Pergamon 0031-9422(95)00635-4 Phytochemistry, Vol. 41, No. 2, pp. 377-384, 1996
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ENDOPEPTIDASES DURING THE DEVELOPMENT AND SENESCENCE OF
LOLIUM TEMULENTUM LEAVES
KARL MORRIS, HOWARD THOMAS and LYNDON J. ROGERS*~'
Institute of Grassland and Environmental Research, Plas Gogerddan, Aberystwyth, Dyfed SY23 3EB, U.K.; *Institute of Biological
Sciences, University of Wales, Aberystwyth, Dyfed SY23 3DD, U.K.
(Received 24 May 1995)
Key Word Index--Lolium temulentum; Gramineae; leaf development; senescence; cysteine endopep-
tidases.
Abstract--The endopeptidase activity of Lolium temulentum leaf tissue was measured using azocasein as a substrate.
The enzyme increased with leaf age, and also during senescence of excised leaf tissue. There were at least two distinct
endopeptidase activities, characterized by different pH optima. The predominant form in leaves of intact plants was
maximally active at pH 5. In detached leaves during the later stages of senescence this activity was replaced by an
enzyme with an optimum at pH 8. An antibody raised against the non-glycosylated cysteine endopeptidase papain
cross-reacted with polypeptides in protein preparations of L. temulentum leaf tissue. The correlation between enzyme
activity and the pattern of immunoreactive polypeptides suggested that the polyclonal antibody was able to recognize
the Lolium homologues of papain. The switch from pH 5 to pH 8 enzyme in detached leaves was associated with an
evident decrease in the M, values of papain-like antigens detected on western immunoblots, from ca 60 000 to 30 000.
It is possible that the alkaline activity is derived from the acid form, perhaps by limited autolysis in protein-depleted
tissue at an advanced stage of senescence. On the other hand, the response of protease activation to treating leaf tissue
with inhibitors of protein biosynthesis is more consistent with de novo appearance of a different form of the enzyme in
late senescence.
INTRODUCTION
The leaves of many plant species are rich sources of
proteolytic enzymes [1-3], but the physiological func-
tions of the major proteases are not clear. Although there
are exceptions, protease activities in most leaves increase
with age, and particularly when foliar senescence is pro-
moted by stress or excision. Protein mobilization is char-
acteristic of senescing tissues, but it has proved difficult to
establish a direct connection with increased levels of
protease. In cereals, grasses and many other species,
most of the measurable proteolytic activity of leaves is
accounted for by a small number of acid endopeptidases
[1,4-6]. Consistent with the low pH optimum is the
observation that the acid endopeptidase activity of me-
sophyll cells is located predominantly in the vacuole
[7-11]. For these enzymes to play a direct part in pro-
teolysis during senescence there must be some kind of
interchange between the vacuole and the chloroplast,
which is the site of most of the mobilizable protein of leaf
cells [12, 13]. Such contacts between the two organelles
have never been convincingly demonstrated.
tAuthor to whom correspondence should be addressed.
As well as acid endopeptidases, activities at neu-
tral-alkaline pH values have been detected [3, 14-16].
The alkaline protease of oat leaves is located outside
the vacuole [ 11, 16]. Experiments with inhibitors indicate
that senescence-related increases in protease activity
require protein synthesis [2]. Recently, cDNAs encod-
ing proteases with homology to cysteine endopeptidases
have been isolated from Arabidopsis [17] and maize
[18] and used to show increased abundance of the
corresponding mRNAs during senescence. It seems
likely, therefore, that both transcription and transl-
ation are necessary for protease activation in ageing leaf
tissue.
Lolium temulentura has been used extensively for
studies of leaf growth and senescence [ 19-21]. Detached
leaves of this species [15] initially accumulated acid
protease activity and subsequently replaced it with a
neutral-alkaline protease, the dominant enzyme in
late senescence. We have re-examined L. temulentura
leaf proteases with the object of characterizing the
pH response in more detail, applying an immunolog-
ical approach to visualizing qualitative changes in pro-
tease complement, and establishing the degree to which
these changes depend on current protein synthesis.
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