|
Plant Physiol, October 1999, Vol. 121, pp. 599-608
Rapid Repression of Maize Invertases by Low Oxygen.
Invertase/Sucrose Synthase Balance, Sugar Signaling Potential, and
Seedling Survival1
Ying
Zeng,
Yong
Wu,
Wayne T.
Avigne, and
Karen E.
Koch*
Plant Molecular and Cellular Biology Program, Horticultural
Sciences Department, 1143 Fifield Hall, University of
Florida, Gainesville, Florida 32611
We show here that invertase gene
expression and the invertase-sucrose (Suc) synthase ratio decrease
abruptly in response to low oxygen in maize root tips. In addition to
aiding in the conservation of carbon and possibly ATP, this response
has the potential to directly affect sugar signaling relative to carbon
flux. Experiments were motivated by the potential for a reduced
invertase/Suc synthase balance to alter the impact of respiratory
and/or membrane carbon flux on sugar signaling. Maize (Zea
mays L.) seedlings with 5-cm primary roots were exposed to
anoxic (0% [v/v] O2), hypoxic (3% [v/v]
O2), and aerobic conditions. Rapid repression of the
Ivr1 and Ivr2 maize invertases by low
oxygen was evident in root tips within 3 h at both the transcript
and activity levels. The speed and extent of this response increased
with the degree of oxygen deprivation and differed with genotypes. This
decrease in expression also contrasted markedly to that of other genes
for respiratory Suc metabolism, such as Suc synthases, which typically
increased or remained constant. Although previous work showed that the
contrasting effects of sugars on Suc synthase genes were reflected in
their regulation by hypoxia and anoxia, the same was not observed for the differentially sugar-responsive invertases. Theoretically advantageous reductions in the invertase/Suc synthase balance thus
resulted. However, where this response was extreme (an Oh43 inbred),
total sucrolytic capacity dropped below an apparent minimum and root
tip viability was reduced. Paradoxically, only Oh43 seedlings showed
survival levels >80% (versus <50%) after extreme, long-term stress,
suggesting a possible advantage for multiple means of reducing sink
activity. Overall, our results demonstrate a rapid change in the
regulation and balance of invertases and Suc synthases that could have
an immediate impact on limiting the extent of Suc cleavage and reducing
the extent of concomitant, hexose-based sugar signaling under low oxygen.
1
This research was supported by a grant from the
National Science Foundation and by the University of Florida Experiment
Station (journal series no. R-07084).
*
Corresponding author; e-mail kek{at}gnv.ifas.ufl.edu; fax
352-392-6479.
© 1999 American Society of Plant Physiologists
This article has been cited by other articles:
|
|
|
|
 
Y. Jin, D.-A. Ni, and Y.-L. Ruan
Posttranslational Elevation of Cell Wall Invertase Activity by Silencing Its Inhibitor in Tomato Delays Leaf Senescence and Increases Seed Weight and Fruit Hexose Level
PLANT CELL,
July 1, 2009;
21(7):
2072 - 2089.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. M. Ismail, E. S. Ella, G. V. Vergara, and D. J. Mackill
Mechanisms associated with tolerance to flooding during germination and early seedling growth in rice (Oryza sativa)
Ann. Bot.,
January 1, 2009;
103(2):
197 - 209.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
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]
|
|
|
|
|
|
|
M. C. Baier, A. Barsch, H. Kuster, and N. Hohnjec
Antisense Repression of the Medicago truncatula Nodule-Enhanced Sucrose Synthase Leads to a Handicapped Nitrogen Fixation Mirrored by Specific Alterations in the Symbiotic Transcriptome and Metabolome
Plant Physiology,
December 1, 2007;
145(4):
1600 - 1618.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
T. Fukao, K. Xu, P. C. Ronald, and J. Bailey-Serres
A Variable Cluster of Ethylene Response Factor-Like Genes Regulates Metabolic and Developmental Acclimation Responses to Submergence in Rice
PLANT CELL,
August 1, 2006;
18(8):
2021 - 2034.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
F. Liu, T. VanToai, L. P. Moy, G. Bock, L. D. Linford, and J. Quackenbush
Global Transcription Profiling Reveals Comprehensive Insights into Hypoxic Response in Arabidopsis
Plant Physiology,
March 1, 2005;
137(3):
1115 - 1129.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
H. Vigeolas, J. T. van Dongen, P. Waldeck, D. Huhn, and P. Geigenberger
Lipid Storage Metabolism Is Limited by the Prevailing Low Oxygen Concentrations within Developing Seeds of Oilseed Rape
Plant Physiology,
December 1, 2003;
133(4):
2048 - 2060.
[Abstract]
[Full Text]
|
|
|
|
|
|
|
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]
|
|
|
|
|
|
|
J. T. van Dongen, U. Schurr, M. Pfister, and P. Geigenberger
Phloem Metabolism and Function Have to Cope with Low Internal Oxygen
Plant Physiology,
April 1, 2003;
131(4):
1529 - 1543.
[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]
|
|
|
|
|
|
|
T. Roitsch, M. E. Balibrea, M. Hofmann, R. Proels, and A. K. Sinha
Extracellular invertase: key metabolic enzyme and PR protein
J. Exp. Bot.,
January 3, 2003;
54(382):
513 - 524.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
C. C. SUBBAIAH and M. M. SACHS
Molecular and Cellular Adaptations of Maize to Flooding Stress
Ann. Bot.,
January 2, 2003;
91(2):
119 - 127.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
O. Komina, Y. Zhou, G. Sarath, and R. Chollet
In Vivo and in Vitro Phosphorylation of Membrane and Soluble Forms of Soybean Nodule Sucrose Synthase
Plant Physiology,
August 1, 2002;
129(4):
1664 - 1673.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
H. Rolletschek, L. Borisjuk, M. Koschorreck, U. Wobus, and H. Weber
Legume embryos develop in a hypoxic environment
J. Exp. Bot.,
May 1, 2002;
53(371):
1099 - 1107.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. C. Long, W. Zhao, A. M. Rashotte, G. K. Muday, and S. C. Huber
Gravity-Stimulated Changes in Auxin and Invertase Gene Expression in Maize Pulvinal Cells
Plant Physiology,
February 1, 2002;
128(2):
591 - 602.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
W. S. da-Silva, G. L. Rezende, and A. Galina
Subcellular distribution and kinetic properties of cytosolic and non-cytosolic hexokinases in maize seedling roots: implications for hexose phosphorylation
J. Exp. Bot.,
June 1, 2001;
52(359):
1191 - 1201.
[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]
|
|
|
|
|
|
|
C. C. Subbaiah, K. P. Kollipara, and M. M. Sachs
A Ca2+-dependent cysteine protease is associated with anoxia-induced root tip death in maize
J. Exp. Bot.,
April 1, 2000;
51(345):
721 - 730.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
H. B. Smith
Sucrose Synthase and the Fruit of Its Labor
PLANT CELL,
December 1, 1999;
11(12):
2261 - 2262.
[Full Text]
|
|
|
|
|
