|
Plant Physiol, April 2003, Vol. 131, pp. 1529-1543
Phloem Metabolism and Function Have to Cope with Low Internal
Oxygen1
Joost T.
van Dongen,
Ulrich
Schurr,
Michelle
Pfister, and
Peter
Geigenberger*
Max Planck Institute of Molecular Plant Physiology, Am
Mühlenberg 1, 14476 Golm, Germany (J.T.v.D., P.G.); Institute for
Phytosphere Research, Forschungszentrum Jülich, 52425 Jülich, Germany (U.S.); and Botanisches Institut der
Universität Heidelberg, Im Neuenheimer Feld 360, 69120 Heidelberg, Germany (M.P.)
We have investigated the consequences of endogenous
limitations in oxygen delivery for phloem transport in Ricinus
communis. In situ oxygen profiles were measured directly across
stems of plants growing in air (21% [v/v] oxygen), using a
microsensor with a tip diameter of approximately 30 µm. Oxygen levels
decreased from 21% (v/v) at the surface to 7% (v/v) in the
vascular region and increased again to 15% (v/v) toward the hollow
center of the stem. Phloem sap exuding from small incisions in the bark
of the stem was hypoxic, and the ATP to ADP ratio (4.1) and energy
charge (0.78) were also low. When 5-cm stem segments of intact plants were exposed to zero external oxygen for 90 min, oxygen levels within
the phloem decreased to approximately 2% (v/v), and ATP to ADP ratio
and adenylate energy charge dropped further to 1.92 and 0.68, respectively. This was accompanied by a marked decrease in the phloem
sucrose (Suc) concentration and Suc transport rate, which is likely to
be explained by the inhibition of retrieval processes in the phloem.
Germinating seedlings were used to analyze the effect of a stepwise
decrease in oxygen tension on phloem transport and energy metabolism in
more detail. Within the endosperm embedding the cotyledons next to the
phloem loading sitesoxygen decreased from approximately 14% (v/v) in
6-d-old seedlings down to approximately 6% (v/v) in 10-d-old
seedlings. This was paralleled by a similar decrease of oxygen inside
the hypocotyl. When the endosperm was removed and cotyledons incubated
in a 100 mM Suc solution with 21%, 6%, 3%, or 0.5%
(v/v) oxygen for 3 h before phloem sap was analyzed, decreasing
oxygen tensions led to a progressive decrease in phloem energy state,
indicating a partial inhibition of respiration. The estimated ratio of
NADH to NAD+ in the phloem exudate remained low
(approximately 0.0014) when oxygen was decreased to 6% and 3% (v/v)
but increased markedly (to approximately 0.008) at 0.5% (v/v) oxygen,
paralleled by an increase in lactate and ethanol. Suc concentration and
translocation decreased when oxygen was decreased to 3% and 0.5%
(v/v). Falling oxygen led to a progressive increase in amino acids,
especially of alanine,  -aminobutyrat, methionine, and isoleucine, a
progressive decrease in the C to N ratio, and an increase in the
succinate to malate ratio in the phloem. These results show that oxygen concentration is low inside the transport phloem in planta and that
this results in adaptive changes in phloem metabolism and function.
1
This work was supported by the Deutsche
Forschungsgemeinschaft (grant no. Ge 878/1-3 to P.G.) and by the
Max-Planck Society (to J.T.v.D.).
*
Corresponding author; e-mail
geigenberger{at}mpimp-golm.mpg.de;fax 49-331-567-8408.
© 2003 American Society of Plant Biologists
This article has been cited by other articles:
|
|
|
|
 
J. T. Van Dongen, A. Frohlich, S. J. Ramirez-Aguilar, N. Schauer, A. R. Fernie, A. Erban, J. Kopka, J. Clark, A. Langer, and P. Geigenberger
Transcript and Metabolite Profiling of the Adaptive Response to Mild Decreases in Oxygen Concentration in the Roots of Arabidopsis Plants
Ann. Bot.,
August 6, 2008;
(2008)
mcn126v2.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
P. Verboven, G. Kerckhofs, H. K. Mebatsion, Q. T. Ho, K. Temst, M. Wevers, P. Cloetens, and B. M. Nicolai
Three-Dimensional Gas Exchange Pathways in Pome Fruit Characterized by Synchrotron X-Ray Computed Tomography
Plant Physiology,
June 1, 2008;
147(2):
518 - 527.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
D. Riewe, L. Grosman, H. Zauber, C. Wucke, A. R. Fernie, and P. Geigenberger
Metabolic and Developmental Adaptations of Growing Potato Tubers in Response to Specific Manipulations of the Adenylate Energy Status
Plant Physiology,
April 1, 2008;
146(4):
1579 - 1598.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
W.-G. Choi and D. M. Roberts
Arabidopsis NIP2;1, a Major Intrinsic Protein Transporter of Lactic Acid Induced by Anoxic Stress
J. Biol. Chem.,
August 17, 2007;
282(33):
24209 - 24218.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R. Spicer and N. M. Holbrook
Effects of carbon dioxide and oxygen on sapwood respiration in five temperate tree species
J. Exp. Bot.,
April 1, 2007;
58(6):
1313 - 1320.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
H. J. Martens, A. G. Roberts, K. J. Oparka, and A. Schulz
Quantification of Plasmodesmatal Endoplasmic Reticulum Coupling between Sieve Elements and Companion Cells Using Fluorescence Redistribution after Photobleaching
Plant Physiology,
October 1, 2006;
142(2):
471 - 480.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
W. S. Peters, A. J. E. van Bel, and M. Knoblauch
The geometry of the forisome-sieve element-sieve plate complex in the phloem of Vicia faba L. leaflets
J. Exp. Bot.,
September 1, 2006;
57(12):
3091 - 3098.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
C. Barber, J. Rosti, A. Rawat, K. Findlay, K. Roberts, and G. J. Seifert
Distinct Properties of the Five UDP-D-glucose/UDP-D-galactose 4-Epimerase Isoforms of Arabidopsis thaliana
J. Biol. Chem.,
June 23, 2006;
281(25):
17276 - 17285.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Meyer, S. Eskandari, S. Grallath, and D. Rentsch
AtGAT1, a High Affinity Transporter for {gamma}-Aminobutyric Acid in Arabidopsis thaliana
J. Biol. Chem.,
March 17, 2006;
281(11):
7197 - 7204.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
T. Will and A. J. E. van Bel
Physical and chemical interactions between aphids and plants
J. Exp. Bot.,
March 1, 2006;
57(4):
729 - 737.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. Mancuso and A. M. Marras
Adaptative Response of Vitis Root to Anoxia
Plant Cell Physiol.,
March 1, 2006;
47(3):
401 - 409.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
W. Shen, Y. Wei, M. Dauk, Y. Tan, D. C. Taylor, G. Selvaraj, and J. Zou
Involvement of a Glycerol-3-Phosphate Dehydrogenase in Modulating the NADH/NAD+ Ratio Provides Evidence of a Mitochondrial Glycerol-3-Phosphate Shuttle in Arabidopsis
PLANT CELL,
February 1, 2006;
18(2):
422 - 441.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
E. Schmalzlin, J. T. van Dongen, I. Klimant, B. Marmodee, M. Steup, J. Fisahn, P. Geigenberger, and H.-G. Lohmannsroben
An Optical Multifrequency Phase-Modulation Method Using Microbeads for Measuring Intracellular Oxygen Concentrations in Plants
Biophys. J.,
August 1, 2005;
89(2):
1339 - 1345.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
T. Terce-Laforgue, F. Dubois, S. Ferrario-Mery, M.-A. Pou de Crecenzo, R. Sangwan, and B. Hirel
Glutamate Dehydrogenase of Tobacco Is Mainly Induced in the Cytosol of Phloem Companion Cells When Ammonia Is Provided Either Externally or Released during Photorespiration
Plant Physiology,
December 1, 2004;
136(4):
4308 - 4317.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. T. van Dongen, G. W. Roeb, M. Dautzenberg, A. Froehlich, H. Vigeolas, P. E. H. Minchin, and P. Geigenberger
Phloem Import and Storage Metabolism Are Highly Coordinated by the Low Oxygen Concentrations within Developing Wheat Seeds
Plant Physiology,
July 1, 2004;
135(3):
1809 - 1821.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
H. Vigeolas, J. T. van Dongen, P. Waldeck, D. Huhn, and P. Geigenberger
Lipid Storage Metabolism Is Limited by the Prevailing Low Oxygen Concentrations within Developing Seeds of Oilseed Rape
Plant Physiology,
December 1, 2003;
133(4):
2048 - 2060.
[Abstract]
[Full Text]
|
|
|
|
|
|
|
K. L. Bologa, A. R. Fernie, A. Leisse, M. Ehlers Loureiro, and P. Geigenberger
A Bypass of Sucrose Synthase Leads to Low Internal Oxygen and Impaired Metabolic Performance in Growing Potato Tubers
Plant Physiology,
August 1, 2003;
132(4):
2058 - 2072.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. J.E. van Bel
Transport Phloem: Low Profile, High Impact
Plant Physiology,
April 1, 2003;
131(4):
1509 - 1510.
[Full Text]
[PDF]
|
|
|
|
|
