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Plant Physiol. (1998) 117: 217-224 Two Structurally Similar Maize Cytosolic Superoxide Dismutase Genes, Sod4 and Sod4A, Respond Differentially to Abscisic Acid and High Osmoticum1
Department of Genetics, Box 7614, North Carolina State University, Raleigh, North Carolina 27695-7614
The maize (Zea mays) superoxide dismutase genes Sod4 and Sod4A are highly similar in structure but each responds differentially to environmental signals. We examined the effects of the hormone abscisic acid (ABA) on the developmental response of Sod4 and Sod4A. Although both Sod4 and Sod4A transcripts accumulate during late embryogenesis, only Sod4 is up-regulated by ABA and osmotic stress. Accumulation of Sod4 transcript in response to osmotic stress is a consequence of increased endogenous ABA levels in developing embryos. Sod4 mRNA is up-regulated by ABA in viviparous-1 mutant embryos. Sod4 transcript increases within 4 h with ABA not only in developing embryos but also in mature embryos and in young leaves. Sod4A transcript is up-regulated by ABA only in young leaves, but neither Sod4 nor Sod4A transcripts changed in response to osmotic stress. Our data suggest that in leaves Sod4 and Sod4A may respond to ABA and osmotic stress via alternate pathways. Since the Sod genes have a known function, we hypothesize that the increase in Sod mRNA in response to ABA is due in part to ABA-mediated metabolic changes leading to changes in oxygen free radical levels, which in turn lead to the induction of the antioxidant defense system.
SOD (EC 1.15.1.1) is a metalloenzyme that is found in almost all
organisms and catalyzes the dismutation of superoxide anion radical to
hydrogen peroxide and molecular oxygen (Fridovich, 1978 The cytosolic isozyme SOD-4A is biochemically indistinct from SOD-4.
Deduced amino acid sequence analysis from cDNA clones showed that there
are only two amino acid differences between the SOD-4 and SOD-4A
proteins (Cannon and Scandalios, 1989 ABA has pleiotropic effects on plant growth and development. A number
of ABA-responsive genes are normally expressed during late
embryogenesis when seed tissues desiccate and the embryos become
dormant (Finkelstein et al., 1985 The inbred maize (Zea mays) lines W64A, M1A4
(Vp5/vp5), and Vp1 were used in these studies. W64A and M1A4
are maintained in this laboratory, and Vp1 was obtained from the Maize
Stock Center at the University of Illinois (Urbana). The maize
vp mutants contain either lowered amounts of ABA (M1A4,
vp5) or are morphologically insensitive to normal endogenous
levels of ABA (vp1), resulting in precocious germination in
the ear. The viviparous kernels can be distinguished from wild-type
kernels early in development based on endosperm and embryo color. The
vp5 mutant in M1A4 interrupts ABA biosynthesis early in the
biosynthetic pathway (Robichaud et al., 1980 Treatment Conditions
RNA Analyses Total RNA was isolated from control and ABA-treated samples by a modification of the cold phenol extraction method (Beachy et al., 1985 ). For northern-blot analysis, total RNA (10 or 20 µg) from each
sample was separated in denaturing 1.2% agarose gels and transferred
onto nylon membranes. The blots were sequentially hybridized with
32P-labeled gene-specific probes for
Sod4 and Sod4A (Cannon and Scandalios, 1989) in
modified Church buffer (Church and Gilbert, 1984) containing 7% SDS,
0.5 m EDTA, 0.5 m sodium phosphate, and 1%
BSA. After these analyses had been performed, probes were stripped from
the filters and reprobed first with insert DNA from clone p1015 containing the coding sequence of the ABA-regulated
Em polypeptide (Williamson et al., 1985) and subsequently
with a DNA fragment from clone pHA2 containing an
18S ribosomal sequence (Jorgensen et al., 1987).
Sod4 and Sod4A Transcript Accumulation in Scutella during Late Embryogenesis We previously found that Sod4 and Sod4A transcripts accumulate to high levels in scutella of mature embryos (Cannon and Scandalios, 1989); however, the expression pattern of
cytosolic Sod at middle to late embryogenesis had not been
determined. Sod4 and Sod4A transcript
accumulation was examined during middle to late embryogenesis (17-30
dpp). Our results show that Sod4 and Sod4A
transcripts start to accumulate at 17 dpp and reach maximum levels 30 dpp (Fig. 1). The typical ABA-responsive
Em transcript of wheat was used as a control and showed a
similar accumulation pattern. The late embryogenesis-abundant gene-like
expression of Sod4 and Sod4A accumulation led us
to speculate that ABA may play a role in Sod transcript
accumulation during middle to late embryogenesis. Since these two
cytosolic Sod genes are almost identical in their coding region, similar expression patterns led us to believe that they may
share some common sequences in their promoter region.
Sequence Comparison of the Promoter of Sod4 and Sod4A We compared the promoter sequence of Sod4 and Sod4A up to the start of transcription. Under the best alignment conditions, Sod4 and Sod4A share only 40% of sequence identity. Sequence alignment also revealed that the ABA-responsive element is found in the promoter of the Sod4 gene (212, CACGTGGT; 322, GACGTACC) but cannot be located in the promoter of Sod4A (Fig. 2). Two Y-box elements are located only in the promoter region of the Sod4A. The Y-box motif mediates redox-dependent transcriptional activation (Duh et al., 1995). These data imply that
Sod4 transcript accumulation during late embryogenesis may
be due to changes in endogenous ABA levels, whereas the accumulation of
Sod4A transcript at the same developmental stage may be due
to signals other than ABA. To prove this hypothesis, we examined the
accumulation of the Sod4 and Sod4A transcripts in
response to exogenously applied ABA in 28-dpp embryos.
Sod4 and Sod4A Transcript Accumulation in Response to ABA in Late-Developing Embryos The effects of ABA on accumulation of the Sod4 and Sod4A transcripts in scutella of developing maize embryos were investigated. The steady-state levels of the Sod4 transcript increased with increasing concentrations of ABA. The Sod4A transcript increased in control embryos ( ABA for
24 h) in comparison with untreated embryos (in planta)
but did not increase further in response to ABA (Fig.
3, top). The Em transcript
increased in response to all ABA concentrations applied. In a
time-course experiment the Sod4 transcript started to
accumulate after 4 h of ABA (10 4
m) treatment and reached highest levels at 24 h. An
interesting finding was that the Sod4 transcript in control
embryos (ABA) was also increased between 4 and 24 h. The
Sod4A transcript in control embryos increased at 8 to
24 h, whereas transcript accumulation was repressed in ABA-treated
embryos (Fig. 3, bottom). The Em transcript increased in
response to ABA within 4 h and reached its maximum 12 h after
ABA treatment.
Effects of ABA on Sod4 and Sod4A Transcript Accumulation in Germinating Embryos The effects of ABA on Sod4 and Sod4A expression were also examined in mature germinating maize embryos. We used 5-dpi germinating embryos to conduct the same ABA treatments as described above for developing embryos. Maize embryos (scutella plus axes) were isolated from 5-dpi W64A seedlings and incubated on Murashige-Skoog medium supplemented with increasing doses of ABA (0, 105, 104, and 103
m) for 24 h. The Sod4 transcript is low in
5-dpi scutella (in planta control) and increased dramatically after
24 h of ABA treatment. The maximum increase in Sod4
transcript was observed at 103 m ABA (Fig.
4, top). The Sod4A transcript
is relatively high in 5-dpi scutella, but it did not change in response
to ABA. A time-course experiment was conducted with 5-dpi embryos.
Northern-blot analysis showed that the Sod4 transcript
started to accumulate after 2 h of ABA treatment and continued to
increase to high levels at 24 h (Fig. 4, bottom). On the other
hand, the Sod4A transcript showed a slight decrease in
response to ABA throughout the 24-h treatment period.
Effects of Osmotic Stress on the Expression of Sod4 and Sod4A in Developing and Germinating Embryos We also examined the effect of high osmoticum (11% mannitol) on Sod4 and Sod4A transcript accumulation. In 28-dpp developing embryos the Sod4 transcript showed a similar accumulation pattern (in comparison with ABA response) in response to osmotic stress (11% mannitol; Fig. 5, top). The Sod4 transcript started to increase in 4 h and reached maximum levels by 24 h in response to mannitol (11%, w/v). Similar to the ABA response, the Sod4A transcript accumulation decreased in response to mannitol. In 5-dpi embryos the Sod4 transcript increased in response to mannitol (11%, w/v), whereas Sod4A did not change (Fig. 5, bottom). The Em transcript normally cannot be detected at that stage. After 24 h of ABA treatment, a different Em transcript was induced with higher Mr than the transcript normally found in developing embryos. Litts et al. (1987) reported that
Em comprises a multigene family, but variable Em
transcript accumulation in response to ABA has not been previously documented.
Accumulation of the Sod4 and Sod4A Transcripts in Scutella of an ABA-Deficient Mutant in Response to ABA and High Osmoticum To understand the possible role of ABA in the accumulation of Sod transcripts in developing embryos treated with high osmoticum, the accumulation of Sod4 and Sod4A transcripts was examined in an ABA-deficient mutant (vp5/vp5) and its wild-type sibling (Vp5/). Ears were harvested from 25-dpp
heterozygous plants. Embryos were isolated and placed on
Murashige-Skoog medium supplemented with 104
m ABA, 20% (w/v) Suc, or 11% (w/v) mannitol for 24 h
in the dark. Scutella were collected for RNA isolation. Exogenous
application of ABA resulted in increased accumulation of the
Sod4 transcript in both wild-type (Vp5/) and
mutant embryos (vp5/vp5). However, increased accumulation of
the Sod4 transcript in response to high osmoticum was
detected only in wild-type embryos and not in the ABA-deficient mutant
(Fig. 6), suggesting that the
accumulation of the Sod4 transcript in response to high
osmoticum is due to an increase in the endogenous ABA levels. In
contrast, the Sod4A transcript did not change in either the
wild-type or the vp5 mutant in response to ABA or high
osmoticum.
Accumulation of the Sod4 and Sod4A Transcripts in Excised Embryos of vp1 Mutants and Their Wild-Type Siblings in Response to ABA The change in Sod4 and Sod4A transcript accumulation was also examined in the ABA-insensitive mutant vp1. Ears containing both mutant (vp1/vp1) and wild-type (Vp1/) kernels were harvested from heterozygous
plants at 18 dpp. Embryos were isolated and placed on Murashige-Skoog
medium supplemented with 104 m ABA
for 24 h in the dark. Scutella were collected for RNA isolation after treatments. Results showed that the Sod4 transcript
increased in response to ABA in both the wild type and the
vp1 mutant, but the absolute levels of the Sod4
transcript are much higher in the wild type than in the vp1
mutant (Fig. 7). The Sod4A
transcript was detectable but showed no change in response to ABA in
both wild-type and vp1 mutant embryos. In contrast to
Sod4, the Em transcript exhibits a significant
increase in wild-type ABA-treated embryos but had very low detectable
transcript levels in 18-dpp vp1 mutant embryos in response
to ABA.
Accumulation of Sod Transcripts in Response to ABA and High Osmoticum in Young Leaves To understand the mechanisms of cytosolic Sod gene responses to ABA, we also examined the effect of ABA on Sod4 and Sod4A expression in young maize leaves. Seven-day-old light-grown W64A seedlings were harvested and roots were soaked in a solution containing 104
m ABA or 11% mannitol for 2, 4, 8, 12, and 24 h in
the light. After treatment, leaves were collected and total RNA was
isolated for northern-blot analysis. The Sod4 transcript was
almost undetectable in untreated leaves but increased dramatically in
response to ABA within 4 h and reached highest levels at 12 to
24 h. The Sod4 transcript increased in response to
mannitol at 8 and 12 h. The Sod4A transcript increased
in response to ABA after 12 to 24 h of treatment. The
Em transcript could not be detected in young leaves. Thus,
we used an ABA-responsive maize Cat1 transcript as a control
(Williamson and Scandalios, 1992a). The Cat1 transcript showed a pattern similar to Sod4 in response to ABA;
however, the Cat1 transcript was also increased dramatically
in response to mannitol at 12 to 24 h of treatment, whereas
Sod4 and Sod4A showed no transcript increase in
response to mannitol after 24 h of treatment (Fig.
8). These data clearly indicate that the Sod4 transcript can be induced by ABA not only in immature
embryos but also in mature embryos and in young leaves. These data also suggest that the Sod4 mRNA accumulation in response to ABA
is not developmental stage dependent and might represent a general stress-response mechanism in which the Sod4 gene product
increases to protect plants from ABA-mediated stress. The change of
Sod4A transcript levels in response to ABA is dependent on
tissue and developmental stages. These data also suggest that there are
different pathways for the response of Sod genes to ABA and
mannitol in young leaves.
We have examined the Sod4 and Sod4A transcript accumulation during embryo development and in response to ABA at late embryogenesis, postgermination, and in young leaves. Our results indicate that the two closely related cytosolic Sod4 and Sod4A genes responded differently to ABA at each developmental stage examined. Both Sod4 and Sod4A transcripts increased to high levels during late embryogenesis; however, only the Sod4 transcript was up-regulated in response to ABA in 28-dpp scutella, in 5-dpi scutella, and in young leaves. The Sod4A transcript, on the other hand, showed no increase in response to ABA in developing and germinating embryos but increased in response to ABA after 12 h in young leaves. The Sod4 transcript increased only after a few hours following ABA treatment at all three stages. This implies that Sod4 might be directly responding to ABA, whereas the response of Sod4A to ABA in leaves is likely to be indirect, responding to ABA-mediated metabolic changes or stress. The Maize Sod4 Gene Is Unique and Different in Its Response to ABA in Comparison with a Typical ABA-Regulated Gene, Em We found that Sod4 and the typical ABA-regulated gene Em have similar expression patterns in response to ABA in W64A developing embryos; however, Sod4 is also unique and different from Em. An interesting finding is that the Sod4 transcript in control embryos (ABA) also increased at
4 h and reached high levels in 24 h, whereas the
Em transcript in controls increased slightly only after
12 h. It is likely that Sod4 responds to developmental
signals other than ABA in the control embryos (ABA), and the effects of ABA are superimposed on the developmental signal in ABA-treated embryos. In germinating embryos and in leaves the developmental signal
no longer affects Sod4 gene expression. Thus, the effect of
ABA on Sod4 expression is clearly observed within a few
hours after ABA treatment. Previous studies showed that the
Sod4 transcript accumulates to high levels in 3- to 6-dpi
scutella, whereas the Sod4A transcript accumulates to high
levels 5 to 10 dpi (Kernodle and Scandalios, 1996). This implies that
the Sod4 transcript accumulates earlier than
Sod4A after germination. They may respond to different signals during that period. The ABA-responsive Em transcript
decreases to undetectable levels after 1 dpi and this is also
coincident with the decrease in endogenous ABA levels after 1 dpi
(Williamson and Scandalios, 1994). Both Sod4 and
Sod4A transcripts increased in control scutella in 28-dpp
embryos. The explanation for this is that when immature embryos are
isolated and cultured in Murashige-Skoog medium without the presence of
ABA, they will start to germinate. Given the fact that the
Sod4 and the Sod4A transcripts accumulate to high
levels after seed germination, the increase in Sod4 and Sod4A transcripts in control developing embryos (ABA,
24 h) may be caused by the same developmental signals that induce
the Sod4 and Sod4A transcripts after seed
germination.
There Are at Least Two Pathways Involved in the Response of the Maize Sod4 Gene to ABA Utilizing the ABA-insensitive mutant line Vp1, we found that Sod4 is induced by ABA in both wild-type (Vp1/) and mutant (vp1/vp1) 18-dpp embryos with
the highest Sod4 mRNA level found in ABA-treated wild-type
embryos. The Em transcript is induced only by ABA in wild-type embryos and there is almost no detectable Em mRNA
in 18-dpp vp1 mutant embryos. In immature embryos the Vp1
trans-acting factor is present (McCarty et al., 1989) and is
required for maximizing the ABA-mediated induction of Sod4
in wild-type embryos where the highest Sod4 mRNA was
detected in response to ABA. However, in germinating embryos and in
young leaves, Vp1 factor is not present (McCarty et al., 1989) and is
not required for the ABA-mediated induction of Sod4 in
vitro. We previously reported that the Sod4 transcript
accumulates to high levels in germinating embryos when ABA and Vp1 are
not present (Kernodle and Scandalios, 1996). This suggests that the
expression of Sod4 during postgermination is regulated by
signals other than ABA in vivo. From the above observations we
concluded that at least two independent pathways are involved in
ABA-mediated Sod4 expression. During embryogenesis, the
Vp1-dependent pathway is most likely to be involved in the ABA-induced
expression of Sod4 because the Sod4 transcript
accumulates to highest levels in ABA-treated wild-type
(Vp1/) embryos. In germinating embryos and in leaves the
induction of Sod4 mRNA by ABA is not dependent on Vp1
because Vp1 transcript is not present during this period.
Sod4 Transcript Accumulation in Response to Osmotic Stress in Maize Embryos Is Due to Increased Endogenous ABA Levels In numerous systems osmotic stress has been shown to increase endogenous ABA levels (Skriver and Mundy, 1990). Thus, it has been
suggested that osmotic stress is mediated via an ABA-driven transduction pathway. Other reports indicate distinctions between the
response to ABA and osmotic stress. A desiccation responsive gene
(Rd 29) in Arabidopsis is rapidly induced by water and salt stress in an ABA-independent manner (Yamaguchi-Shinozaki and Shinozaki, 1993). The MMK4 (MAP kinase; mitogen-activated protein) gene in alfalfa
accumulates after drought and cold treatment but not in response to
ABA, indicating that the MMK4 kinase pathway mediates drought and cold
signaling independently of ABA (Jonak et al., 1996). Utilizing the
ABA-deficient mutant vp5, we have demonstrated that the
Sod4 transcript is increased only in wild-type embryos in
response to osmotic stress; however, Sod4 mRNA increased to the same levels in wild-type and vp5 embryos in response to
ABA. These data suggest that the increase of Sod4 transcript
in response to high osmoticum is mediated by an increase in endogenous
ABA levels in developing embryos. The Em transcript showed a
similar expression in response to ABA and high osmoticum. It has been reported that the transcript of the wheat Em gene can also
accumulate in seedlings in response to ABA and desiccation (Morris et
al., 1988); however, we cannot detect Em transcript in young
maize leaves under ABA treatment or under osmotic stress. In young
leaves both Sod4 and Sod4A transcripts increase
in response to ABA; however, Sod4 and Sod4A
transcripts do not change in response to mannitol in leaves. These data
imply that the Sod4 and Sod4A response to mannitol is dependent on the developmental stage. Their transcripts do
not change in response to mannitol and may be due to different sensitivity to mannitol-mediated ABA accumulation in young leaves or
simply due to different pathways between the mannitol response in
leaves and in embryos. Another antioxidant gene, Cat1,
responds positively to both ABA and mannitol in young leaves under the same treatment conditions.
* Corresponding author; e-mail jgs{at}unity.ncsu.edu; fax 1-919-515-3355. Received October 24, 1997;
accepted February 3, 1998.
Abbreviations: Cat1, catalase-1. dpi, days postimbibition. dpp, days postpollination. ROS, reactive oxygen species. SOD, superoxide dismutase. Vp1, viviparous-1.
We thank Stephanie Ruzsa and Sheri Kernodle for expert technical assistance.
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Abstract
Introduction
end of the cDNA, we
isolated and characterized the Sod4 and Sod4A
genomic clones (Kernodle and Scandalios, 1996
-conglycin in seeds of transformed petunia plants.
EMBO J
4:
3047-3053