Pergamon 0031-9422(94)00774-8 Phytochemistry, Vol. 38, No. 5, pp. t 147-1150, 1995
Copyright © 1995 Elsevier Science Ltd
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ANAEROBIC ACCUMULATION OF 4-AMINOBUTYRATE IN RICE
SEEDLINGS; CAUSES AND SIGNIFICANCE
NICOLETTA AURISANO,ALCIDEBERTANI and REMO REGGIANI
Istituto Biosintesi Vegetali, C.N.R., Via Bassini, 15, 20133 Milano, Italy
(Received in revisedform 25 July 1994)
Key Word Index--Oryza sativa; Gramineae; rice; 4-aminobutyrate; anoxia; root; shoot; glutamate;
protein; amino acids.
Abstract--Accumulation of 4-aminobutyrate is induced by anoxia in rice seedlings. The induction of 4-aminobutyrate
accumulation in aerobic conditions by treatments with exogenous 4-aminobutyrate, Gabaculine and glutamate is well
tolerated by the seedlings. The inhibition of protein synthesis in aerobic and anaerobic conditions by cycloheximide
shows that this process competes with glutamate decarboxylase for glutamic acid. The sensitivity of the anaerobic 4-
aminobutyrate accumulation to azaserine indicates that glutamate synthase is important in maintaining glutamate
availability. The different tolerance to anoxia and protein metabolism of shoot and root of rice suggests that the causes
leading to 4-aminobutyrate accumulation in these tissues are different. It is suggested that ammonia reassimilation in
root plays an important role in the synthesis of 4-aminobutyrate.
INTRODUCTION
In the plant kingdom, the non-protein amino acid 4-
aminobutyrate (Gaba) is ubiquitous and its concentra-
tion in the tissues is often similar to those of the normal
protein amino acids [I, 2]. The physiological role of
Gaba in plants has not been clearly established. This
compound is present in transport fluids and can provide,
through the Gaba shunt, carbon for energy production
and nitrogen for amino acid biosynthesis [2]. In the
central and peripheral nervous system of vertebrates,
Gaba acts as an inhibitory neurotransmitter by increas-
ing the membrane conductance to CI- ions and mem-
brane polarization [3]. Evidence of a similar function in
plants is lacking. Many reports indicate that the level of
Gaba increases rapidly in plant tissues in response to
various forms of stress [4-6] among which anaerobiosis
is the condition inducing the largest accumulation [7, 8].
In wheat roots, the process of Gaba accumulation has
been shown to be mediated by the phytohormone ABA
[9].
Gaba is synthesized in plant tissues by the irreversible
~-decarboxylation of L-glutamic acid in a reaction cata-
lysed by glutamate decarboxylase (GDC). An alternative
source of Gaba is the oxidation of polyamines but this is
probably lower than for glutamate decarboxylation and
null under anaerobiosis [7, 9]. The synthesis of Gaba has
been suggested to be an adaptive response of plant tissues
to stress-induced cellular acidosis [2]. The advantage of
this process would be the concomitant H + consumption
during decarboxylation which ameliorates the eytosolic
acidification [10]. A decline in the cytosolic pH is a
phenomenon extremely marked under oxygen deficit
stress [11, 12].
This investigation used seedlings of rice which tolerate
an anaerobic stress [12]. The coleoptile of rice is also
capable of anaerobic elongation [13]. This study seeks to
widen the knowledge about the role of Gaba in plants and
the causes leading to its accumulation under anoxia.
RESULTSAND DISCUSSION
The effect of anaerobic conditions on the Gaba content
in shoot and root of rice is shown in Fig. I. As can be seen,
24 hr of anoxia induced an accumulation of ca 3.5 and
6.3/zmolg-i fr. wt of Gaba in shoot and root, respect-
ively. No change in Gaba concentration was observed
after an additional day of growth in air. The large increase
in Gaba content in anaerobiosis is in agreement with that
previously described by us [7] and other authors [8,
14-16]. Moreover, the synthesis of Gaba under stress
conditions, advantageous for the pH-stat of the cell [I, 2,
9], could also occur due to the low toxicity of this amino
acid. To test this hypothesis, we carried out 24 hr treat-
merits with exogenous Gaba (I mM), Gabaculine (I mM,
an inhibitor of Gaba transaminase, Fig. 2, arrow H) or
glutamate (I raM) in order to increase the level of Gaba in
non-stress conditions (aerobiosis). As can be seen in
Fig. I, the Gaba and glutamate treatments increased the
concentration of this amino acid in both shoot and root.
The exogenous supply of Gaba led to endogenous values
similar to those observed in anaerobic shoot and root.
The Gabaculine treatment induced Gaba accumulation
1147