| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
|
Plant Physiol. (1998) 116: 1573-1583 Differential Regulation of Sugar-Sensitive Sucrose Synthases by Hypoxia and Anoxia Indicate Complementary Transcriptional and Posttranscriptional Responses1
Plant Molecular and Cellular Biology Program, Horticultural Sciences Department, Fifield Hall, University of Florida, Gainesville, Florida 32611
The goal of this research was to resolve the hypoxic and anoxic responses of maize (Zea mays) sucrose (Suc) synthases known to differ in their sugar regulation. The two maize Suc synthase genes, Sus1 and Sh1, both respond to sugar and O2, and recent work suggests commonalities between these signaling systems. Maize seedlings (NK508 hybrid, W22 inbred, and an isogenic sh1-null mutant) were exposed to anoxic, hypoxic, and aerobic conditions (0, 3, and 21% O2, respectively), when primary roots had reached approximately 5 cm. One-centimeter tips were excised for analysis during the 48-h treatments. At the mRNA level, Sus1 was rapidly up-regulated by hypoxia (approximately 5-fold in 6 h), whereas anoxia had less effect. In contrast, Sh1 mRNA abundance increased strongly under anoxia (approximately 5-fold in 24 h) and was much less affected by hypoxia. At the enzyme level, total Suc synthase activity rose rapidly under hypoxia but showed little significant change during anoxia. The contributions of SUS1 and SH1 activities to these responses were dissected over time by comparing the sh1-null mutant with the isogenic wild type (Sus+, Sh1+). Sh1-dependent activity contributed most markedly to a rapid protein-level response consistently observed in the first 3 h, and, subsequently, to a long-term change mediated at the level of mRNA accumulation at 48 h. A complementary midterm rise in SUS1 activity varied in duration with genetic background. These data highlight the involvement of distinctly different genes and probable signal mechanisms under hypoxia and anoxia, and together with earlier work, show parallel induction of "feast and famine" Suc synthase genes by hypoxia and anoxia, respectively. In addition, complementary modes of transcriptional and posttranscriptional regulation are implicated by these data, and provide a mechanism for sequential contributions from the Sus1 and Sh1 genes during progressive onset of naturally occurring low-O2 events.
Low O2 induces marked changes in physiology
and gene expression in plants and poses an important environmental
stress (for review from different perspectives, see Perata and Alpi,
1993 Among these low-O2-induced proteins, Suc synthase
occupies a prominent position because it typically catalyzes the
essential first step in C use by Suc-importing cells. Although Suc
synthase and invertase can both cleave Suc, invertase activity declines under anoxia (Guglielminetti et al., 1997 In addition, the two Suc synthase genes in maize are differentially
responsive to sugar availability (Koch et al., 1992 Finally, increasing evidence points to distinct differences between
hypoxic and anoxic stresses (Johnson et al., 1989 The purpose of this research was to further define the
low-O2 responses of the maize Suc synthases,
which are known to be differentially sugar modulated. Effects of
hypoxia and anoxia were compared over time at the mRNA, protein, and
enzyme activity levels, and results were examined in the context of a
possible link between sugar- and O2-sensing
systems. An additional, unexpected aspect of this work was the contrast
in patterns of temporal regulation revealed for both Sus1
and Sh1 by time-course analyses of
low-O2 responses. Both transcriptional and
posttranscriptional modes of up-regulation are implicated.
Maize (Zea mays L.) seeds of hybrid NK508,
inbred W22, and an isogeneic sh1-deletion mutant (in a W22
background) were surface sterilized for 20 min in 0.525% (v/v) bleach,
and rinsed with water for 20 min. Seeds were germinated in the dark at
18°C on two layers of moist 3MM paper (Whatman) in 27- × 39-cm
glass pans. Each pan was sealed with plastic (except import and export
tubes) and supplied with a continuous air flow of 1 L
min Hypoxic and Anaerobic Treatments
Enzyme Extraction and Assay Frozen samples were ground to a fine powder in liquid N2 using a mortar and pestle. Frozen powder was transferred to a second, chilled mortar for continued extraction in medium containing 200 mm Hepes buffer, pH 7.5, 1 mm DTT, 5 mm MgCl2, 1 mm EGTA, 20 mm sodium ascorbate, 1 mm PMSF, and 10% (w/v) polyvinylpolypyrrolidone. The buffer-to-tissue ratio was 10:1. Buffered extract was centrifuged at 14,000g for 1 min, and the supernatant was dialyzed (10,000 Mr cutoff) at 4°C for 24 h against extraction buffer diluted 1:40. The buffer was changed several times during dialysis.RNA Extraction and Analysis Frozen samples were ground to a fine powder in liquid N2. RNA was extracted using the method of McCarty (1986) , and quantified by A260. Ten
micrograms of total RNA was separated by electrophoresis in 1% agarose
gels containing formaldehyde, transferred to a nylon membrane, and
hybridized with maize cDNA probes for Sh1 and
Sus1 (gift from L.C. Hannah, University of Florida,
Gainesville), and Alcohol dehydrogenase 1 (Adh1,
a gift from R. Ferl, University of Florida), as in Koch et al. (1992).
Blots were visualized on radiographic film at  80°C, and the
relative abundance of mRNA was quantified using a phosphor imager
(Molecular Dynamics, Sunnyvale, CA).
Protein Gel Blots Protein extracts were denatured and separated by SDS-PAGE in a vertical gel apparatus. Each lane was loaded with 5 µg of protein and electrophoresed at 4°C. Acrylamide was 7.5 and 3.0% (w/v) in the separating and stacking gels, respectively. Samples entered gels at a constant voltage of 200 V and moved through stacking and separating gels at 70 and 200 V, respectively. Proteins were electroblotted onto nitrocellulose membrane, blocked with BSA (3% [w/v] in PBS plus 0.05% Tween 20), and reacted with antibody against SH1 and SUS1 proteins (Koch et al., 1992) (a 1:2000 antibody dilution at 22°C for
1 h in PBS-Tween containing 1% [w/v] BSA). Following
initial hybridization, membranes were rinsed with PBS-Tween for 3 × 20 min and reacted with secondary antibody (alkaline
phosphatase-conjugated goat anti-rabbit IgG [Bio-Rad] diluted 1:2000
in PBS-Tween 20 containing 1% BSA). Antibody hybridization was
visualized using nitroblue tetrazolium chloride and
5-bromo-4-chloro-3-indolyl phosphate.
Sus1 mRNA Levels Respond Markedly to Hypoxia A pronounced feature of the low-O2 responses of root tips of maize seedlings shown in Figure 1 is the rapid increase of Sus1 mRNA abundance in response to hypoxia (3% O2). Within the first 6 h, Sus1 mRNA levels rose to levels 4- to 5-fold greater than in the aerobic controls of both the hybrid (NK508) and inbred (W22) maize genotypes tested. However, responses of the two genotypes differed in that the abundance of Sus1 mRNA in the NK508 (hybrid) plateaued at a high level for at least 48 h under hypoxia, whereas Sus1 message levels in the W22 (inbred) began to decrease after a peak at 6 h, declining to near noninduced levels by 48 h. This difference was initially unexpected because overt contrasts in growth or other low-O2 responses had not been evident between NK508 and W22. The latter was examined as a second, wild-type control for more precise comparisons with a sh1-null mutant in the same isogenic background.
Sh1 mRNA Levels Respond Markedly to Anoxia Figure 2 shows that although Sh1 mRNA levels did not rise significantly above those of aerobic controls until 12 h of anoxia, they ultimately increased by more than 5-fold during a 24-h period in both maize genotypes. Sh1 mRNA abundance continued to rise slowly thereafter. Other studies have reported anaerobic responses as great or greater for Sh1 at the mRNA level in 24-h experiments (McCarty et al., 1986; Springer et al., 1986; Bailey-Serres et al., 1988; McElfresh and
Chourey, 1988; Rowland et al., 1989) and also in shorter-term
experiments (S.L. Fennoy, T. Nong, and J. Bailey-Serres, personal
communication). In contrast, hypoxic conditions had a rapid but less
marked effect on mean Sh1 mRNA levels. The increase was
variable in the NK508 hybrid, and although a significant rise was
observed within the first 6 h in W22, the mRNA level declined
thereafter. Comparison of these hypoxic and anoxic responses defines
Sh1 as an anaerobic gene that is distinctly less sensitive
to hypoxia than to anoxia (unlike Sus1), and demonstrates the extended time course that can be involved in the Sh1
response.
Enzyme Responses Include Changes in Protein Abundance and Activity Figure 3 shows that total Suc synthase activity rose rapidly in response to hypoxia, approximately doubling within the first 3 h for both genotypes. Activity persisted at the elevated levels throughout the 48-h time course, increasing more slowly after 6 h. In seedlings of both genetic backgrounds (NK508 and W22), little or no change in mean total activity was observed after 48 h of anoxic treatment.
Sus1 Gene and SUS1 Protein Responses to Hypoxia and Anoxia in the sh1-Null Mutant To appraise the individual contributions from the Sh1 and Sus1 genes to hypoxic and anoxic responses, comparative studies were conducted using a sh1-null mutant in which the sh1 gene has been deleted, but is otherwise isogenic to the W22 wild type. Results shown in Figure 4A confirm that in the sh1-null mutant, the low-O2 responses of Sus1 mRNA were similar to those shown for the W22 wild type shown in Figure 1B (note quantified values in both figures). This comparison is consistent with earlier work (Chourey and Talercio, 1994) indicating that Sus1 does not fully compensate in the absence of Sh1.
Adh1 as an Indicator of O2 Status The known anaerobic up-regulation of Adh1 (Dennis et al., 1984, 1988; Paul and Ferl, 1991a, 1991b) was used here to verify the low-O2 status at the metabolic level in each
experiment. The mRNA analyses shown in Figure
5 were from blots identical to those for
experiments using NK508 shown in Figure 1. Responses to hypoxia and
anoxia were rapid, rising approximately 5- to 6-fold within 6 h of
treatment, and continuing for 24 h for 0%
O2. The extent and kinetics of this increase were
as reported earlier, although mRNA levels persisted longer in the
present work (Andrews et al., 1994).
Contrasting Temporal Profiles for Hypoxic and Anoxic Contributions at the mRNA and Protein Accumulation Levels Figure 6 compares the temporal profiles of hypoxic and anoxic responses of the two Suc synthases at the mRNA and enzyme activity levels, and presents these relative to concurrent changes in SUS1- and SH1-dependent enzyme activities in the W22 inbred. SUS1 activity was assayed directly in the sh1-null mutant, and SH1-dependent activity was determined as the difference between the sh1-null mutant and its isogenic wild type. Collectively, these data indicate marked differences in responses depending on whether they occur in the first 3 to 6 h, during a second 6- to 12-h period, or as part of a long-term response over 24 to 48 h. In addition, the effects of hypoxia and anoxia have distinctly different temporal profiles that are typified at the mRNA level by rapid Sus1 and more prolonged Sh1 increases, respectively. Contrasts between profiles for mRNA and enzyme activity indicate that complementary modes of transcriptional and posttranscriptional regulation are operating under hypoxia and anoxia, and that these change over the duration of each stress.
This study provides evidence for Sus1 and Sh1 as predominantly hypoxic and anoxic genes, respectively (parallel to their induction by carbohydrate "feast and famine" conditions), and describes the contributions by each of these Suc synthase genes to low-O2 responses at the mRNA, protein, and enzyme levels.
Sus1 and Sh1 Are Up-Regulated Preferentially by Hypoxia and Anoxia, Respectively Until relatively recently, hypoxia (3% O2) and anoxia (0% O2) were not widely viewed as distinctly different types of low-O2 stress. In fact, anaerobic genes have sometimes been used to describe a collective, broadly inclusive group of genes induced under varying degrees of O2 deprivation. Results shown here, however, demonstrate a preferential up-regulation of Sus1 under hypoxia and of Sh1 under anoxia.
Time-Course Profiles Suggest Different Roles for Sus1 and Sh1 mRNAs Contrasts in the time course of the rapid hypoxic (Sus1) and more prolonged anaerobic (Sh1) response profiles observed here over 48-h periods (Figs. 1 and 2) indicate that different mechanisms may be involved in regulating mRNA levels by affecting synthesis and/or longevity. In addition, the temporal variations observed emphasize the extent to which results can differ if compared at a single point in time. Even measurements at 6 h can differ markedly from those at 12 h for mRNA levels and run-on transcriptional analyses of several genes responding to anoxia (Fennoy and Bailey-Serres, 1995; S.L. Fennoy, T. Nong, and J. Bailey-Serres, personal communication). Furthermore, rapid
readjustments in adenylate turnover that occur during initial
low-O2 adjustments (Hochachka et al., 1996) could easily be linked to changes in C flux through glycolysis, a process recently implicated in altering expression of sugar-responsive genes
such as Sus1 and Sh1 (Koch, 1996; Jang et al.,
1997). Eventual depletion of sugars via the Pasteur effect would thus
be separated in time from initial signals of sugar abundance associated
with high flux. This provides one means of testing the degree to which sugar-sensing systems and Suc synthase gene responses can distinguish between supply and flux. Effects of the former could also be enhanced under anoxia relative to hypoxia by limited phloem transport (Saglio, 1985).
O2 and Sugar Availability Exert Similar Patterns of Differential Expression Differential expression of the Sus1 and Sh1 Suc synthase genes may also contribute to the functional roles of isozymes that apparently have otherwise similar characteristics (Su and Preiss, 1978; Echt and Chourey, 1985) and phosphorylation sites (Huber et al., 1996). Expression of these genes differs markedly between tissues (Heinlein and Starlinger, 1989; Rowland et al., 1989; Nolte and
Koch, 1993; Nolte et al., 1995) and also in response to sugar
availability (Koch et al., 1992; Koch, 1996). Extension of these
distinctions to hypoxic and anoxic conditions potentially enhances our
collective understanding of both mechanisms.
Both Suc Synthases Respond to Low O2 at the Protein/Enzyme Activity Level In each of our experiments Suc synthase activity showed a consistent and statistically significant increase in response to hypoxic conditions from as early as 3 h after the start of treatment (Fig. 3, A and B). Little or no significant change in total activity was observed in response to more severe anoxic treatments. However, changes were also observed in both SH1 and SUS1 protein abundance by western-blot analysis, particularly after longer time periods (Figs. 3C and 4B). Results suggest Suc synthase gene expression responds to anoxia and hypoxia not only at the mRNA level, but also at the protein level. Previous reports based on analysis of activity and protein at 20 to 24 h suggest that maize Suc synthase may not be fully inducible under anaerobic conditions (McElfresh and Chourey, 1988; Taliercio and Chourey, 1989). The present
work concurs with the earlier result for total activity at 24 h,
but comparison of wild-type and sh1-null mutant responses
(Figs. 3, 4, and 6B) indicated that there were significant increases in the SH1 portion of this activity. Although increases in Sh1
mRNA levels were markedly greater under anoxia than hypoxia (Figs. 2
and 6A), further analysis revealed SH1 involvement at the
enzyme level under both conditions (Fig. 6B). Data presented here also concur to some degree with earlier evidence for SUS1 as an
anaerobic protein (Bailey-Serres et al., 1988), since activities
consistently increased between 6 and 12 h under both hypoxia and
anoxia (Fig. 6B). However, SUS1 mRNA responses and enzyme
contributions to total activity were far greater under hypoxia than
anoxia, and decreases in activity under anoxia surpassed transient
increases (Fig. 6B).
Comparative Analyses of the sh1-Null Mutant Distinguishes Individual Contributions of SUS1 and SH1 under 0 and 3% O2 In addition to the comparisons discussed above, analysis of temporal response profiles shown in Figure 6 highlights the extent to which short-and long-term responses to low O2 can differ. The most rapid adjustments (< 3 h) are evident at the activity level and differ markedly for SUS1 and SH1. Within 12 h both return to the levels observed in aerobic controls, and more sustained responses related to mRNA accumulation gain prominence. Together, these data suggest that this combination of changes results in sequential, alternating contributions to low-O2 activity, first by very rapid increases in SH1 activity (probably posttranscriptional), followed by relatively rapid up-regulation of Sus1 expression, and finally superseded by sustained up-regulation of Sh1 at the mRNA and enzyme activity level.Closing Comments This research resolves and extends previous studies of maize Suc synthase responses to low O2 in several key respects: (a) distinct responses to hypoxia and anoxia are shown at the gene expression level, with Sus1 and Sh1 preferentially showing rapid hypoxic and prolonged anaerobic responses, respectively; (b) responses involved not only mRNA accumulation, but also enzyme activity and protein abundance; (c) the time-course analyses shown here indicate that for Suc synthases, these changes occur in three phases, the first of which appears to involve rapid, protein-level responses (< 3 h) and to be much like a similar phase proposed to aid rapid readjustment of adenylate levels in animal systems (Hochachka et al., 1996), and the second two are mediated,
respectively, by a relatively rapid up-regulation of Sus1
mRNA accumulation, followed by a slower, more sustained increase in
mRNA accumulation and translation of Sh1; (d) complementary
patterns of regulation are indicated at transcriptional and
posttranscriptional levels; and (e) the distinctly different responses
of Sus1 and Sh1 genes to hypoxia and anoxia
implied markedly different sensitivities to O2
and/or sugar signals. Such differences could provide an effective
mechanism for optimizing sequential contributions by different Suc
synthases (and possibly other genes) to progressively greater stress
during natural episodes of O2 depletion.
* Corresponding author; e-mail kek{at}gnv.ifas.ufl.edu; fax 1-352-392-6479. Received September 26, 1997;
accepted January 14, 1998.
Andrews DL, Drew MC, Johnson JR, Cobb BG (1994) The response of maize seedlings of different ages to hypoxic and anoxic stress. Changes in induction of Adh mRNA, ADH activity, and survival of anoxia. Plant Physiol 105: 53-60 [Abstract] Bailey-Serres J, Kloeckner-Gruissem B, Freeling M (1988) Genetic and molecular approaches to the study of the anaerobic responses and tissue specific gene expression in maize. Plant Cell Environ 11: 351-357 [CrossRef] Bouny JM, Saglio P (1996) Glycolytic flux and hexokinase activities in anoxic maize root tips acclimated by hypoxic pretreatment. Plant Physiol 111: 187-194 [Abstract] Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254 [CrossRef][Web of Science][Medline]
Chourey PS,
Taliercio EW
(1994)
Epistatic interaction and functional compensation between the two tissue- and cell-specific sucrose synthase genes in maize.
Proc Natl Acad Sci
91:
7917-7921
Chourey PS,
Taliercio EW,
Kane EJ
(1991)
Tissue-specific expression and anaerobically induced posttranscriptional modulation of sucrose synthase genes in Sorghum bicolor M.
Plant Physiol
96:
485-490
Dennis ES,
Gerlach WL,
Pryor AJ,
Bennetzen JL,
Inglis A,
Lewellyn D,
Sachs MM,
Ferl RJ,
Peacock WJ
(1984)
Molecular analysis of the alcohol dehydrogenase 1 (Adh1) gene of maize.
Nucleic Acids Res
12:
3983-4000
Dennis ES, Gerlach WL, Walker JC, Lavin M, Peacock WJ (1988) Anaerobically regulated aldolase gene of maize: a chimeric origin? J Mol Biol 202: 759-767 [CrossRef][Web of Science][Medline]
Dennis ES,
Sachs MM,
Gerlach WL,
Finnegan EJ,
Peacock WJ
(1985)
Molecular analysis of the alcohol dehydrogenase 2 (Adh2) gene of maize.
Nucleic Acids Res
13:
727-743
Dolferus R,
Ellis M,
Bruxelles GD,
Trevaskis B,
Hoeren F,
Dennis ES,
Peacock WJ
(1997)
Strategies of gene action in Arabidopsis during hypoxia.
Ann Bot
79:
21-31
Drew MC (1997) Oxygen deficiency and root metabolism: injury and acclimation under hypoxia and anoxia. Annu Rev Plant Physiol Plant Mol Biol 48: 223-250 [CrossRef][Web of Science][Medline]
Echt CS,
Chourey PS
(1985)
A comparison of two sucrose synthase isozymes from normal and shrunken-1 maize.
Plant Physiol
79:
530-536
Farrar J, Williams JHH (1991) Control of the rate of respiration in roots: compartmentation, demand, and the supply of substrate. In M Emms, eds, Compartmentation of Metabolism. Butterworths, London, pp 167-188 Fennoy SL, Bailey-Serres J (1995) Post-transcriptional regulation of gene expression in oxygen-deprived roots of maize. Plant J 7: 287-295 [CrossRef][Web of Science] Guglieminetti L, Alpi A, Perata P (1996) Shrunken-1-encoded sucrose synthase is not required for the sucrose-ethanol transition in maize under anaerobic conditions. Plant Sci 119: 1-10 [CrossRef] Guglielminetti L, Perata P, Alpi A (1995) Effect of anoxia on carbohydrate metabolism in rice seedlings. Plant Physiol 108: 735-741 [Abstract] Guglielminetti L, Wu Y, Boschi E, Yamaguchi J (1997) Effects of anoxia on sucrose degrading enzymes in cereal seeds. J Plant Physiol 150: 251-258 [Web of Science]
Hake S,
Kelley PM,
Taylor WC,
Freeling M
(1985)
Coordinate induction of alcohol dehydrogenase 1, aldolase, and other anaerobic RNAs in maize.
J Biol Chem
260:
5050-5054
He CJ, Finlayson SA, Drew MC, Jordan WR, Morgan PW (1996a) Ethylene biosynthesis during aerenchyma formation in roots of maize subjected to mechanical impedance and hypoxia. Plant Physiol 112: 1679-1685 [Abstract] He CJ, Morgan PW, Drew MC (1996b) Transduction of an ethylene signal is required for cell death and lysis in the root cortex of maize during aerenchyma formation induced by hypoxia. Plant Physiol 112: 463-472 [Abstract] Heinlein M, Starlinger P (1989) Tissue and cell-specific expression of the two sucrose synthase isozymes in developing maize kernels. Mol Gen Genet 215: 441-446 [CrossRef][Web of Science]
Hochachka PW,
Buck LT,
Doll CJ,
Land SC
(1996)
Unifying theory of hypoxia tolerance: molecular/metabolic defense and rescue mechanisms for surviving oxygen lack.
Proc Natl Acad Sci USA
93:
9493-9498
Huber SC, Huber JL, Liao PC, Gage DA, McMichael RW, Chourey PS, Hannah LC, Koch KE (1996) Phosphorylation of serine-15 of maize leaf sucrose synthase. Plant Physiol 112: 793-802 [Abstract] Jang JC, Leon P, Zhou L, Sheen J (1997) Hexokinase as a sugar sensor in higher plants. Plant Cell 9: 5-19 [Abstract]
Johnson JR,
Cobb BG,
Drew MC
(1989)
Hypoxic induction of anoxia tolerance in root tips of Zea mays.
Plant Physiol
91:
837-841
Johnson JR, Cobb BG, Drew MC (1994) Hypoxic induction of anoxia tolerance in root tips of Adh1-null Zea mays L. Plant Physiol 105: 61-67 [Abstract]
Kelley PM,
Freeling M
(1984a)
Anaerobic expression of maize fructose-1,6-diphosphate aldolase.
J Biol Chem
259:
14180-14183
Kelley PM,
Freeling M
(1984b)
Anaerobic expression of maize glucose phosphate isomerase I.
J Biol Chem
259:
673-677
Kelly PM, Tolan DR (1986) The complete amino acid sequence of the anaerobically induced aldolase from maize derived from cDNA clones. Plant Physiol 100: 1-6 Koch KE (1996) Carbohydrate-modulated gene expression in plants. Annu Rev Plant Physiol Plant Mol Biol 47: 509-540 [CrossRef][Web of Science]
Koch KE,
Nolte KD,
Duke ER,
McCarty DR,
Avigne WT
(1992)
Sugar levels modulate differential expression of maize sucrose synthase genes.
Plant Cell
4:
59-69
Lal SK, Johnson S, Conway T, Kelley PM (1991) Characterization of a maize cDNA that complements an enolase-deficient mutant of Escherichia coli. Plant Mol Biol 16: 787-795 [CrossRef][Medline] Lal SK, Kelly PM, Elthon TE (1994) Purification and differential expression of enolase from maize. Physiol Plant 91: 587-592 [CrossRef] Martin T, Frommer WB, Salanoubat M, Willmitzer L (1993) Expression of an Arabidopsis sucrose synthase gene indicates a role in metabolization of sucrose both during phloem loading and in sink organs. Plant J 4: 367-377 [CrossRef][Web of Science][Medline] McCarty DR (1986) A rapid and simple method for extracting RNA from maize tissues. Maize Gen Coop News Lett 60: 61
McCarty DR,
Shaw JR,
Hannah LC
(1986)
The cloning, genetic mapping, and expression of the constitutive sucrose synthase locus of maize.
Proc Natl Acad Sci USA
83:
9099-9103
McElfresh KC,
Chourey PS
(1988)
Anaerobiosis induces transcription but not translation of sucrose synthase in maize.
Plant Physiol
87:
542-546
Nolte KD, Hendrix DL, Radin JW, Koch KD (1995) Sucrose synthase localization during initiation of seed development and trichome differentiation in cotton ovules. Plant Physiol 109: 1285-1293 [Abstract] Nolte KD, Koch KE (1993) Companion-cell-specific localization of sucrose synthase in zones of phloem loading and unloading. Plant Physiol 101: 899-905 [Abstract] Paul A-L, Ferl RJ (1991a) Adh1 and Adh2 regulation. Maydica 36: 129-134
Paul A-L,
Ferl RJ
(1991b)
In vivo footprinting reveals unique cis-elements and different modes of hypoxic induction in maize Adh1 and Adh2.
Plant Cell
3:
159-168
Perata P, Alpi A (1993) Plant responses to anaerobiosis. Plant Sci 93: 1-17 [CrossRef]
Perata P,
Guglielminetti L,
Alpi A
(1997)
Mobilization of endosperm reserves in cereal seeds under anoxia.
Ann Bot
79:
49-56
Peschke VM, Sachs MM (1993) Multiple maize pyruvate decarboxylase genes are induced by hypoxia. Mol Gen Genet 240: 206-212 [Medline]
Ricard B,
Rivoal J,
Spiteri A,
Pradet A
(1991)
Anaerobic stress induces the transcription and translation of sucrose synthase in rice.
Plant Physiol
95:
669-674
Rivoal J, Thind S, Pradet, Richard B (1997) Differential induction of pyruvate decarboxylase subunits and transcripts in anoxic rice seedlings. Plant Physiol 114: 1021-1029 [Abstract] Rowland LJ, Chen YC, Chourey PS (1989) Anaerobic treatment alters the cell specific expression of Adh-1, Sh, and Sus1 genes in roots of maize seedlings. Mol Gen Genet 218: 33-40
Russell DA,
Sachs MM
(1989)
Differential expression and sequence analysis of the maize glyceraldehyde-3-phosphate dehydrogenase gene family.
Plant Cell
1:
793-803
Sachs MM, Freeling M, Okimoto R (1980) The anaerobic proteins of maize. Cell 20: 761-767 [CrossRef][Web of Science][Medline] Sachs MM, Subbaiah CC, Saab IN (1996) Anaerobic gene expression and flooding tolerance in maize. J Exp Bot 47: 1-15
Saglio PH
(1985)
Effect of path or sink anoxia on sugar translocation in roots of maize seedlings.
Plant Physiol
77:
285-290
Setter TL,
Ellis M,
Laureles EV,
Ella ES,
Senadhira D,
Mishra SB,
Sarkarung S,
Datta S
(1997)
Physiology and genetics of submergence tolerance in rice.
Ann Bot
79:
67-77
Shaw JR, Ferl RJ, Baier J, St Clair D, Carson C, McCarty DR, Hannah LC (1994) Structural features of the maize Sus1 gene and protein. Plant Physiol 106: 1659-1665 [Abstract] Springer B, Werr W, Starlinger P, Bennett CD, Zokolica M, Freeling M (1986) The shrunken gene on chromosome 9 of Zea mays L. is expressed in various plant tissues and encodes an anaerobic protein. Mol Gen Genet 205: 461-468 [CrossRef][Web of Science][Medline]
Su J-C,
Preiss J
(1978)
Purification and properties of sucrose synthase from maize kernels.
Plant Physiol
61:
389-393
Taliercio EW,
Chourey PS
(1989)
Post-transcriptional control of sucrose synthase expression in anaerobic seedlings of maize.
Plant Physiol
90:
1359-1364
Vartapetian BB, Jackson MB (1997) Plant adaptations to anaerobic stress. Ann Bot (Suppl. A) 79: 3-20 Zhang XQ, Chollet R (1997) Seryl-phosphorylation of soybean nodule sucrose synthase (nodulin-100) by a Ca+2-dependent protein kinase. FEBS Lett 410: 126-130 [CrossRef][Web of Science][Medline].
Copyright Clearance Center: 0032-0889/98/116/1573/11
|
|||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
|
|
 |
|
  J. Kreuzwieser, J. Hauberg, K. A. Howell, A. Carroll, H. Rennenberg, A. H. Millar, and J. Whelan Differential Response of Gray Poplar Leaves and Roots Underpins Stress Adaptation during Hypoxia Plant Physiology, January 1, 2009; 149(1): 461 - 473. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 K. A. Duncan, S. C. Hardin, and S. C. Huber The Three Maize Sucrose Synthase Isoforms Differ in Distribution, Localization, and Phosphorylation Plant Cell Physiol., July 1, 2006; 47(7): 959 - 971. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 C. C. Subbaiah, A. Palaniappan, K. Duncan, D. M. Rhoads, S. C. Huber, and M. M. Sachs Mitochondrial Localization and Putative Signaling Function of Sucrose Synthase in Maize J. Biol. Chem., June 9, 2006; 281(23): 15625 - 15635. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. C. Hardin, H. Winter, and S. C. Huber Phosphorylation of the Amino Terminus of Maize Sucrose Synthase in Relation to Membrane Association and Enzyme Activity Plant Physiology, April 1, 2004; 134(4): 1427 - 1438. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S. Baud, M.-N. Vaultier, and C. Rochat Structure and expression profile of the sucrose synthase multigene family in Arabidopsis J. Exp. Bot., February 1, 2004; 55(396): 397 - 409. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. L. Bologa, A. R. Fernie, A. Leisse, M. Ehlers Loureiro, and P. Geigenberger A Bypass of Sucrose Synthase Leads to Low Internal Oxygen and Impaired Metabolic Performance in Growing Potato Tubers Plant Physiology, August 1, 2003; 132(4): 2058 - 2072. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
P. Geigenberger Regulation of sucrose to starch conversion in growing potato tubers J. Exp. Bot., January 3, 2003; 54(382): 457 - 465. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D.H. P. Barratt, L. Barber, N. J. Kruger, A. M. Smith, T. L. Wang, and C. Martin Multiple, Distinct Isoforms of Sucrose Synthase in Pea Plant Physiology, October 1, 2001; 127(2): 655 - 664. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. C. Subbaiah and M. M. Sachs Altered Patterns of Sucrose Synthase Phosphorylation and Localization Precede Callose Induction and Root Tip Death in Anoxic Maize Seedlings Plant Physiology, February 1, 2001; 125(2): 585 - 594. [Abstract] [Full Text]
|
|
|
|
|
|
K. E. Koch, Z. Ying, Y. Wu, and W. T. Avigne Multiple paths of sugar-sensing and a sugar/oxygen overlap for genes of sucrose and ethanol metabolism J. Exp. Bot., February 1, 2000; 51(90001): 417 - 427. [Abstract] [Full Text]
|
|
|
|
|
|
W. W.P. Chang, L. Huang, M. Shen, C. Webster, A. L. Burlingame, and J. K.M. Roberts Patterns of Protein Synthesis and Tolerance of Anoxia in Root Tips of Maize Seedlings Acclimated to a Low-Oxygen Environment, and Identification of Proteins by Mass Spectrometry Plant Physiology, February 1, 2000; 122(2): 295 - 318. [Abstract] [Full Text]
|
|
|
|
|
|
Y. Zeng, Y. Wu, W. T. Avigne, and K. E. Koch Rapid Repression of Maize Invertases by Low Oxygen. Invertase/Sucrose Synthase Balance, Sugar Signaling Potential, and Seedling Survival Plant Physiology, October 1, 1999; 121(2): 599 - 608. [Abstract] [Full Text]
|
|
| |||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
| ASPB Publications | PLANT PHYSIOLOGY® | THE PLANT CELL | |
|---|---|---|---|
Top
Abstract
Introduction
1 throughout the 5- to 7-d
germination period. Entire seedlings were exposed to this environment
and remained on moist filter paper throughout the experiment. During
subsequent experimental treatments, terminal 1-cm tips were excised
from primary roots at selected time points, weighed, frozen in liquid
N2, and stored at 
