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Ectopic expression of mitochondrial gamma carbonic anhydrase 2 causes male sterility by anther indehiscence

Research output: Contribution to journalArticleResearchpeer review

Authors

  • Fernando Villarreal
  • Victoria Martín
  • Alejandro Colaneri
  • Nahuel González-Schain
  • Hans Peter Braun

Research Organisations

External Research Organisations

  • CONICET
  • Universidad Nacional de La Plata

Details

Original languageEnglish
Pages (from-to)471-485
Number of pages15
JournalPlant molecular biology
Volume70
Issue number4
Publication statusPublished - 27 Mar 2009

Abstract

Plant mitochondria include gamma-type carbonic anhydrases (γCAs) of unknown function. In Arabidopsis, the γCAs form a gene family of five members which all are attached to the NADH dehydrogenase complex (complex I) of the respiratory chain. Here we report a functional analysis of gamma carbonic anhydrase 2 (CA2). The gene encoding CA2 is constitutively expressed in all plant organs investigated but it is ten fold induced in flowers, particularly in tapetal tissue. Ectopic expression of CA2 in Arabidopsis causes male sterility in transgenic plants. In normal anther development, secondary thickenings of the endothecial cell wall cause anthers to open upon dehydration. Histological analyses revealed that abnormal secondary thickening prevents anther opening in 35S::CA2 transgenic plants. CA2 abundance in transgenic plants is increased 2-3 fold compared to wild-type plants as revealed by Western blotting analyses. Moreover, abundance of other members of the CA family, termed CA3 and CAL2, is increased in transgenic plants. Oxygen uptake measurements revealed that respiration in transgenic plants is mainly based on NADH reduction by the alternative NADH dehydrogenases present in plant mitochondria. Furthermore, the formation of reactive oxygen species (ROS) is very low in transgenic plants. We propose that reduction in ROS inhibits H2O2 dependent lignin polymerization in CA2 over-expressing plants, thereby causing male sterility.

Keywords

    Anther, Arabidopsis thaliana, Gamma carbonic anhydrases, Mitochondria, Reactive oxigen species

ASJC Scopus subject areas

Cite this

Ectopic expression of mitochondrial gamma carbonic anhydrase 2 causes male sterility by anther indehiscence. / Villarreal, Fernando; Martín, Victoria; Colaneri, Alejandro et al.
In: Plant molecular biology, Vol. 70, No. 4, 27.03.2009, p. 471-485.

Research output: Contribution to journalArticleResearchpeer review

Villarreal, F, Martín, V, Colaneri, A, González-Schain, N, Perales, M, Martín, M, Lombardo, C, Braun, HP, Bartoli, C & Zabaleta, E 2009, 'Ectopic expression of mitochondrial gamma carbonic anhydrase 2 causes male sterility by anther indehiscence', Plant molecular biology, vol. 70, no. 4, pp. 471-485. https://doi.org/10.1007/s11103-009-9484-z
Villarreal, F., Martín, V., Colaneri, A., González-Schain, N., Perales, M., Martín, M., Lombardo, C., Braun, H. P., Bartoli, C., & Zabaleta, E. (2009). Ectopic expression of mitochondrial gamma carbonic anhydrase 2 causes male sterility by anther indehiscence. Plant molecular biology, 70(4), 471-485. https://doi.org/10.1007/s11103-009-9484-z
Villarreal F, Martín V, Colaneri A, González-Schain N, Perales M, Martín M et al. Ectopic expression of mitochondrial gamma carbonic anhydrase 2 causes male sterility by anther indehiscence. Plant molecular biology. 2009 Mar 27;70(4):471-485. doi: 10.1007/s11103-009-9484-z
Villarreal, Fernando ; Martín, Victoria ; Colaneri, Alejandro et al. / Ectopic expression of mitochondrial gamma carbonic anhydrase 2 causes male sterility by anther indehiscence. In: Plant molecular biology. 2009 ; Vol. 70, No. 4. pp. 471-485.
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title = "Ectopic expression of mitochondrial gamma carbonic anhydrase 2 causes male sterility by anther indehiscence",
abstract = "Plant mitochondria include gamma-type carbonic anhydrases (γCAs) of unknown function. In Arabidopsis, the γCAs form a gene family of five members which all are attached to the NADH dehydrogenase complex (complex I) of the respiratory chain. Here we report a functional analysis of gamma carbonic anhydrase 2 (CA2). The gene encoding CA2 is constitutively expressed in all plant organs investigated but it is ten fold induced in flowers, particularly in tapetal tissue. Ectopic expression of CA2 in Arabidopsis causes male sterility in transgenic plants. In normal anther development, secondary thickenings of the endothecial cell wall cause anthers to open upon dehydration. Histological analyses revealed that abnormal secondary thickening prevents anther opening in 35S::CA2 transgenic plants. CA2 abundance in transgenic plants is increased 2-3 fold compared to wild-type plants as revealed by Western blotting analyses. Moreover, abundance of other members of the CA family, termed CA3 and CAL2, is increased in transgenic plants. Oxygen uptake measurements revealed that respiration in transgenic plants is mainly based on NADH reduction by the alternative NADH dehydrogenases present in plant mitochondria. Furthermore, the formation of reactive oxygen species (ROS) is very low in transgenic plants. We propose that reduction in ROS inhibits H2O2 dependent lignin polymerization in CA2 over-expressing plants, thereby causing male sterility.",
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AU - Villarreal, Fernando

AU - Martín, Victoria

AU - Colaneri, Alejandro

AU - González-Schain, Nahuel

AU - Perales, Mariano

AU - Martín, Mariana

AU - Lombardo, Cristina

AU - Braun, Hans Peter

AU - Bartoli, Carlos

AU - Zabaleta, Eduardo

N1 - Funding information: Acknowledgments This work was supported in part by ANPCyT (13432 and 31669) (Argentina), DAAD (Germany), ECOS-Sud, (A06B03) (France-Argentina). FV and MVM (CONICET, Argentina) are doctoral fellows and this work is part of their doctoral theses.

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Y1 - 2009/3/27

N2 - Plant mitochondria include gamma-type carbonic anhydrases (γCAs) of unknown function. In Arabidopsis, the γCAs form a gene family of five members which all are attached to the NADH dehydrogenase complex (complex I) of the respiratory chain. Here we report a functional analysis of gamma carbonic anhydrase 2 (CA2). The gene encoding CA2 is constitutively expressed in all plant organs investigated but it is ten fold induced in flowers, particularly in tapetal tissue. Ectopic expression of CA2 in Arabidopsis causes male sterility in transgenic plants. In normal anther development, secondary thickenings of the endothecial cell wall cause anthers to open upon dehydration. Histological analyses revealed that abnormal secondary thickening prevents anther opening in 35S::CA2 transgenic plants. CA2 abundance in transgenic plants is increased 2-3 fold compared to wild-type plants as revealed by Western blotting analyses. Moreover, abundance of other members of the CA family, termed CA3 and CAL2, is increased in transgenic plants. Oxygen uptake measurements revealed that respiration in transgenic plants is mainly based on NADH reduction by the alternative NADH dehydrogenases present in plant mitochondria. Furthermore, the formation of reactive oxygen species (ROS) is very low in transgenic plants. We propose that reduction in ROS inhibits H2O2 dependent lignin polymerization in CA2 over-expressing plants, thereby causing male sterility.

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KW - Arabidopsis thaliana

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KW - Mitochondria

KW - Reactive oxigen species

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ER -

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