the interstitial
2Abbreviation: H.,, daily period of light saturated photosynthesis.
Downloaded from on June 15, 2017 - Published by www.plantphysiol.org
Copyright © 1984 American Society of Plant Biologists. All rights reserved.
1058
SMITH ETAL.
of eelgrass beds in relation to the rhizosphere. J Exp Mar Biol Ecol
41: 191-201
1 1. JUSTIN,SHFW, W ARMSTRONG 1983 Oxygen transport in the salt marsh genus
Puccinellia with particular reference to the diffusive resistance of the rootshoot junction and the use of parffin oil as a diffusive barrier in plant
studies. J Exp Bot 34: 980-986
12. KRAMER PJ 1983 Water Relations of Plants. Academic Press, New York
13. MAZZELLA L, D MAUZERALL, RS ALBERTE 1980 Photosynthetic light adaptawaters
tion features of Zostera marina L. (eelgrs). Biol Bull 159: 500
14. McRoY CP, C McMILLAN 1977 Production ecology and physiology of seagrsses. In CP McRoy, C Helifferich, eds, Seagras Ecosystems: A Scientific
Perspective. M Dekker Inc, New York, pp 53-87
15. OREMLAND RS, BF TAYLOR 1977 Diurnal fluctuations of 02, N2, and CH4 in
Plant Physiol. Vol. 74, 1984
the rhizosphere of Thalassia lestudinum. Limnol Oceanogr 22: 566-570
16. PENHALE PA, RG WETZEL 1983 Structural and functional adaptations of
eelgrass to the anaerobic sediment environment. Can J Bot 61: 1421-1428
17. SCHEGEL HG 1975 Mechanisms of chemo-autotrophy. In 0 Kinne, ed, Manrne
Ecology, Vol 2. Wiley-Interscience, New York, pp 9-60
18. SMITH RD, WC DENNISON, RS ALBERTE 1982 Role of shoot photosynthesis in
root-rhizome respiration in Zostera marina L. (eelgrass). Biol Bull 163: 368369
19. TEAL JM, JW KANWISHER 1966 Gas transport in the marsh grass. Spartina
alterniflora. J Exp Bot 17: 355-361
20. TOMLINSON PB 1980 Leaf morphology and anatomy in searsses. In RC
Phillips, CP McRoy, Handbook of Seagrass Biology: An Ecosystem Perspective. Garland STPM Press, pp 7-28
Downloaded from on June 15, 2017 - Published by www.plantphysiol.org
Copyright © 1984 American Society of Plant Biologists. All rights reserved.