Plant, Cell & Environment
Volume 21 Page 63 - January 1998
doi:10.1046/j.1365-3040.1998.00240.x
Volume 21 Issue 1
UV-B induction of NADP-malic enzyme in etiolated and green maize seedlings
M. F. Drincovich, P. Casati, C. S. Andreo, R. Donahue & G. E. Edwards
The effect of treatment of etiolated maize seedlings with UV-B and UV-A radiation, and different levels of photosynthetic
400–700 nm), on the activity and quantity of NADP-malic enzyme (NADP-ME) and on RNA levels was determined. Und
μmol m 2 s 1), exposure to UV-B radiation (9 μmol m 2 s 1) but not UV-A radiation (11 μmol m 2 s 1) for 6–24 h cause
activity of the enzyme similar to that observed under high PAR (300 μmol m 2 s 1) in the absence of UV-B. Western blo
was a specific increase of the photosynthetically active isoform of the enzyme. This increase was also measured at the
analysis, indicating that the induction is displayed at the level of NADP-ME transcription. UV-B treatment of green leave
also caused an increase in the activity and level of NADP-ME. The UV-B induction of NADP-ME synthesis may reflect a
of photosynthetic processes in C4 photosynthesis. Alternatively, the relatively low intensity of UV-B radiation present und
provide a signal that facilitates repair of UV-B-induced damage through the increased activity of different enzymes such
speculated that the reducing power and pyruvate generated by activity of NADP-ME may be used for respiration in cellu
as substrates for the fatty acid synthesis required for membrane repair.
INTRODUCTION
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Light is essential for normal plant growth and development, not only as a source of energy but also as a stimulus that regulate
metabolic processes through the induction of gene expression. Plant responses to the light environment are mediated by gene
by three major classes of photoreceptors: the phytochrome family, ultraviolet-A (UV-A)/blue-light (cryptochrome) receptors and
Smith 1994). Light-regulated genes respond to one or more of these photoreceptors via different signal transduction pathways
tempered by other environmental factors or developmental stages of the plants (Thompson & White 1991; von Arnim & Deng
The molecular structure of the phytochrome chromophore has been determined (Rüdiger & Thümmler 1994) and phytochrome
response to light conditions has been widely investigated (Quail 1994). In contrast, the structure and biochemical nature of the
has only recently been described, while the mechanism of UV-B photoreception has not been clarified (Terzaghi & Cashmore
the spectrum of ultraviolet radiation is generally divided into three parts: UV-C, UV-B and UV-A. Ultraviolet-C (wavelengths ≤ 2
extremely damaging to biological systems; because it is strongly absorbed by oxygen and ozone in the stratosphere, there is n
sunlight. Ultraviolet-B (280–320 nm) is also potentially harmful and is strongly absorbed by ozone in the atmosphere. As the tr
through the atmosphere is a function of ozone concentration, terrestrial levels of UV-B are increasing as stratospheric ozone i
Teramura & Tevini 1989; Teramura & Sullivan 1994). Ultraviolet-A (320–400 nm) is not attenuated by atmospheric ozone, is le
important photomorphogenic signal in plant development (Bjorn 1994).
The effect of UV-B radiation on plant growth and photosynthesis has been widely investigated but the extent of damage to agr
clear (Fiscus & Booker 1995). The amount of damage induced by UV-B is dependent on the plant material tested, the UV-B d
white light, which facilitates repair of the induced damage through photoreactivation and use of the reducing power provided b
radiation has been reported to reduce photosynthetic capacity by damaging photosystem II (PSII) and vital components of the
this damage can be repaired by de novo enzyme biosynthesis and PSII turnover (Jordan et al. 1992; Strid, Chow & Anderson
formation of cyclo-butyl pyrimidine dimers in DNA; these are normally repaired by photoreactivation in the presence of UV-A a
plants caused by UV-B can be alleviated or avoided by gene expression that induces biosynthetic pathways that help prevent
suggested that the activation of signalling pathways for defence genes by exposure to ultraviolet light is mediated by the octad
(Conconi et al. 1996). For the phenylpropanoid pathway, which produces ultraviolet-screening flavonoids and other secondary
chalcone synthase isomerase and phenylalanine ammonia lyase are induced by UV-B irradiation and other stresses such as t
temperatures (Thompson & White 1991). There is evidence that flavonoids accumulate in the epidermal tissue of plants and re
radiation because of their absorption of UV-B (Cen & Bornman 1990).
Inspection of the NADP-ME gene of a bean (Phaseolus vulgaris L.) (Walter, Grima-Pettenati & Feuillet 1994) showed a motif t
sequence responsible for the induction of genes by UV-B radiation and fungal-elicitor-induced genes of the phenylpropanoid p
Moreover, the examination of the promoter region for this gene (Schaaf, Walter & Hess 1995) showed that it responds to diffe
defence against different elicitors. It has not been determined whether or not UV-B radiation affects induction of NADP-ME, an
help plants tolerate or respond to UV-B radiation. However, NADP-ME levels from wheat were reported to increase after treatm
macerozyme, enzymes that degrade the cell-wall (Casati, Spampinato & Andreo 1997). In this way, NADP-ME from bean and
lignin biosynthesis by providing NADPH for the two NADP-dependent reductive steps in monolignol biosynthesis (Walter et al.
In the present paper we report an investigation in which we used artificial light sources to determine the effect of UV-A and UV
activity of NADP-malic enzyme. NADP-malic enzyme occurs in C3 and C4 plants and catalyses the decarboxylation of L-malat
C4 plants, such as maize, the enzyme is implicated in the photosynthetic process, yielding CO 2 to be fixed in bundle-sheath ch
(Edwards & Andreo 1992). There are at least two different isoforms of the enzyme in maize tissues, both of which are located
1997). The isoform implicated in the C4 cycle is induced by white light, while the constitutive form of the enzyme, which is the m
remains almost constant upon illumination with PAR (Maurino, Drincovich & Andreo 1996). It is also known that this white-ligh
transcription level (Collins & Hague 1983; Maurino et al. 1996). In the present paper we report that for etiolated and green mai
isoform of NADP-ME increases in content and activity, as well as in amounts of steady-state RNA, after treatment with environ
radiation in the presence of low PAR, in a manner similar to the induction of NADP-malic enzyme by high PAR.
MATERIALS AND
METHODS
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Plant material
Maize (Zea mays L.) lines with normal (wt) and deficient (224H) chalcone synthase activity —C2Whp1 and c2whp1 genotypes
from the Maize Genetics Cooperative Stock Centre, USDA, Urbana, IL, USA. Etiolated seedlings were grown in complete dark
maize and the 224H mutant deficient in flavonoids were used in the different experiments described below. In the case of gree
grown at 25°C for 15 d under a 12 h light/12 h dark photoperiod with 300 μmol m 2 s 1 white light (PAR) from metal halide lam
Belgium).
Plant treatments
Leaves on intact etiolated and green maize seedlings were exposed to different light conditions as described below. In each c
plant was positioned horizontally to the light source and the fluence rates of PAR (400–700 nm), UV-A (320–400 nm) and UVleaf surface were measured at the beginning and end of each experiment. For experiments using high levels of white light (PA
illumination was provided by the same light source as that used to grow green seedlings. Low-level white light (14 μmol m 2 s
fluorescent lamps (40 W Phillips). Ultraviolet radiation was supplied by ultraviolet lamps (UVB-313, Q-Panel, Cleveland, OH, U
mm cellulose acetate to remove all wavelengths < 280 nm for the UV-B treatment, and 0·127 mm sheets of polyester to remov
the UV-A treatment. Table 1 shows the time of exposure and the amount of PAR, UV-A and UV-B in μmol photons m 2 s 1 us
different samples. PAR was measured with a quantum sensor and light meter (Li-189, Licor Inc., Lincoln, NB, USA) and ultrav
with UV-B and UV-A sensors (SUV and UVA, Ultraviolet Meter Model 3D, Solar Light Co., Philadelphia, PA, USA). The ultravi
calibrated for the different light sources with a spectroradiometer (Optronics 754, Optronics Inc, Orlando, FL, USA). For the pr
treatments are presented as μmol photons m 2 s 1. For comparison, the peak solar UV-B irradiance measured at Pullman, W
5·3 μmol photons m 2 s 1, and we consider the UV-B treatment used in this investigation, 9 μmol photons m 2 s 1, to be a ph
Protein extraction
For enzyme activity assays, total soluble protein from the cut leaves was extracted with a buffer containing: 0·1 kmol m 3 Tris
mol m 3 EDTA, 10 mol m 3 2-mercaptoethanol, 10 mmol m 3 leupeptin, 1 mol m 3 PMSF, and 20% (v/v) glycerol. The sampl
were ground in a mortar using liquid nitrogen and centrifuged at 10 000 r.p.m. for 10 min. The supernatant was desalted in a S
equilibrated with Tris-HCl, 50 mol m 3 pH 8·0, according to Penefsky (1977) before the activity measurement.
For Western blot analysis, total soluble protein from the cut leaves was extracted immediately after the light treatment (extract
pH 7·5, 0·1 kmol m 3 KCl, 0·7 kmol m 3 sucrose, 50 mol m 3 EDTA, 2% mercaptoethanol, 10 mmol m 3 leupeptin, 1 mol m
(1 cm3 buffer/0·5 g tissue) were extracted in a mortar using liquid nitrogen and centrifuged at 10 000 r.p.m. for 10 min. Total so
measured using the Sedmak & Grossberg (1977) method.
Activity measurement
NADP-ME activity was determined spectrophotometrically at 30°C by following NADPH production by measuring the absorban
spectrophotometer (DW-2, Aminco Inc., Urbana, IL, USA). The standard assay medium contained 50 mol m 3 Tris-HCl, pH 8·
NADP, and 4 mol m 3L-malate in a final volume of 1 cm3.
SDS-polyacrylamide gel electrophoresis and Western blot
SDS-polyacrylamide gel electrophoresis (PAGE) was carried out using gradient acrylamide gels (7·5–15%). All samples were
SDS and 0·5% 2-mercaptoethanol for 2 min at 100 °C before being loaded onto the gel. Gels were stained with Coomasie bril
nitrocellulose membrane for Western blot analysis using an antibody raised and purified against the 62 kD subunit of malic en
(photosynthetic form) (Maurino et al. 1996). Bound antibodies were visualized by linking to alkaline phosphatase-conjugated g
Measurement of leaf mRNAs
Steady-state levels of malic enzyme mRNA were measured by hybridization with a cloned cDNA of the 3' end of the enzyme (
RNA samples (Rothermel & Nelson 1989). Total RNA from leaves was prepared according to Wadsworth, Redinbaugh & Sca
containing 30 μg of RNA were denatured and blotted to Hybond-N according to the manufacter's suggestions (Amersham, Am
cDNA fragment was labelled by random priming with [32P]dATP (Promega, Madison, Wisconsin, USA). Hybridizations were ca
manufacturer's instructions (Amersham). Stringent washes of the membranes were made at 65 °C.
RESULTS
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Etiolated maize seedlings were exposed to different light conditions (Table 1), and the third leaf of each plant was excised for
NADP-ME was measured by enzyme activity assays, Western blot analysis of protein extracts using an antibody for maize 62
analysis of RNA samples using a specific probe of the cloned cDNA. All the assays were performed in triplicate in samples ob
experiments conducted with different maize seedlings. The different light treatments as indicated in Table 1 correspond to sam
NADP-ME activity of etiolated maize seedlings was markedly increased above constitutive levels after exposure to high levels
white light supplemented with UV-B radiation (Fig. 1). Treatment with UV-B radiation increased activity by 50% or more relativ
low levels of white light, while supplementary UV-A radiation caused no measurable increase in activity (Fig. 1). The low spec
soluble protein) measured in extracts from etiolated plants (sample 1) can be attributed to the expression of the constitutive is
of the photosynthetic isoform in etiolated maize tissue, or both (Maurino et al. 1996).
In this way, after 6 h of illumination with low PAR intensity (sample 4), the specific activity increased 1·7 times relative to value
hand, after treatment with high PAR and low PAR plus UV-B light, the specific activity increased about 2·6 times relative to tha
8; Fig. 1).
NADP-ME activity also increased with time of light exposure. Low PAR intensity for 24 h (sample 5) increased the enzyme act
etiolated tissue, even though activity never reached the levels attained for treatment with either high PAR intensity (8·1 times)
UV-B (7 times) (sample 10). The enzyme activity in etiolated leaves exposed to low light levels was not increased by suppleme
7 versus 4 & 5).
To determine whether these results were attributable to an increased quantity of the protein, Western blot analyses of the sam
antibody raised and purified against the photosynthetic isozyme of NADP-ME (Maurino et al. 1996). Figure 2 shows a typical r
Expression of the photosynthetic isoform of NADP-ME is low in etiolated tissue (sample 1) and leaves illuminated with low ligh
(sample 6) for 6 h (Fig. 2a). High levels of induction of the synthesis of this protein are clearly shown after illumination with hig
+ UV-B (samples 8, 9, 10). Induction of the appearance of NADP-ME by low light increased with time (sample 5), although to a
high PAR (sample 3) or low PAR + UV-B (sample 10) (Fig. 2a). Western blot analyses performed with higher loadings of total
that the constitutive non-photosynthetic isoform of NADP-ME (72 kDa) was also evident (Maurino et al. 1996). However, the le
isoform of NADP-ME was not affected by the light treatments used. General visual inspection of gels stained with Coomassie
amount of protein was loaded in each lane. The apparent absence of change in some protein bands indicates selectivity in the
Densitometric analyses were performed on Western blots (a typical result is shown in Fig. 2) to compare the intensity of bands
shows an average of the densitometric areas of the Western blots for the different light treatments tested. The results clearly s
was induced by light in a way that is dependent on both the quantity and quality of light. Seedlings exposed to high light for 6 h
protein as those exposed to low light (sample 4) and low light in the presence of UV-A (sample 6). Low light supplemented wit
resulted in NADP-ME levels comparable to that reached under high light exposure for the same time. The amount of NADP-M
and the higher amount of protein is found after 24 h of treatment with high PAR (sample 3) and low PAR in the presence of UV
To determine whether the levels of NADP-ME RNA were also changing with the different treatments, dot blots of total RNA we
of the NADP-ME messenger were found in etiolated leaves. After 3 h of treatment with UV-B radiation the level of RNA marke
maximum between 6 h and 12 h of UV-B treatment. Nevertheless, after 6 h of treatment with low PAR, the level of RNA was a
induced the level of NADP-ME RNA in a similar manner to UV-B. Thus, the amount of RNA correlates with the increase in pro
Western blot analyses were also performed on etiolated maize seedlings defective in flavonoids (mutant 224H). The same ind
quality and quantity was obtained for mutant 224H and wild-type maize (data not shown). These results suggest that flavonoid
the maize seedlings did not affect NADP-ME induction in response to ultraviolet radiation.
Experiments were also performed on normal green maize seedlings, similar to those undertaken on etiolated seedlings (Fig. 5
exposed to the different light treatments indicated in Table 1 after a 12 h dark period. As already seen with etiolated tissue, NA
tissue as a function of light quality, quantity and time of exposure (Fig. 5a). There was a significant increase in activity after on
UV-B radiation (sample 8), or high light without UV-B radiation (sample 2). Only a slight increase in activity was measured afte
or without supplemental UV-A radiation (samples 7 & 5). Green seedlings treated with 24 h of low light + UV-B radiation, follow
increase in NADP-ME activity (sample 10). The Western blot studies performed with these light-grown seedlings show high NA
treatment is lower than the 24h UV-B treatment (samples 7 and 10, Fig. 5b).
To test the effect of UV-B fluence on NADP-ME content, etiolated maize seedlings were irradiated with different amounts of U
1) for up to 32 h. Figure 6 shows NADP-ME specific activity as a function of the time of exposure to the different light regimens
initial rate of increase in activity or the final activity measured. The level of the enzyme after the three UV-B radiation treatmen
treatment with high light, but considerably higher than that after low-light treatment without UV-B radiation.
DISCUSSION
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NADP-ME was induced by UV-B radiation to almost the same extent as by high levels of white light. Thus, induction of synthe
by both white light and UV-B radiation, light intensity, and the duration of the light treatment. The increase in the steady-state l
attributable to a high rate of transcription or a higher stability of the synthesized RNA, or both. Further experiments will be requ
radiation and white light induce synthesis of NADP-ME through controlling gene expression via different cis-acting elements o
transduction pathways to act on the same element or, alternatively, through some kind of post-transcriptional process.
The induction profile observed in the present study with the Western blot analyses, after treatment of maize seedlings with ultr
parallels the results obtained for the specific activity measurements for NADP-ME. However, the magnitude of the increase in
than that in enzyme protein, monitored by Western blotting. This difference might be attributed to the non-linear nature of the W
intensity of the bands measured with the densitometric method is not completely linear with the amount of protein loaded; Mau
underestimate the actual increase in protein. Alternatively, the greater response in activity could occur by light causing some a
to the observed increase in protein content. NADP-ME RNA levels increase in the same way as the amount of protein, indicati
transcriptional events, or both, are involved in the process of induction of the enzyme.
As noted in the introduction, multiple photoreceptors regulate the expression of certain genes. One wavelength region can affe
enzymes (Bjorn 1994), for example, the induction by UV-B radiation (280–320 nm) of a group of enzymes involved in flavonoid
only ultraviolet radiation can induce the flavonoid pathway and red or far-red light alone has no inductive effect. However, afte
magnitude of the response can be affected by phytochrome action (Wellman 1971). Later work showed that both phytochrome
interact in the response induced by ultraviolet radiation (Duell-Pfaff & Wellman 1982). In general, the synthesis of flavonoids a
UV-B exposure in various species (Beggs, Stolzer-Jehler & Wellman 1985; Kubaseck et al. 1992). Both pigments absorb UV-B
accumulate in the epidermis, where they can filter out UV-B radiation and prevent it from reaching photosynthetic tissues. The
induction of phenylalanine ammonia-lyase (PAL), an enzyme that participates in flavonoid biosynthesis, is unclear. It has been
Fastami 1982) that phytochrome is the sole photoreceptor involved in PAL induction, although the data do not completely rule
as well as in Arabidopsis, both ultraviolet radiation and phytochrome sensitivity have been demonstrated for hypocotyl photom
Dickinson 1979; Young, Liscum & Hangarter 1992).
It is interesting to find that both UV-B radiation and high levels of white light induce formation of the photosynthetically active is
etiolated and green tissue of maize. The effect of UV-B radiation on the level of NADP-ME in C4 plants, like maize, may be imp
increased levels of NADP-ME could provide plants with more reductive power for cellular repair, as well as increased pyruvate
substrate for lipid synthesis and membrane repair. The relatively low intensity of UV-B present in full sunlight might provide an
facilitate repair of UV-B induced damage through the increased activity of different enzymes, including NADP-ME. The 20–30%
green tissue also indicates a potential role for UV-B radiation in upregulation of key enzymes for C4 photosynthesis. Increased
to UV-B radiation could enhance maximum carbon assimilation in high light conditions, which in nature are typically accompan
radiation. The potential effect on photosynthetic capacity of increased levels of activity of NADP-ME, and possibly other photo
UV-B radiation needs to be evaluated.
Acknowledgements
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This work was funded in part by grants from the Environmental Protection Agency (Grant R 822346-01-0 to G.E.E.) and the C
Investigaciones Bioquímicas y Técnicas (CONICET), and from the Fundacion Antorchas to C.S.A. We thank Dr T. Nelson (Ya
the cDNA clone for the maize NADP-ME. P.C. is a fellow from CONICET and M.F.D. and C.S.A. are members of the Researc
Institution.
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630
Footnotes
Present address: Department of Biological Sciences, Idaho State University, Pocatello, ID 83209–8007, USA.
Plant, Cell & Environment
Volume 21 Page 63 - January 1998