Diurnal control of the drought-inducible putative histone H1 gene in tomato (Lycopersicon esculentum Mill. L.)
Journal of Experimental Botany
Diurnal control of the drought-inducible putative histone H1 gene in tomato (Lycopersicon esculentum Mill. L.)
Janet E. Corlett 0
Sally Wilkinson 0
Andrew J. Thompson 0
Horticulture Research International 0
Warwick CV 0
0 Institute of Environmental and Natural Sciences, Department of Biological Sciences, Lancaster University , Lancaster LA1 4YQ , UK
The mRNA of genes le20, lcyP2, lhcII, and asr1 was quantified in leaves and roots of tomato plants (Lycopersicon esculentum Mill. L.) during three day/night cycles and 48 h constant illumination. lcyp2 and lhcII are known to exhibit diurnal or circadian rhythms in leaf tissue while asr1 has shown no evidence of diurnal fluctuations. Previously reported diurnal fluctuations of le20 mRNA in leaves could have been due to either changes in plant water status and abscisic acid concentration (le20 is a drought- and ABA-inducible gene) or changes in climate variables. Plants were grown hydroponically and at constant temperature (20.6±0.5 °C) and humidity (66±1%) such that no changes in plant water status or tissue ABA concentration were detectable. le20, lcyP2 and lhcII mRNAs all fluctuated diurnally in leaf tissue and all reached a maximum during the light period. Surprisingly, le20 and lcyP2 mRNA showed diurnal cycles in root tissue. There was no evidence for diurnal trends in asr1 mRNA, but levels increased steadily during constant light in both leaves and roots. le20, lcyP2 and lhcII mRNA showed only one cycle during 48 h illumination and while carbon assimilation remained high and constant during this period, stomatal conductance decreased after 6 h light and then remained low. Photosystem II efficiency decreased during illumination, recovered during dark periods and showed a weak rhythm during constant light. It was concluded that le20 and lcyP2 have a diurnal component controlling their expression in leaves and roots, responding to light/dark cycles independently of water status or ABA concentration.
Tomato; histone H1; le20; lcyP2; diurnal trends
Several tomato (Lycopersicon esculentum Mill. L.) genes
have been isolated (eg. cDNAs le4, le16, le20, and le25)
whose expression is increased by elevated abscisic acid
(ABA) and by drought
(Cohen and Bray, 1990; Kahn
et al., 1993)
. These genes were identified as a result of
their elevated expression in detached, water-stressed
leaves of wild-type compared to ABA-deficient flacca
plants. However, experimental evidence for the function
of these genes is lacking, and further characterization of
their expression patterns may provide clues about
The le20 gene is of particular interest because it encodes
a protein with strong sequence homology to histone H1.
Putative histone H1 genes, with drought-induced
expression and close homology with le20, have also been
detected in Lycopersicon pennellii, L. chilense and
( Wei and O’Connell, 1996)
(Ascenzi and Gantt, 1997)
H1, a highly polymorphic histone, is known to bind to
the internucleosomal regions of chromatin and its
function may be to modulate the expression of specific groups
of genes, or to repress transcription initiation through
changing high-order chromatin structure ( Zlatanova and
3 To whom correspondence should be addressed. Fax: +44 1 789 470552. E-mail:
Abbreviations: DW, dry weight; Fm (15 min), maximal chlorophyll fluorescence on full reduction of the primary quinone electron acceptor of photosystem
II with a saturating flash after 15 min dark adaptation; Fo, the point of discontinuity in the initial rise of induced fluorescence in dark adapted leaves—
indicating fluorescence obtained before any reduction of the primary quinone electron acceptor occurs; Fv, variable fluorescence (Fm (15 min)−Fo); Fv/Fm,
Fv/Fm (15 min).
Van Holde, 1992;
Workman and Buckman, 1993
Paranjape et al., 1994
). Most reports to date have shown
histone H1 acting to repress gene expression, for example,
reduction of histone H1 expression in Xenopus using
ribozymes led to a specific increase in the expression
of 5S genes
(Bouvet et al., 1994 )
. However, using
Tetrahymena cells in which histone H1 genes were deleted
it was shown that histone H1 acts as both a positive and
negative gene-specific regulator of transcription
and Gorovsky, 1996)
In a previous expression study, le20 mRNA was
detected in leaves of well-watered plants and increased
during the day apparently in response to mild water
( Thompson and Corlett, 1995 )
. Over a 3 d period
of increasing water deficits, diurnal trends in gene
expression were superimposed on an overall increase in le20
mRNA. le20 mRNA levels declined significantly
overnight in the absence of any change in plant water status.
Evidence for a diurnal fluctuation in histone H1
transcripts has been presented for L. pennellii Corr.
( Wei and
O’Connell, 1996 )
(Szekeres et al., 1995 )
in neither case has this diurnal rhythm been shown to be
independent of diurnal fluctuations in water status or
climate variables such as irradiance, temperature and
humidity. Root expression of 1e20 in L. esculentum and
of homologous genes in L. pennellii, and L. chilense is
( Kahn et al, 1993; Wei and O’Connell,
, but has not been quantified in time-course studies.
lcyP2 is a putative cysteine proteinase gene and shares
88% amino acid identity with two wound-inducible
tobacco genes whose mRNA fluctuates diurnally
( Linthorst et al., 1993a)
. Four other putative cysteine
proteinase genes responsive to osmotic stress have been
isolated from Arabidopsis and pea ( Thompson and
Corlett, 1995, and references therein), and recently the
product of the pea gene Cyp15a was localised to the
(Jones and Mullet, 1995 )
. In a previous study, lcyP2
mRNA expression was enhanced in unwatered versus
well-watered plants, but also showed a strong diurnal
rhythm, falling in the afternoon when water deficits were
( Thompson and Corlett, 1995)
. Thus, for a
‘water-deficit inducible’ gene, the diurnal rhythm of lcyP2
mRNA was in opposition to the daily trends in plant
water status. It was likely, therefore, that stress and time
of day responses for this gene were independently
The current experiment was designed to test whether
le20 has a diurnal rhythm of expression in leaves and/or
roots independent of drought stress or ABA signals. Also
studied was the expression of two genes expected to have
diurnal or circadian components to their mRNA
(lcyP2; Linthorst et al. 1993a; lhcII; Pichersky et al.,
and a gene expected to have no diurnal pattern
(asr1; Rossi and Iusem, 1994; Thompson and Corlett,
Materials and methods
Controlled environment and plant material
Tomato seeds (Lycopersicon esculentum Mill. L. cv. Ailsa Craig)
were sown into sand in individual modules, watered with
commercial tomato feed ( Vitafeed 214, Vitax Ltd., Skelmersdale,
UK ) and grown in a glasshouse for approximately 3 weeks.
Plants of uniform size were selected and transferred to a
hydroponic system after washing the sand oV the roots. Each
plant was supported in the hydroponic system so that its roots
were kept in the dark and individually supplied with a constantly
circulating nutrient solution. The nutrient solution (N:
190 mg l−1, P: 60 mg l−1, K: 280 mg l−1, Ca: 135 mg l−1 plus
trace elements Mg, Fe, Zn, Mn, Cu, B, S, Na, and Cl ) was
continuously aerated and cooled by a heat-exchange system.
Prior to the experiments the pH of the solution was adjusted
daily to remain in the range 6.3–6.5 (conductivity 30–34 mV )
either by adding concentrated nutrient solution or HCl. During
experiments, solution pH, conductivity and temperature were
measured each time plant samples were taken. Plants were
arranged in four 2 m long troughs, 14 plants to a trough in a
3×3×3 m walk-in growth room ( Weiss Technik, Ascot, UK ).
Radiative heating of the hydroponic system was minimized by
using white reflective plastic to cover exposed surfaces.
Photosynthetically active radiation (PAR) at plant height was
approximately 500 mmol m−2 s−1 during the 12 h day and all
light was excluded during the 12 h night except for a green ‘safe
light’ used during measurements. Vertical air velocity through
the chamber was 0.3 m s−1, air temperature was set at 20 °C
and humidity at 66% for both day and night. Temperature and
humidity were recorded at 10 min intervals by both the growth
chamber’s own monitoring system and by a temperature/
humidity probe at plant height (Datahog, Skye, Llandrindod
Welles, UK ). Plants were acclimated for at least seven day/night
cycles before the start of each experiment.
At specific sampling times (see below) randomly selected plants
were removed from the hydroponics and roots were separated
from shoots. For each plant, root material was divided into
two equivalent sub-samples for immediate freezing in liquid
nitrogen. Leaflets were separated from stem and petiole and the
leaflet material only was frozen in paired sub-samples as for
roots. One sub-sample was used for ABA and sugar analysis
and the other for total RNA extraction.
In a 24 h experiment, sampling was started 1 h before the
beginning of the light period and triplicate samples taken at 4 h
intervals with two plants bulked per triplicate. In a 96 h
experiment triplicate samples (one plant per sample) were taken
at 12 h intervals starting 1 h before the beginning of the light
period, continuing through two day/night cycles followed by
48 h continuous light. Additional single or triplicate samples
were taken at 2 or 4 h intervals as shown in the figures.
Plant water status
Leaf thickness varies with the turgor pressure of leaf cells, and
can therefore provide a sensitive and non-invasive indicator of
leaf water status
. In the 96 h experiment leaf
thickness was monitored continuously for the first 72 h on four
experimental plants using displacement transducers. Changes in
output were compared with a ‘control’ transducer to identify
variation caused by factors other than leaf thickness (e.g.
movement of the supporting bench). These plants were not
Tissue was freeze-dried for 48 h, finely ground and extracted
overnight at 5 °C with distilled deionized water using an
extraction ratio of 1:25 (g dry weight:ml water). The ABA
concentration of the extract was determined using a
radioimmunoassay (RIA) following the protocol of
Quarrie et al.
. [G–3H ] (+/−)-ABA, specific activity 2.0 TBq mmol−1
(Amersham International, Bucks, UK ) was diluted to
8.9 nmol dm−3 in phosphate buVered saline and stored at
−20 °C in the dark. The monoclonal antibody used (AFRC
MAC 252) is specific for (+)-ABA.
Hexoses, sucrose and starch were extracted from leaves and
roots and quantified following the methods of
Pearce et al.
Total RNA extraction, blotting and hybridization were
according to the methods described by
Thompson and Corlett (1995)
Origin of probes asr1 (previously named pNI3212), le20 and
lcyP2 was also described by
Thompson and Corlett (1995)
The lhcII probe was a 550 base pair HindII/PvuII fragment
from plasmid pTAB2.0
(Pichersky et al., 1985)
In the case of triplicate total RNA samples, a separate
blot was prepared for each set of replicates so that variation
between blots could be accounted for. Each blot also
contained two common samples to allow comparison between
blots. Hybridization signal was determined by use of a
PhosphorImager (Molecular Dynamics). Signal was quantified
by volume integration using ImageQuaNT v4.1 software, and
the background subtracted. Background was taken as the signal
from an equivalent area of the blot with no loaded RNA.
Absolute mRNA values (attomole mg−1 total RNA) were
calculated for le20 and lcyP2 by including on the blots samples
taken from a previous experiment
( Thompson and Corlett,
. Absolute values for lhcII and asr1 were not measured
and data were therefore expressed as a percentage of the
maximum signal. Adjustment of values for rRNA content was
unneccessary as visual inspection of methylene blue stained
blots showed little variation, and the variation in total RNA
loadings was in any case accounted for in the experimental
design by the use of triplicate sampling.
Gas exchange and chlorophyll fluorescence
CO2 assimilation and stomatal conductance ( gs) were measured
on six fully expanded, attached leaves (six diVerent plants and
generally leaf four or five) at each sampling time using an
infrared gas analyser (LCA3, ADC, Hoddesdon, UK ).
Chlorophyll fluorescence induction was followed on six similar
attached leaves on diVerent plants during a 3 s flash of
approximately 1500 mmol m−2 s−1 after 15 min dark adaptation
in standard leaf cuvettes (PEA, Hansatech, King’s Lynn, UK ).
Results and discussion
Environment, plant water status and ABA concentration
Air temperature was maintainted at 20.6±0.5°C
throughout the experiments and relative humidity varied by less
than 2%. The temperature of the hydroponic solution
varied between 22 °C at the end of 12 h darkness and
22.8 °C after 12 h light, rising to 23.6 °C after 48 h
continuous light. Because of the large total volume of circulating
solution, ion concentrations dropped only slowly during
the experiments accompanied by a slow increase in pH.
No alterations were made to the hydroponic solution
during the 24 h experiment and during the 96 h
experiment additions were made only once such that there was
no diurnal cycling of hydroponic composition in either
As plant roots were continuously bathed in hydroponic
solution it is reasonable to assume that root tissue
experienced minimal water deficit during the experiments.
Similarly one would expect leaf water deficits to be small
and leaf water potential to be higher than the −0.6 MPa
previously shown to induce the expression of le20 and
asr1 in tomatoes growing in drying soil
( Thompson and
Corlett, 1995 )
. No detectable changes in leaf thickness
were measured by the displacement transducers (data not
shown). Previous work on various species including
tomato has shown that both small and transient changes
in leaf water potential can be detected using the transducer
(Malone, 1992; Malone et al., 1994 )
concentrations were variable in both leaf and root tissue
but there was no evidence for a diurnal rhythm in either
the 24 h experiment (data not shown) or the 96 h
experiment ( Fig. 1). ABA concentrations were higher in leaves
than roots and within the ranges reported for
wellFig. 1. ABA concentration during two day/night cycles and 48 h
continuous light. Roots (+) leaves ($). Open symbols are single data
points, bars show standard error of mean for triplicate samples. Open
and filled boxes on the x-axis represent light and dark periods,
respectively, stippled boxes indicate where dark periods would have
fallen if the day–night cycle had continued.
hydrated tomato leaf and root tissue
Zeevaart, 1988; Cohen et al., 1991)
Trends in mRNA and sucrose levels
The 24 h experiment showed diVering diurnal patterns of
mRNA abundance for the genes lhcII, lcyP2 and le20 in
tomato leaves ( Fig. 2). While all showed highest levels in
the light, lhcII increased most rapidly at the start of the
light period and there was some evidence of both an
increase before the beginning of the light period and a
decrease before the beginning of the dark period. lcyP2
and le20 mRNA did not increase during the first 3 h of
the light period and while lcyP2 peaked after 7 h light,
le20 did not reach its maximum until the end of the light
period. In roots, similar diurnal trends were observed,
but there was more lcyP2 and le20 mRNA per mg total
RNA than in leaves ( Fig. 3).
From the results of the 24 h experiment, triplicate
sampling times were chosen in a 96 h experiment to
specifically follow le20 mRNA through two day/night
cycles and 48 h of continuous light ( Figs 4, 5 ). Expression
patterns for le20, lcyP2 and lhcII mRNA in leaves and
roots were broadly consistent with the previous
experiment during the two day/night cycles and during this
period there was no significant change in the mRNA
levels of asr1 (included as a possible negative control ).
Fig. 2. Leaf mRNA for three genes during a 12 h light/dark cycle. le20
(&); lcyp2 (+) and lhcII ($). Bars show standard errors of the means
for triplicate samples—where no bar is shown error is smaller than the
symbol. Data are expressed either as percentage maximum signal, or
attomoles mRNA per mg total RNA. Open and filled boxes on the
x-axis represent light and dark periods, respectively.
In continuous light le20, lcyP2 and lhcII all showed one
peak after 7–11 h and then declined rapidly, but there
was no evidence of a second peak 24 h later. There was
less asr1 mRNA in leaves than roots and unexpectedly
expression increased gradually and significantly through
the continuous light period in both leaves and roots ( Figs
3, 4). The increase in asr1 expression was not
accompanied by any significant increase in ABA concentrations
( Fig. 1). lhcII mRNA in roots was close to the limit of
detection (0.1% of maximum) for this assay and diYcult
to quantify (data not shown).
Genes encoding putative histone H1 were previously
reported to respond to ABA and water deficit
et al., 1993)
and to have a diurnal component in mRNA
expression in the leaves of tomato
( Thompson and
Corlett, 1995; Wei and O’Connell, 1996)
(Szekeres et al., 1995)
, but in each case diurnal changes
in water status or environmental conditions (e.g.
irradiance, temperature or humidity) may have been driving
the rhythm. It has been shown that le20 and lcyP2 mRNA
in leaves and roots varies in a diurnal manner
independently of temperature, humidity, plant water status or bulk
tissue ABA concentration. The presence of a diurnal
rhythm of gene expression in the roots was unexpected
and as the roots were kept under relatively constant
conditions throughout the experiment this suggests
control by a signal transported from the shoot, although the
transmission of a very low level of light into the root
chambers cannot be discounted as a signal.
The fact that le20 and lcyP2 mRNA showed only
one cycle in 48 h of constant light implies that their
expression does not have a circadian component. However,
mRNA for lhcII, a gene with known circadian control
( Kellman et al., 1993)
, did not exhibit multiple cycles in
this experimental system either. Circadian rhythms in gene
expression are known to be damped out rapidly in
, but most studies
of circadian expression have utilized continuous light of
(e.g. 135 mmol PAR m−2 s−1; Anderson
et al., 1994 )
. Continuing rhythms have been seen under
higher continuous irradiances
(e.g. 76 W m−2#380 mmol
PAR m−2 s−1; Piechulla, 1989 )
while the irradiance used
in our experiments was 500 mmol PAR m−2 s−1 ( 20% of
full sunlight). Circadian rhythms in variables other than
gene expression have been found to disappear rapidly
under constant ‘high’ irradiance
(Mansfield and Snaith,
. Hennessey et al. (1993 ) reported circadian rhythms
with almost constant amplitude for carbon assimilation
and stomatal conductance in Phaseolus vulgaris under
constant irradiances of 100 or 200 mmol m−2 s−1 while at
500 mmol m−2 s−1 the rhythms were gradually damped,
but still exhibited three distinct peaks. These authors
measured large increases in starch and sucrose
concentration in leaves during constant high light and concluded
that the decrease in amplitude of rhythms was due to
feed-back inhibition of photosynthesis by carbohydrate
In the 96 h experiment hexose concentrations showed
no significant trends, however, there were significant
increases in sucrose concentrations in both root and leaf
tissue ( Fig. 6) and in leaf starch content (data not shown)
during the period of constant illumination. It is possible,
then, that there was feed-back repression of transcription
of photosynthetic genes such as lhcII.
maize mesophyll protoplasts and a GUS reporter system,
found that the transcriptional activity of seven
photosynthetic gene promoters (including cab2m1 and cab2m5)
was repressed by glucose, fructose and sucrose. This
metabolite repression over-rode other forms of regulation
such as by light or tissue type. Van-Oosten and Besford
(1994 ) found in tomato that exposure to high CO2
concentrations caused down-regulation in the leaf of the
nuclear gene family encoding the ribulose-bisphosphate
carboxylase small subunit. This eVect could be mimicked
by feeding sucrose or glucose to detached leaves, and
carbohydrate analysis indicated glucose and fructose
accumulation under high CO2 conditions
et al., 1994 )
. The response of asr1 to sugar levels has not
been tested, but increased tissue sucrose observed in the
current experiment during constant light may have
contributed to the increase in asr1 mRNA as well as
repressing circadian rhythms in lhcII.
Photosynthetic rates were high during the light periods
with no detectable trends despite the tendency of stomata
to close in anticipation of the dark period ( Fig. 7). During
48 h of continuous light, assimilation remained high with
only minor fluctuations while conductance peaked after
5 h and then dropped considerably to reach a minimum
13 h into the light period. A small and transient second
peak in conductance occurred 26 h after the first peak in
continuous light. The eYciency of photosystem II (PSII )
after 15 min dark adaptation as indicated by Fv/Fm was
high throughout the experiment with small but significant
diurnal trends during the day/night cycles ( Fig. 8). The
drop in Fv/Fm at the beginning of the light period was
due to a rapid increase in Fo and a slower decrease in Fv.
In continuous light, Fv/Fm dropped to a minimum after
7 h, increased significantly over the next 10 h and reached
a second minimum 13 h later. The fluctuations of Fv/Fm
in continuous light were the result of changes in Fv rather
than Fo. However, Fo did rise quite rapidly during the
last 12 h of the experiment which may indicate some
The negligible variation in photosynthesis during
constant light despite the changes in stomatal conductance
and PSII eYciency suggests that photosynthesis was not
Fig. 8. vRh(&yt)h.mPsoiinntschaloreropmheyalnlsfluoofre6scmenecaesuvraermiaebnltess.aFnd/Fbmar(s$s)h:oFwo
(+); F v
standard error. Open and filled boxes on the x-axis represent light and
dark periods, respectively, stippled boxes indicate where dark periods
would have fallen if the day–night cycle had continued.
limited by either irradiance or CO2 uptake, nor was it
inhibited by the increases in leaf sucrose concentration
or changes in gene expression. In Phaseolus vulgaris
Hennessey et al. (1993)
reported cycles in carbon
assimilation and concluded that this was due to cycles in PSII
activity rather than stomatal conductance or dark
( Freeden et al., 1991 )
. Although cycling of PSII
eYciency was detected, this did not aVect net CO2 uptake
and the period of the rhythm that was observed in
constant light was less than 15 h suggesting that control
was not circadian, but rather through metabolic feedback.
The time-scale of fluctuations in Fv suggests that
depression of PSII eYciency was due to increases in slowly
relaxing components of non-photochemical quenching
( Demming and Winter, 1988) that could be reversed in a
few hours. Depressions in eYciency due to
photoinhibitory damage would have taken longer to disappear.
It may be assumed too often that, if a variable (such
as mRNA concentration, stomatal conductance or carbon
assimilation) does not show a 24 h cycle under constant
conditions then there is no circadian component in the
control of that variable. Because, in reality, many
interlinked pathways containing many control points will
combine to control the size of a particular variable, a
circadian rhythm will only be observed if the prevailing
conditions (environmental and physiological ) cause the
control point acted upon by the oscillator to become rate
limiting for that variable. It could be postulated for a
particular variable that the wider the range of constant
conditions under which a circadian rhythm is maintained,
the more critical is the control point acted upon by the
oscillator and/or the smaller the biochemical/biophysical
‘distance’ between the action of the oscillator and the
‘expression’ of that variable.
Although previous reports have regarded le20 as a
( Kahn et al., 1993 )
, it was found
that le20 was diurnally regulated independently of plant
water status or bulk tissue ABA concentration, implying
that le20 has a role in unstressed plants, and that there
is benefit to the plant if its expression fluctuates with the
daily light–dark cycle. The increased mRNA level under
drought stress may reflect an enhanced requirement for
the same function under stress and day/night cycles, or a
dual function of the gene product. However, it is not
known whether changes in mRNA are reflected in protein
abundance or activity (in mammalian cells the binding
activity of histone H1 may be regulated by
phosphorylation or partitioning of a protein pool between cytoplasm
and nucleus; Zlatanova and Van Holde, 1992) or if
expression of the gene is a positive adaptation or simply
a secondary consequence of stress. Manipulation of
expression in transgenic plants could allow the relevance
of le20 to plant performance under stress to be
determined. The strong diurnal rhythms in both root and leaf
mRNA for a gene (le20 ) previously thought to be
predominantly regulated by drought and ABA underlines
the importance of taking into account time-of-day and
environmental eVects when designing and interpreting
experiments to study gene expression.
We thank Steve Quarrie, Institute of Plant Science Research,
Norwich, UK. for the gift of MAC 252 antibody, Birgit
Piechulla, Institut fur Biochemie der Pflanze, Gottingen, FRG
for plasmid pTAB2.0, and Mike Malone, Wellesbourne for
performing leaf thickness measurements. We also thank James
Lynn for statistical advice and Brian Thomas for helpful
comments on the manuscript. This work was funded by
Anderson SL , Teakle GR , Martino-Catt SJ , Kay SA . 1994 . Circadian clock- and phytochrome-regulated transcription is conferred by a 78 bp cis-acting domain of the Arabidopsis CAB2 promoter . The Plant Journal 6 , 457 - 70 .
Ascenzi R , Gantt JS . 1997 . A drought-stress-inducible histone gene in Arabidopsis thaliana is a member of a distinct class of plant linker histone variants . Plant Molecular Biology 34 , 629 - 41 .
Bouvet P , Dimitrov S , WolVe AP . 1994 . Specific regulation of Xenopus chromosomal 5S rRNA gene transcription in vivo by histone H1 . Genes and Development 8 , 1147 - 59 .
Cohen A , Bray EA . 1990 . Characterization of three mRNAs that accumulate in wilted tomato leaves in response to elevated levels of endogenous abscisic acid . Planta 182 , 27 - 33 .
Cohen A , Plant AL , Moses MS , Bray EA . 1991 . Organ-specific and environmentally regulated expression of two abscisic acid-induced genes of tomato . Plant Physiology 97 , 1367 - 74 .
Cornish K , Zeevaart JAD . 1988 . Phenotypic expression of wildtype tomato and three wilty mutants in relation to abscisic acid accumulation in roots and leaflets of reciprocal grafts . Plant Physiology 87 , 190 - 4 .
Demming B , Winter K. 1988 . Characteristics of three components of non-photochemical quenching and their response to photoinhibition . Australian Journal of Plant Physiology 15 , 163 - 77 .
Freeden AL , Hennessey TL , Field CB . 1991 . Biochemical correlates of the circadian rhythm in photosynthesis in Phaseolus vulgaris . Plant Physiology 97 , 415 - 19 .
Hennessey TL , Freeden AL , Field CB . 1993 . Environmental eVects on circadian rhythms in photosynthesis and stomatal opening . Planta 189 , 369 - 76 .
Jones JT , Mullet JE . 1995 . A salt- and dehydration-inducible pea gene, Cyp15a, encodes a cell-wall protein with sequence similarity to cysteine proteases . Plant Molecular Biology 28 , 1055 - 65 .
Kahn TL , Fender SE , Bray EA , O'Connell MA. 1993 . Characterization of expression of drought- and abscisic acidregulated tomato genes in the drought-resistant species Lycopersicon pennellii . Plant Physiology 103 , 597 - 605 .
Kellmann JW , Merforth N , Wiese M , Pichersky E , Piechulla B. 1993 . Concerted circadian transcript level oscillations of nineteen Lhca/b (cab) genes in Lycopersicon esculentum (tomato) . Molecular and General Genetics 237 , 439 - 48 .
Linthorst HJM , van der Does C , Brederode F , Bol JF . 1993 . Circadian expression and induction by wounding of tobacco genes for cysteine proteinase . Plant Molecular Biology 21 , 685 - 94 .
Malone M. 1992 . Kinetics of wound-induced hydraulic signals and variation potentials in wheat seedlings . Planta 187 , 505 - 10 .
Malone M , Palumbo L , Boari F , Monteleon M , Jones HG . 1994 . The relationship betweeen wound-induced proteinase inhibitors and hydraulic signals in tomato seedlings . Plant, Cell and Enivronment 17 , 81 - 7 .
Mansfield TA , Snaith PJ . 1984 . Circadian rhythms . In: Wilkins MB, ed. Advanced plant physiology . London: Pitman, 201 - 18 .
van Oosten JJ , Besford RT . 1994 . Sugar feeding mimics eVect of acclimation to high CO2-rapid down regulation of RuBisCo small subunit transcripts, but not of the large subunit transcripts . Journal of Plant Physiology 143 , 306 - 312 .
van Oosten JJ , Wilkins D , Besford RT . 1994 . Regulation of the expression of photosynthetic nuclear genes by CO2 is mimicked by regulation by carbohydrates: a mechanism for the acclimation of photosynthesis to high CO2? Plant , Cell and Environment 17 , 913 - 23 .
Paranjape SM , Kamakaka RT , Kadonaga JT . 1994 . Role of chromatin structure in the regulation of transcription by RNA polymerase II . Annual Review of Biochemistry 63 , 265 - 97 .
Pearce B , Brown M , Grange B. 1992 . A method for assessing diurnal changes in concentrations of sugars and malate in the pericarp of growing tomato fruit . Journal of Horticultural Science 67 , 231 - 7 .
Pichersky E , Bernatzky R , Tanksley SD , Breidenbach RB , Kausch AP , Cashmore AR . 1985 . Molecular characterization and genetic-mapping of 2 clusters of genes encoding chlorophyll a/b-binding proteins in Lycopersicon esculentum (tomato) . Gene 40 , 247 - 58 .
Piechulla B. 1989 . Changes of the diurnal and circadian (endogenous) mRNA oscillations of the chlorophyll a/b binding protein in tomato leaves during altered day/night ( light/dark) regimes . Plant Molecular Biology 12 , 317 - 27 .
Piechulla B. 1993 . ' Circadian clock' directs the expression of plant genes . Plant Molecular Biology 22 , 533 - 42 .
Quarrie SA , Whitford PN , Appleford NEJ , Wang TL , Cook SK , Henson IE , Loveys BR . 1988 . A monoclonal antibody to (S )- abscisic acid: its characterisation and use in radioimmunoassay for measuring abscisic acid in crude extracts of cereals and lupin leaves . Planta 173 , 330 - 9 .
Rossi M , Iusem ND . 1994 . Tomato (Lycopersicon esculentum) genomic clone homologous to a gene encoding an abscisic acid-induced protein . Plant Physiology 104 , 1073 - 4 .
Sheen J. 1990 . Metabolite repression of transcription in higher plants . The Plant Cell 2 , 1027 - 38 .
Shen X , Gorovsky MA . 1996 . Linker histone H1 regulates specific gene expression but not global transcription in vivo . Cell 86 , 475 - 83 .
Szekeres M , Haizel T , Adam E , Nagy F. 1995 . Molecular characterization and expression of a tobacco H1 cDNA . Plant Molecular Biology 27 , 597 - 605 .
Thompson AJ , Corlett JE . 1995 . mRNA levels of four tomato (Lycopersicon esculentum Mill . L.) genes related to fluctuating plant and soil water status . Plant, Cell and Environment 18 , 773 - 80 .
Wei T , O'Connell MA. 1996 . Structure and characterization of a putative drought-induced H1 histone gene . Plant Molecular Biology 30 , 255 - 68 .
Workman JL , Buckman AR . 1993 . Multiple functions of nucleosomes and regulatory factors in transcription . Trends in Biochemical Science 18 , 90 - 5 .
Zlatanova J , Van Holde K. 1992 . Histone H1 and transcription: still an enigma? Journal of Cell Science 103 , 889 - 95 .