Selective transcriptional down-regulation of anther invertases precedes the failure of pollen development in water-stressed wheat

P. K. Koonjul, J. S. Minhas, C. Nunes, I. S. Sheoran, H. S. Saini

Research output: Contribution to journalArticle

92 Citations (Scopus)

Abstract

Water deficit during male meiosis in wheat (Triticum aestivum L.) causes pollen sterility. With a view to identifying the internal trigger for this failure, it was found that water stress specifically impairs the activities of vacuolar and cell-wall invertases in anthers prior to the arrest of pollen development. The enzymes are affected only when water deficit occurs around meiosis. Three invertase cDNAs, two encoding the cell-wall (Ivr1, Ivr3) and one the vacuolar (Ivr5) isoform, were isolated from an anther cDNA library. RNA gelblot analysis using floral organs of well-watered plants revealed that these genes were expressed preferentially, though not exclusively, in anthers. Semi-quantitative RT-PCR demonstrated that transitory water deficit during meiosis selectively down-regulated the transcription of two of the three genes, one encoding the vacuolar (Ivr5) and the other a cell-wall (Ivr1) isoform, without affecting the Ivr3 message. Their expression did not recover upon resumption of watering. Another homologue of Ivr1 was also down-regulated, but only during the post-stress period. The stress effects on invertase transcripts were consistent with those on the developmental profiles of the corresponding enzyme activities. In situ hybridization revealed that the stress-sensitive invertase genes, unlike an insensitive one, were expressed within the microspores. No evidence for an invertase inhibitor under stress was found. Together the results show that the decline in invertase activity is probably regulated primarily at the transcriptional level in a gene- and cell-specific manner.

Original languageEnglish
Pages (from-to)179-190
Number of pages12
JournalJournal of Experimental Botany
Volume56
Issue number409
DOIs
Publication statusPublished - 1 Jan 2005
Externally publishedYes

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beta-Fructofuranosidase
beta-fructofuranosidase
Pollen
anthers
Triticum
Down-Regulation
pollen
wheat
Water
Meiosis
meiosis
Cell Wall
water
cell walls
Protein Isoforms
genes
Genes
Plant Genes
microspores
Enzymes

Cite this

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title = "Selective transcriptional down-regulation of anther invertases precedes the failure of pollen development in water-stressed wheat",
abstract = "Water deficit during male meiosis in wheat (Triticum aestivum L.) causes pollen sterility. With a view to identifying the internal trigger for this failure, it was found that water stress specifically impairs the activities of vacuolar and cell-wall invertases in anthers prior to the arrest of pollen development. The enzymes are affected only when water deficit occurs around meiosis. Three invertase cDNAs, two encoding the cell-wall (Ivr1, Ivr3) and one the vacuolar (Ivr5) isoform, were isolated from an anther cDNA library. RNA gelblot analysis using floral organs of well-watered plants revealed that these genes were expressed preferentially, though not exclusively, in anthers. Semi-quantitative RT-PCR demonstrated that transitory water deficit during meiosis selectively down-regulated the transcription of two of the three genes, one encoding the vacuolar (Ivr5) and the other a cell-wall (Ivr1) isoform, without affecting the Ivr3 message. Their expression did not recover upon resumption of watering. Another homologue of Ivr1 was also down-regulated, but only during the post-stress period. The stress effects on invertase transcripts were consistent with those on the developmental profiles of the corresponding enzyme activities. In situ hybridization revealed that the stress-sensitive invertase genes, unlike an insensitive one, were expressed within the microspores. No evidence for an invertase inhibitor under stress was found. Together the results show that the decline in invertase activity is probably regulated primarily at the transcriptional level in a gene- and cell-specific manner.",
keywords = "Gene expression, Invertase, Male sterility, Pollen development, Reproduction, Sugar metabolism, Water stress",
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Selective transcriptional down-regulation of anther invertases precedes the failure of pollen development in water-stressed wheat. / Koonjul, P. K.; Minhas, J. S.; Nunes, C.; Sheoran, I. S.; Saini, H. S.

In: Journal of Experimental Botany, Vol. 56, No. 409, 01.01.2005, p. 179-190.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Selective transcriptional down-regulation of anther invertases precedes the failure of pollen development in water-stressed wheat

AU - Koonjul, P. K.

AU - Minhas, J. S.

AU - Nunes, C.

AU - Sheoran, I. S.

AU - Saini, H. S.

PY - 2005/1/1

Y1 - 2005/1/1

N2 - Water deficit during male meiosis in wheat (Triticum aestivum L.) causes pollen sterility. With a view to identifying the internal trigger for this failure, it was found that water stress specifically impairs the activities of vacuolar and cell-wall invertases in anthers prior to the arrest of pollen development. The enzymes are affected only when water deficit occurs around meiosis. Three invertase cDNAs, two encoding the cell-wall (Ivr1, Ivr3) and one the vacuolar (Ivr5) isoform, were isolated from an anther cDNA library. RNA gelblot analysis using floral organs of well-watered plants revealed that these genes were expressed preferentially, though not exclusively, in anthers. Semi-quantitative RT-PCR demonstrated that transitory water deficit during meiosis selectively down-regulated the transcription of two of the three genes, one encoding the vacuolar (Ivr5) and the other a cell-wall (Ivr1) isoform, without affecting the Ivr3 message. Their expression did not recover upon resumption of watering. Another homologue of Ivr1 was also down-regulated, but only during the post-stress period. The stress effects on invertase transcripts were consistent with those on the developmental profiles of the corresponding enzyme activities. In situ hybridization revealed that the stress-sensitive invertase genes, unlike an insensitive one, were expressed within the microspores. No evidence for an invertase inhibitor under stress was found. Together the results show that the decline in invertase activity is probably regulated primarily at the transcriptional level in a gene- and cell-specific manner.

AB - Water deficit during male meiosis in wheat (Triticum aestivum L.) causes pollen sterility. With a view to identifying the internal trigger for this failure, it was found that water stress specifically impairs the activities of vacuolar and cell-wall invertases in anthers prior to the arrest of pollen development. The enzymes are affected only when water deficit occurs around meiosis. Three invertase cDNAs, two encoding the cell-wall (Ivr1, Ivr3) and one the vacuolar (Ivr5) isoform, were isolated from an anther cDNA library. RNA gelblot analysis using floral organs of well-watered plants revealed that these genes were expressed preferentially, though not exclusively, in anthers. Semi-quantitative RT-PCR demonstrated that transitory water deficit during meiosis selectively down-regulated the transcription of two of the three genes, one encoding the vacuolar (Ivr5) and the other a cell-wall (Ivr1) isoform, without affecting the Ivr3 message. Their expression did not recover upon resumption of watering. Another homologue of Ivr1 was also down-regulated, but only during the post-stress period. The stress effects on invertase transcripts were consistent with those on the developmental profiles of the corresponding enzyme activities. In situ hybridization revealed that the stress-sensitive invertase genes, unlike an insensitive one, were expressed within the microspores. No evidence for an invertase inhibitor under stress was found. Together the results show that the decline in invertase activity is probably regulated primarily at the transcriptional level in a gene- and cell-specific manner.

KW - Gene expression

KW - Invertase

KW - Male sterility

KW - Pollen development

KW - Reproduction

KW - Sugar metabolism

KW - Water stress

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U2 - 10.1093/jxb/eri018

DO - 10.1093/jxb/eri018

M3 - Article

VL - 56

SP - 179

EP - 190

JO - Journal of Experimental Botany

JF - Journal of Experimental Botany

SN - 0022-0957

IS - 409

ER -