Diurnal control of the drought-inducible putative histone H1 gene in tomato (Lycopersicon esculentum Mill. L.)

Journal of Experimental Botany, Jun 1998

The mRNA of genes le20, lcyP2, lhcll, 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 lhcll 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 lhcll 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 lhcll 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.

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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 Wellesbourne 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 Introduction 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 function. 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 Nicotiana tabacum ( Wei and O’Connell, 1996) and in Arabidopsis thaliana (Ascenzi and Gantt, 1997) . Histone 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 (Shen 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 deficit ( 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 ) and tobacco (Szekeres et al., 1995 ) , but 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 constitutively high ( Kahn et al, 1993; Wei and O’Connell, 1996 ) , 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 cellwall (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 increasing ( 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 regulated. 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 expression (lcyP2; Linthorst et al. 1993a; lhcII; Pichersky et al., 1985 ) and a gene expected to have no diurnal pattern (asr1; Rossi and Iusem, 1994; Thompson and Corlett, 1995 ) . 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. Sampling 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 (Malone, 1992) . 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 otherwise sampled. ABA determination 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. (1988) . [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. Sugar analysis Hexoses, sucrose and starch were extracted from leaves and roots and quantified following the methods of Pearce et al. (1992) . mRNA quantification 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, 1995) . 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 experiment. 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 technique (Malone, 1992; Malone et al., 1994 ) . ABA 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 ($). Open symbols are single data points, bars show standard error of mean for triplicate samples. Open and filled boxes on the x-axis represent light and dark periods, respectively, stippled boxes indicate where dark periods would have fallen if the day–night cycle had continued. hydrated tomato leaf and root tissue (Cornish and Zeevaart, 1988; Cohen et al., 1991) . Trends in mRNA and sucrose levels The 24 h experiment showed diVering diurnal patterns of mRNA abundance for the genes lhcII, lcyP2 and le20 in tomato leaves ( Fig. 2). While all showed highest levels in the light, lhcII increased most rapidly at the start of the light period and there was some evidence of both an increase before the beginning of the light period and a decrease before the beginning of the dark period. lcyP2 and le20 mRNA did not increase during the first 3 h of the light period and while lcyP2 peaked after 7 h light, le20 did not reach its maximum until the end of the light period. In roots, similar diurnal trends were observed, but there was more lcyP2 and le20 mRNA per mg total RNA than in leaves ( Fig. 3). From the results of the 24 h experiment, triplicate sampling times were chosen in a 96 h experiment to specifically follow le20 mRNA through two day/night cycles and 48 h of continuous light ( Figs 4, 5 ). Expression patterns for le20, lcyP2 and lhcII mRNA in leaves and roots were broadly consistent with the previous experiment during the two day/night cycles and during this period there was no significant change in the mRNA levels of asr1 (included as a possible negative control ). Fig. 2. Leaf mRNA for three genes during a 12 h light/dark cycle. le20 (&); lcyp2 (+) and lhcII ($). 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 ( Kahn 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) and tobacco (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 continuous darkness (Piechulla, 1993) , but most studies of circadian expression have utilized continuous light of low irradiance (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, 1984 ) . 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 accumulation. 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. Sheen (1990) , using 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 (van-Oosten 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. Physiological variables 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 cumulative damage. 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 reactions ( 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. Concluding remarks Although previous reports have regarded le20 as a ‘drought-induced’ gene ( 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. Acknowledgements 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 the BBSRC. Anderson SL , Teakle GR , Martino-Catt SJ , Kay SA . 1994 . 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Janet E. Corlett, Sally Wilkinson, Andrew J. Thompson. Diurnal control of the drought-inducible putative histone H1 gene in tomato (Lycopersicon esculentum Mill. L.), Journal of Experimental Botany, 1998, 945-952, DOI: 10.1093/jxb/49.323.945