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

Publikation: Beitrag in FachzeitschriftArtikelForschungPeer-Review

Autorschaft

  • Fernando Villarreal
  • Victoria Martín
  • Alejandro Colaneri
  • Nahuel González-Schain
  • Mariano Perales
  • Mariana Martín
  • Cristina Lombardo
  • Hans Peter Braun
  • Carlos Bartoli
  • Eduardo Zabaleta

Organisationseinheiten

Externe Organisationen

  • CONICET
  • Universidad Nacional de La Plata
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Details

OriginalspracheEnglisch
Seiten (von - bis)471-485
Seitenumfang15
FachzeitschriftPlant molecular biology
Jahrgang70
Ausgabenummer4
PublikationsstatusVeröffentlicht - 27 März 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.

ASJC Scopus Sachgebiete

Zitieren

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, Jahrgang 70, Nr. 4, 27.03.2009, S. 471-485.

Publikation: Beitrag in FachzeitschriftArtikelForschungPeer-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, Jg. 70, Nr. 4, S. 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 Mär 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 ; Jahrgang 70, Nr. 4. S. 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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author = "Fernando Villarreal and Victoria Mart{\'i}n and Alejandro Colaneri and Nahuel Gonz{\'a}lez-Schain and Mariano Perales and Mariana Mart{\'i}n and Cristina Lombardo and Braun, {Hans Peter} and Carlos Bartoli and Eduardo Zabaleta",
note = "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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T1 - Ectopic expression of mitochondrial gamma carbonic anhydrase 2 causes male sterility by anther indehiscence

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.

PY - 2009/3/27

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.

AB - 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.

KW - Anther

KW - Arabidopsis thaliana

KW - Gamma carbonic anhydrases

KW - Mitochondria

KW - Reactive oxigen species

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U2 - 10.1007/s11103-009-9484-z

DO - 10.1007/s11103-009-9484-z

M3 - Article

C2 - 19326245

AN - SCOPUS:67650594778

VL - 70

SP - 471

EP - 485

JO - Plant molecular biology

JF - Plant molecular biology

SN - 0167-4412

IS - 4

ER -

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