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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
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