Cold-induced repression of the rice anther-specific cell wall invertase gene OSINV4 is correlated with sucrose accumulation and pollen sterility

Sandra N. Oliver, Joost T. Van Dongen, Sanjeev C. Alfred, Ezaz A. Mamun, Xiaochun Zhao, Hargurdeep S. Saini, Sussan F. Fernandes, Christopher L. Blanchard, Bruce G. Sutton, Peter Geigenberger, Elizabeth S. Dennis, Rudy Dolferus

Research output: Contribution to journalArticle

161 Citations (Scopus)

Abstract

Low temperatures during rice (Oryza sativa L.) pollen development cause pollen sterility and decreased grain yield. We show that the time of highest sensitivity to cold coincides with the time of peak tapetal activity: the transition of the tetrad to early uni-nucleate stage (young microspore, YM stage). Low temperatures at this stage of pollen development result in an accumulation of sucrose in the anthers, accompanied by decreased activity of cell wall bound acid invertase and depletion of starch in mature pollen grains. Expression analysis of two cell wall (OSINV1, 4) and one vacuolar (OSINV2) acid invertase genes showed that OSINV4 is anther-specific and down-regulated by cold treatment. OSINV4 is transiently expressed in the tapetum cell layer at the YM stage, and later from the early binucleate stage in the maturing microspores. The down-regulation of OSINV4 expression in the tapetum at YM may cause a disruption in hexose production and starch formation in the pollen grains. In a cold-tolerant cultivar, OSINV4 expression was not reduced by cold; sucrose did not accumulate in the anthers and starch formation in the pollen grains was not affected.

Original languageEnglish
Pages (from-to)1534-1551
Number of pages18
JournalPlant, Cell and Environment
Volume28
Issue number12
DOIs
Publication statusPublished - 1 Dec 2005
Externally publishedYes

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beta-Fructofuranosidase
beta-fructofuranosidase
Pollen
anthers
Cell Wall
Infertility
Sucrose
cell walls
pollen
sucrose
rice
Starch
Genes
genes
starch
microspores
Temperature
Hexoses
hexoses
Oryza

Cite this

Oliver, Sandra N. ; Van Dongen, Joost T. ; Alfred, Sanjeev C. ; Mamun, Ezaz A. ; Zhao, Xiaochun ; Saini, Hargurdeep S. ; Fernandes, Sussan F. ; Blanchard, Christopher L. ; Sutton, Bruce G. ; Geigenberger, Peter ; Dennis, Elizabeth S. ; Dolferus, Rudy. / Cold-induced repression of the rice anther-specific cell wall invertase gene OSINV4 is correlated with sucrose accumulation and pollen sterility. In: Plant, Cell and Environment. 2005 ; Vol. 28, No. 12. pp. 1534-1551.
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abstract = "Low temperatures during rice (Oryza sativa L.) pollen development cause pollen sterility and decreased grain yield. We show that the time of highest sensitivity to cold coincides with the time of peak tapetal activity: the transition of the tetrad to early uni-nucleate stage (young microspore, YM stage). Low temperatures at this stage of pollen development result in an accumulation of sucrose in the anthers, accompanied by decreased activity of cell wall bound acid invertase and depletion of starch in mature pollen grains. Expression analysis of two cell wall (OSINV1, 4) and one vacuolar (OSINV2) acid invertase genes showed that OSINV4 is anther-specific and down-regulated by cold treatment. OSINV4 is transiently expressed in the tapetum cell layer at the YM stage, and later from the early binucleate stage in the maturing microspores. The down-regulation of OSINV4 expression in the tapetum at YM may cause a disruption in hexose production and starch formation in the pollen grains. In a cold-tolerant cultivar, OSINV4 expression was not reduced by cold; sucrose did not accumulate in the anthers and starch formation in the pollen grains was not affected.",
keywords = "Carbohydrate metabolism, Cold stress, Invertase, Pollen sterility, Rice, Tapetum",
author = "Oliver, {Sandra N.} and {Van Dongen}, {Joost T.} and Alfred, {Sanjeev C.} and Mamun, {Ezaz A.} and Xiaochun Zhao and Saini, {Hargurdeep S.} and Fernandes, {Sussan F.} and Blanchard, {Christopher L.} and Sutton, {Bruce G.} and Peter Geigenberger and Dennis, {Elizabeth S.} and Rudy Dolferus",
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Oliver, SN, Van Dongen, JT, Alfred, SC, Mamun, EA, Zhao, X, Saini, HS, Fernandes, SF, Blanchard, CL, Sutton, BG, Geigenberger, P, Dennis, ES & Dolferus, R 2005, 'Cold-induced repression of the rice anther-specific cell wall invertase gene OSINV4 is correlated with sucrose accumulation and pollen sterility', Plant, Cell and Environment, vol. 28, no. 12, pp. 1534-1551. https://doi.org/10.1111/j.1365-3040.2005.01390.x

Cold-induced repression of the rice anther-specific cell wall invertase gene OSINV4 is correlated with sucrose accumulation and pollen sterility. / Oliver, Sandra N.; Van Dongen, Joost T.; Alfred, Sanjeev C.; Mamun, Ezaz A.; Zhao, Xiaochun; Saini, Hargurdeep S.; Fernandes, Sussan F.; Blanchard, Christopher L.; Sutton, Bruce G.; Geigenberger, Peter; Dennis, Elizabeth S.; Dolferus, Rudy.

In: Plant, Cell and Environment, Vol. 28, No. 12, 01.12.2005, p. 1534-1551.

Research output: Contribution to journalArticle

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T1 - Cold-induced repression of the rice anther-specific cell wall invertase gene OSINV4 is correlated with sucrose accumulation and pollen sterility

AU - Oliver, Sandra N.

AU - Van Dongen, Joost T.

AU - Alfred, Sanjeev C.

AU - Mamun, Ezaz A.

AU - Zhao, Xiaochun

AU - Saini, Hargurdeep S.

AU - Fernandes, Sussan F.

AU - Blanchard, Christopher L.

AU - Sutton, Bruce G.

AU - Geigenberger, Peter

AU - Dennis, Elizabeth S.

AU - Dolferus, Rudy

PY - 2005/12/1

Y1 - 2005/12/1

N2 - Low temperatures during rice (Oryza sativa L.) pollen development cause pollen sterility and decreased grain yield. We show that the time of highest sensitivity to cold coincides with the time of peak tapetal activity: the transition of the tetrad to early uni-nucleate stage (young microspore, YM stage). Low temperatures at this stage of pollen development result in an accumulation of sucrose in the anthers, accompanied by decreased activity of cell wall bound acid invertase and depletion of starch in mature pollen grains. Expression analysis of two cell wall (OSINV1, 4) and one vacuolar (OSINV2) acid invertase genes showed that OSINV4 is anther-specific and down-regulated by cold treatment. OSINV4 is transiently expressed in the tapetum cell layer at the YM stage, and later from the early binucleate stage in the maturing microspores. The down-regulation of OSINV4 expression in the tapetum at YM may cause a disruption in hexose production and starch formation in the pollen grains. In a cold-tolerant cultivar, OSINV4 expression was not reduced by cold; sucrose did not accumulate in the anthers and starch formation in the pollen grains was not affected.

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KW - Carbohydrate metabolism

KW - Cold stress

KW - Invertase

KW - Pollen sterility

KW - Rice

KW - Tapetum

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