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Plant Physiol. (1998) 116: 439-444
The Small, Methionine-Rich Chloroplast Heat-Shock Protein
Protects Photosystem II Electron Transport during Heat
Stress1
Scott A. Heckathorn2, *,
Craig A. Downs,
Thomas D. Sharkey, and
James S. Coleman3
Department of Biology, Syracuse University, 130 College Place,
Syracuse, New York 13244-1220 (S.A.H., J.S.C.); and Department of
Botany, University of Wisconsin, 430 Lincoln Drive, Madison,
Wisconsin 53706 (C.A.D., T.D.S.)
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ABSTRACT |
Evidence
suggests that the small chloroplast heat-shock protein (Hsp) is
involved in plant thermotolerance but its site of action is unknown.
Functional disruption of this Hsp using anti-Hsp antibodies or addition
of purified Hsp to chloroplasts indicated that (a) this Hsp protects
thermolabile photosystem II and, consequently, whole-chain electron
transport during heat stress; and (b) this Hsp completely accounted for
heat acclimation of electron transport in pre-heat-stressed plants.
Therefore, this Hsp is a major adaptation to acute heat stress in
plants.
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INTRODUCTION |
PSII (the H2O-oxidizing, quinone-reducing
complex) is usually the most heat sensitive of the chloroplast
thylakoid-membrane protein complexes involved in photosynthetic
electron transfer and ATP synthesis and is one of the most thermolabile
photosynthetic processes in general (Berry and Björkman, 1980 ;
Weis and Berry, 1988; Havaux, 1993). Within PSII, the
O2-evolving-complex proteins are frequently the
most susceptible to heat stress, although both the reaction center and
the light-harvesting complexes can be disrupted by high temperatures as
well (Berry and Björkman, 1980; Weis and Berry, 1988; Havaux,
1993). Thermotolerance of PSII varies widely among species and there is
also variation in the extent of acclimation of PSII to heat stress
(Berry and Björkman, 1980; Weis and Berry, 1988). With the
exception of the probable protective effect of xanthophyll-cycle
carotenoids (Havaux et al., 1996) and isoprene (Sharkey and Singaas,
1995) on membrane stability and PSII function, little is known about
the protective adaptations of PSII to heat stress. However,
accumulating evidence suggests that chloroplast Hsps are involved in
photosynthetic and PSII thermotolerance.
For example, when phenotypic variation in the production of the major
chloroplast lmw Hsp is induced (e.g. by manipulating N availability),
increased levels of the lmw Hsp are positively correlated with
increased thermotolerance of PSII (Stapel et al., 1993; Clarke and
Critchley, 1994; Heckathorn et al., 1996). Additionally, greater
production of the chloroplast lmw Hsp, both within (Park et al., 1996)
and among species (Downs et al., 1997), is positively correlated with
whole-plant thermotolerance. Also in support of this, several
chloroplast fractionation studies indicate that the lmw Hsp is a
stromal protein that associates with the thylakoid membranes in
response to heat stress (Restivo et al., 1986; Glaczinski and
Kloppstech, 1988; Adamska and Kloppstech, 1991; Debel et al., 1997;
also see Vierling, 1991; Clark and Critchley, 1994). However, a
definite role of this or other Hsps in photosynthetic thermotolerance has not been demonstrated.
In contrast to most hmw Hsps, which are constitutively expressed and
are essential for protein folding and import into organelles (i.e. they
are molecular chaperones) (Gatenby and Viitanen, 1994; Hartl, 1996),
lmw Hsps (approximately 17-30 kD) are generally produced only in
response to environmental stress and little is known about their
function (Vierling, 1991; Howarth and Ougham, 1993; Parsell and
Lindquist, 1994; Boelens and de Jong, 1995; Waters et al., 1996).
Purified lmw Hsps from both plants and animals have been shown to
prevent aggregation or facilitate reactivation of other proteins in
vitro (Jakob et al., 1993; Merck et al., 1993; Lee et al., 1995). Also,
natural in vivo production of lmw Hsps is often correlated with cell or
organismal thermotolerance (Vierling, 1991; Howarth and Ougham, 1993;
O'Connell, 1994; Parsell and Lindquist, 1994; Boelens and de Jong,
1995; Waters et al., 1996), and thermotolerance of mutant mammalian,
protistan, and fungal cells that over- or underexpress lmw Hsps
increases or decreases, respectively (Loomis and Wheeler, 1982; Landry
et al., 1989; Plesofsky-Vig and Brambl, 1995). These studies indicate that lmw Hsps are an important adaptation to heat stress, perhaps by
functioning as molecular chaperones.
lmw Hsps are often the most abundant group of Hsps in plants, whereas
in other organisms hmw Hsps are the most abundant (Vierling, 1991;
Howarth and Ougham, 1993; O'Connell, 1994; Parsell and Lindquist, 1994; Boelens and de Jong, 1995; Waters et al., 1996). Plants typically
produce more than 10 lmw Hsps in response to heat stress, with each Hsp
belonging to one of six distinct gene classes. In other organisms, only
one or two lmw Hsps of a single class are produced. Two of these gene
classes encode proteins that localize to the cytosol, one class each
encodes proteins that localize to the ER, mitochondria, and
chloroplasts, and localization of the sixth class is unknown (Vierling,
1991; Waters, 1995; Waters et al., 1996).
The chloroplast lmw Hsp, first described in 1986 (Vierling et al.,
1986), has two conserved regions in common with other lmw Hsps, but has
a third domain that is unique. This Met-rich domain is predicted to
form an amphipathic  -helix, similar to the 54-kD signal-recognition
particle (Vierling, 1991). This Hsp is nuclear encoded, is produced
only in response to environmental stress, and is usually the most heat
responsive of the chloroplast Hsps. The function of the chloroplast lmw
Hsp remains unknown; however, as noted above, this protein may be
involved in PSII thermotolerance. In this study we directly test
whether the chloroplast lmw Hsp confers thermotolerance to PSII
function or to other aspects of thylakoid electron transfer.
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MATERIALS AND METHODS |
Plant Material and Growth Conditions
Tomato (Lycopersicon esculentum Mill. cv UC82B) plants
were grown from seed in 8-L pots containing commercial potting soil, and were watered daily and fertilized weekly with one-half-strength Hoagland solution. Plants were raised in growth chambers under 25/18°C day/night temperatures and at 900 µmol
m 2 s1 PPFD. Plants were
heat stressed by gradually increasing the chamber temperature over
2 h to 42°C, holding this temperature for 6 h, and then
gradually decreasing the temperature over 2 h back to control
conditions. Control plants were maintained throughout at 25°C. During
heat stress the plants were kept well watered and the growth chambers
were humidified by misting to prevent water stress.
Antisera Production
Polyclonal rabbit antiserum specific to the Met-rich domain of the
chloroplast lmw Hsp (Abmet) was produced using a
synthetic oligopeptide antigen (as described by Downs et al., 1997).
Antiserum with broad specificity (among species and lmw Hsp classes) to the highly conserved -crystallin region of plant lmw Hsps
(Ab ) was generated in a similar way, using an
amino acid sequence that encompasses domain II and part of the segment
between domains I and II of the carboxyl-terminal region of lmw Hsps
(i.e. the -crystallin region) (Vierling, 1991; Caspers et al., 1995;
Waters, 1995; Waters et al., 1996). The sequence of the oligopeptide
antigen, designed using amino acid sequences obtained from GenBank (see Waters, 1995), is as follows:
NH2-RVERSSGKFVRRFRLPENAKVDQVKASMENGVLTVTVPK-COOH. The oligopeptide and antiserum were produced by Bio-Synthesis (Lewisville, TX).
Electron-Transport Assays
Intact chloroplasts were isolated as described by Downs et al.
(1997), but without protease treatment, inspected microscopically for
purity and intactness (approximately 80-90%), and lysed in 50 mm Hepes, pH 7.6, 50 mm sorbitol, 5 mm MgCl2, 5 mm NaCl, 19 mm NH4Cl, to which was added: 5 mm (final concentration) NaN3 and 50 µm MV, for whole-chain assays; 10 µm
dichlorophenyl dimethylurea, 100 µm dichlorophenol
indophenol, and 5 mm ascorbate for PSI assays; or 50 µm parabenzoquinone and 25 µm dibromomethyl
isopropyl benzoquinone for PSII assays (Allen and Holmes, 1986).
Chloroplasts were incubated at either 25 or 47°C for 2 min, and then
Abmet or Ab was added
(1:300) to some chloroplast samples; either nothing, whole-molecule goat IgG (1:300), or BSA (250 µg/mL) was added to other samples as
negative controls. Similar results were obtained whether IgG, Abmet, and Ab were added
at dilutions of 1:60, 1:150, 1:300, or 1:1,500; however, at 1:10,000,
the efficiency of Abmet and Ab began to decrease.
Proteins were added 1 min after steady-state rates of electron
transport were observed (approximately 90 s after samples were illuminated and 2 min after incubation began); similar results were
obtained when proteins were added before illumination. The rate of
electron transport for whole-chain (water-to-MV), PSII (water-to-parabenzoquinone), and PSI (ascorbate/dichlorophenol indophenol-to-MV) assays was determined by monitoring liquid-phase O2 uptake (whole-chain and PSI) or evolution
(PSII) (Walker, 1990). The chlorophyll concentration of the samples was
25 µg/mL. The light intensity was 1000 µmol
m2 s1 PPFD. Results
were analyzed by three-way (control/heat stress × incubation
temperature × protein addition) ANOVA. Differences among protein
additions within each control/heat-stress × incubation-temperature combination were analyzed by Sheffe's
multiple-comparison test, following significant ANOVA results for
effects of protein additions.
Purification of lmw Hsp
Abmet was purified from whole serum by first
removing all IgGs using protein A-Sepharose, and then separating
Abmet from other IgGs using immobilized purified
antigen. Affinity-purified Abmet was then
covalently conjugated to 3M Emphaze Biosupport medium AB1 (Pierce),
following the suppliers' protocols. Chloroplasts were isolated from
heat-stressed tomato plants, lysed, and resuspended in 50 mm Hepes, pH 7.8, 1 mm PMSF, 1 mm
benzamide, 100 mm EDTA, 10 µm leupeptin, and
10 µm antipain. Chloroplast samples were filtered (0.45 µm) and passed by gravity flow through a 3-mL column (60 × 5 mm) containing 1.5 mL of beads with
Abmet. The column was washed with PBS and bound
proteins were eluted using 0.1 m Gly, pH 2.5. The elution
was titrated to pH 7.0 using KOH and then centrifuged in a 30-kD
pore-size microconcentrator (Millipore) to separate Hsp from any eluted
IgG. Hsp purity was determined by SDS-PAGE (12.5% gel; 5 µg of total
protein per lane), followed by staining with silver or Coomassie blue
(as described by Heckathorn et al., 1996; Downs et al., 1997). The
identity of the lmw Hsp was confirmed by electroblotting proteins in
unstained replicate lanes to PVDF membranes, and then probing with
Abmet, followed by secondary antibody conjugated
to alkaline phosphatase. Secondary antibody was detected with nitroblue
tetra- zolium/5-bromo-4-chloro-3-indolyl phosphate.
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RESULTS AND DISCUSSION |
To examine the importance of the lmw Hsp to photosynthetic
electron transport, we used polyclonal antibodies specific to either the unique Met-rich domain of the chloroplast lmw Hsp
(Abmet), or to another conserved domain common to
most plant lmw Hsps (Ab), to disrupt the
function of the lmw Hsp in chloroplasts isolated from tomato plants. We
then monitored photosynthetic electron transport by measuring
O2 exchange of chloroplasts from unstressed control plants and plants that had been heat stressed at 43°C (pre-heat-stressed plants). Electron transport in control and pre-heat-stressed plants was assayed at both 25 and 47°C.
The rate of whole-chain electron transport was lower when assayed at
47°C than at 25°C (ANOVA; P < 0.0001), and pre-heat-stressed plants had lower rates of whole-chain electron transport compared with
control plants (P < 0.0001) (Fig.
1A). Whole-chain electron transport was
greater in pre-heat-stressed plants relative to controls at 47°C,
which indicates that acclimation to high temperature occurred in
pre-heat-stressed plants. This acclimation appeared to be entirely the
result of the production of the chloroplast lmw Hsp, because the
addition of Abmet and
Ab, which we predicted would disrupt the
function of the chloroplast lmw Hsp, decreased whole-chain electron
transport in pre-heat-stressed plants incubated at 47°C by 54%,
slightly less than that of control plants at the same temperature.
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| Figure 1.
The effect of Hsp-specific antibodies on
photosynthetic electron transport. Chloroplasts were isolated from
10-week-old tomato plants grown at 25/18°C day/night
temperatures or from plants heat stressed for 6 h at 43°C
(control or pre-heat-stressed, respectively). Chloroplasts were lysed
and then incubated at 25 or 47°C. Either nothing (no addition), IgG,
BSA, Abmet, or Ab was added to chloroplast
samples before determination of the rate of whole-chain (A), PSII (B),
or PSI electron transport (C). Results are means ± 1 se; n = 3 to 4 (each from a separate
set of chloroplasts). Differences (P < 0.05) among protein
additions within each control/heat stress × incubation-temperature combination are indicated by asterisks (*). chl,
Chlorophyll.
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The addition of IgG or BSA had little effect on whole-chain electron
transport of chloroplasts from pre-heat-stressed plants assayed at 25 or 47°C or in control plants at 25 and 47°C. Preimmune serum also
had no effect on whole-chain electron transport, regardless of assay
temperature or previous heat-stress status (not shown; limited
availability of preimmune serum constrained the number of replicates to
two and precluded conducting similar assays for PSII and PSI electron
transport, but see below). No effect of Abmet or
Ab was observed in control plants at either 25 or 47°C, as expected, because we observed no significant accumulation of the chloroplast lmw Hsp in leaves in the absence of heat stress (Downs et al., 1997). We also observed no effect of
Abmet or Ab at 25°C in
pre-heat-stressed plants. These results indicate that the chloroplast
lmw Hsp protects photosynthetic electron transport at high temperature,
but has no effect at control temperatures, and causes heat acclimation
of whole-chain electron transport resulting from pre-heat stress.
We next measured PSII and PSI electron transport separately, while
disrupting the function of the chloroplast lmw Hsp with antibodies, to
determine more specifically which aspects of photosynthetic electron
transport were protected by the lmw Hsp. Results for PSII electron
transport were nearly identical to those obtained for whole-chain
electron transport (Fig. 1B); PSII electron transport was lower at
47°C, relative to 25°C (ANOVA; P < 0.0001), and we observed
an increase in electron transport in pre-heat-stressed plants at 47°C
relative to controls at 47°C. This indicates that heat acclimation of
PSII function occurred in pre-heat-stressed plants. Again, this
acclimation was apparently related exclusively to the chloroplast lmw
Hsp, because the addition of Abmet and Ab decreased PSII electron transport in
pre-heat-stressed plants assayed at 47°C by 56%, to slightly less
than that of control plants at 47°C. As before, the addition of IgG
or BSA had little effect on PSII electron transport at 47°C in
pre-heat-stressed plants. No effect of antibody/protein additions was
observed in control plants at either 25 or 47°C or in
pre-heat-stressed plants at 25°C. Similar results, including a
negative effect of Abmet and
Ab and no effect of preimmune serum, were
obtained when PSII function was monitored by analysis of chlorophyll
fluorescence from PSII (i.e. the ratio of variable to maximum
fluorescence of dark-adapted chloroplast samples; data not shown).
In contrast to PSII function, PSI electron transport was slightly
increased by heat stress (Fig. 1C), as is often the case (Berry and
Björkman, 1980; Weis and Berry, 1988; Havaux, 1993). Incubation
of samples at 47°C increased PSI electron transport by 7% compared
with 25°C (ANOVA; P < 0.0165), and pre-heat-stressed plants had
slightly higher rates of electron transport than did controls (12%;
P < 0.0001), but there was no significant interaction between
incubation temperature and pre-heat-stress conditioning (P < 0.0893). PSI electron transport was also unaffected by antibody/protein additions (P < 0.9794). Collectively, results from this
experiment indicate that the chloroplast lmw Hsp protects PSII and,
consequently, whole-chain electron transport during heat stress.
To determine if the chloroplast lmw Hsp could protect photosynthetic
electron transport during heat stress when added to chloroplasts lacking this protein, we purified the chloroplast lmw Hsp from intact
chloroplasts isolated from heat-stressed tomato plants to apparent
homogeneity by antibody-affinity-column chromatography using
Abmet, and then monitored the effects of purified
lmw Hsp on whole-chain electron transport. Both silver (not shown) and Coomassie-blue staining of total protein eluted from the columns and
subjected to SDS-PAGE indicated that only one protein was purified
(Fig. 2A). Immunoblotting (western) on
the other half of the same gels with Abmet
indicated that this protein was the chloroplast lmw Hsp (Fig. 2B). When
purified protein was added to thylakoid membrane preparations derived
from chloroplasts isolated from unstressed control plants (i.e. plants
that did not contain lmw Hsp) incubated at 47°C, the rate of
whole-chain electron transport was 78% of that exhibited by
chloroplast samples incubated at 25°C (Fig.
3). When purified lmw Hsp was not added
to samples at 47°C, the rate of whole-chain electron transport was
only 20% of the rate at 25°C. These results confirm that the
chloroplast lmw Hsp confers thermotolerance to photosynthetic electron
transport.
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| Figure 2.
Homogeneity of the lmw Hsp purified from intact
chloroplasts isolated from heat-stressed tomato plants. Coomassie-blue
stain (A) and immunoblot (western) (B) of protein samples eluted from an Abmet column. Eluted proteins were fractionated by gel
electrophoresis. One-half of the gel (two lanes) was stained with
Coomassie blue to detect all proteins present. Proteins in unstained
replicate lanes were electroblotted to membranes and probed with
Abmet. The locations of molecular mass markers (M), which
were included on both the Coomassie-blue-stained gel and the
immunoblot, are indicated.
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| Figure 3.
The effect of purified chloroplast lmw Hsp on
whole-chain electron transport. Chloroplasts were isolated from
6-week-old unstressed tomato plants grown at 25/18°C day/night
temperatures (i.e. plants without detectable levels of lmw Hsp).
Chloroplasts were lysed and then incubated at 25 or 47°C; samples at
47°C were incubated with or without the addition of purified
chloroplast lmw Hsp (0.0017 µg Hsp/µL). Assuming that all of the
added protein was lmw Hsp and assuming a chlorophyll:PSII stoichiometry
of 400, we estimate that there were approximately 14 lmw Hsps available
per PSII. Results are means ± 1 se;
n = 3. chl, Chlorophyll.
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The rapidity with which the chloroplast lmw Hsp affects PSII function
when disrupted with Abmet and
Ab, or when purified protein is added to
chloroplasts, is unusual among the stress-related functions of Hsps
studied to date (Vierling, 1991; Howarth and Ougham, 1993; O'Connell,
1994; Parsell and Lindquist, 1994; Boelens and de Jong, 1995; Waters et
al., 1996). For example, both lmw and hmw Hsps have demonstrated the
capacity to reactivate previously aggregated or denatured proteins, but
the time required to do so is at least 15 min (Showyra et al., 1990;
Höll-Neugebauer et al., 1991; Jakob et al., 1993; Merck et al.,
1993; Schröder et al., 1993; Lee et al., 1995). The addition of
purified lmw Hsp to chloroplasts had an almost immediate (<1 min)
effect on PSII function (Fig. 4). The
disruptive effect of Abmet and
Ab on PSII function (e.g. Fig. 1) was equally
rapid (not shown). The speed with which the lmw Hsp protects PSII in
vivo may not necessarily equal that observed in vitro.
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| Figure 4.
Time course of the effect of purified chloroplast
lmw Hsp on whole-chain electron transport. Shown is a trace of an
O2 electrode millivolt output through time of a
representative chloroplast sample from unstressed control plants (i.e.
lacking lmw Hsp). The sample was incubated with illumination (1000 µmol m2 s1 PPFD) at 47°C in a
well-stirred, transparent, temperature-controlled cuvette. Chloroplast
lmw Hsp was added approximately 2 min after steady-state rates of
electron transport were observed. The rate of whole-chain electron
transport was calculated from the rate of liquid-phase O2
uptake, which is proportional to the millivolt output generated by the
O2-electrode sensor.
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The method used in this study to rupture intact chloroplasts (mild
hypotonic lysis) and the NaCl concentration of the medium in which
broken chloroplasts were resuspended (5 mm) should have ruptured the chloroplast outer envelope without rupturing the thylakoids, and resulted in unstacked thylakoid membranes (Gegenheimer, 1990). Thus, accessibility to PSII may be greater in vitro than in
vivo, where most PSII reaction centers are localized to relatively inaccessible grana regions. In vitro disruption of thylakoid
organization may therefore increase the speed of Hsp function relative
to in vivo speed, and may also increase antibody accessibility to Hsp.
Taken together, our results demonstrate that the chloroplast lmw Hsp is
an important determinant of photosynthetic thermotolerance. The
chloroplast lmw Hsp (a) increases PSII and, consequently, whole-chain
electron transport during heat stress (by as much as 7-fold in our
experiments; Fig. 3, 47°C for  Hsp versus 47°C for +Hsp); (b)
completely accounts for all of the observed heat acclimation of PSII
and whole-chain electron transport in pre-heat-stressed plants (Fig.
1); and (c) imparts protection to PSII very rapidly (Fig. 4). These
observations are consistent with those of a number of studies
demonstrating a correlation between the production of the chloroplast
lmw Hsp and PSII or organismal thermotolerance (Stapel et al., 1993;
Clarke and Critchley, 1994; Heckathorn et al., 1996; Park et al., 1996;
Downs et al., 1997). To our knowledge, results from this study are the
first direct evidence that Hsps (chloroplast or otherwise) play a role
in photosynthetic thermotolerance. Because it is well established that
PSII is a highly thermolabile component of photosynthetic electron
transport in particular, and one of the most thermosensitive aspects of
net photosynthesis and plant performance in general (Berry and
Björkman, 1980; Weis and Berry, 1988; Havaux, 1993), production
of the chloroplast lmw Hsp represents an important adaptation of plants
to acute heat stress.
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FOOTNOTES |
1
This work was supported by grants from the
National Science Foundation (IBN 9317900 to T.D.S. and IBN 9357302 and
9207203 to J.S.C.) and the Andrew W. Mellon Foundation (to J.S.C.).
C.A.D. was an Advanced Opportunity Predoctoral Fellow.
2
Present address: Department of Biology,
University of Charleston, 58 Coming Street, Charleston, SC 29424.
3
Present address: Desert Research Institute, 7010 Dandini Boulevard, Reno, NV 89512.
*
Corresponding author; e-mail heckathorns{at}cofc.edu; fax
1-803-953-5453.
Received August 4, 1997;
accepted September 18, 1997.
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ABBREVIATIONS |
Abbreviations:
Ab, antibody.
ANOVA, analysis of variance.
hmw, high-molecular-weight.
Hsp, heat-shock protein.
lmw, low-molecular-weight.
MV, methyl viologen.
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ACKNOWLEDGMENTS |
We thank E. Craig, J. Slovin, and anonymous reviewers for
helpful comments on the manuscript and M. Shahan for assistance with
affinity purification of Abmet.
| |
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Abstract
Introduction