Biochemical and functional characterization of ORF138, a mitochondrial protein responsible for Ogura cytoplasmic male sterility in Brassiceae

Duroc, Yann; Gaillard, Catherine; Hiard, Sophie; Defrance, M.C.; Pelletier, Georges; Budar, Françoise

doi:10.1016/j.biochi.2005.05.009

Cited by 67 publications

(50 citation statements)

References 48 publications

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“…It was previously shown that the maize CMS-T gene urf13 also encodes a cytotoxic peptide (Dewey et al, 1988). In addition, the expression of CMS-associated genes orf552 from sunflower (Helianthus annuus) and orf138 from radish were also lethal to E. coli (Nakai et al, 1995;Duroc et al, 2005;Y.-G. Liu, unpublished data). Therefore, we suggest that many abnormal mitochondrial CMS genes, if not all, may encode cytotoxic proteins that can disrupt the development of male sporophytic and/or gametophytic cells.…”

Section: Discussion Abnormal Mitochondrial Orfs and Cmsmentioning

confidence: 97%

Cytoplasmic Male Sterility of Rice with Boro II Cytoplasm Is Caused by a Cytotoxic Peptide and Is Restored by Two Related PPR Motif Genes via Distinct Modes of mRNA Silencing

et al. 2006

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Cytoplasmic male sterility (CMS) and nucleus-controlled fertility restoration are widespread plant reproductive features that provide useful tools to exploit heterosis in crops. However, the molecular mechanism underlying this kind of cytoplasmicnuclear interaction remains unclear. Here, we show in rice (Oryza sativa) with Boro II cytoplasm that an abnormal mitochondrial open reading frame, orf79, is cotranscribed with a duplicated atp6 (B-atp6) gene and encodes a cytotoxic peptide. Expression of orf79 in CMS lines and transgenic rice plants caused gametophytic male sterility. Immunoblot analysis showed that the ORF79 protein accumulates specifically in microspores. Two fertility restorer genes, Rf1a and Rf1b, were identified at the classical locus Rf-1 as members of a multigene cluster that encode pentatricopeptide repeat proteins. RF1A and RF1B are both targeted to mitochondria and can restore male fertility by blocking ORF79 production via endonucleolytic cleavage (RF1A) or degradation (RF1B) of dicistronic B-atp6/orf79 mRNA. In the presence of both restorers, RF1A was epistatic over RF1B in the mRNA processing. We have also shown that RF1A plays an additional role in promoting the editing of atp6 mRNAs, independent of its cleavage function.

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Section: Discussion Abnormal Mitochondrial Orfs and Cmsmentioning

confidence: 97%

Cytoplasmic Male Sterility of Rice with Boro II Cytoplasm Is Caused by a Cytotoxic Peptide and Is Restored by Two Related PPR Motif Genes via Distinct Modes of mRNA Silencing

et al. 2006

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“…The cytotoxicity of several CMS-inducing proteins when expressed in E. coli strongly suggests that these proteins may be detrimental to mitochondrial respiration. [4][5][6] A few CMS-causing proteins were effectively shown to moderately impair respiratory chain activity or to form large pores within the mitochondrial inner membrane, but how this correlates with pollen abortion remains elusive. [7][8][9][10][11] Male fertility can be restored by the expression of nuclearencoded genes called restorer of fertility (Rf ), which re-establish partial to normal pollen production to plants carrying a corresponding sterility-inducing cytoplasm.…”

Section: The Rf and Rf-like Ppr In Higher Plants A Fast-evolving Submentioning

confidence: 99%

The Rf and Rf-like PPR in higher plants, a fast-evolving subclass of PPR genes

Dahan¹,

Mireau²

2013

RNA Biology

130

110

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“…In contrast with many sterilityinducing proteins, ORF138 is not a chimeric polypeptide composed of fragments of conventional mitochondrial proteins. The ORF138 protein was recently shown to reside in the inner membrane of mitochondria, likely assembled as a homopolymer, but the mechanism by which it interferes with pollen production is still unclear (Grelon et al, 1994;Duroc et al, 2005). Nevertheless, because the expression of orf138 was shown to strongly inhibit bacterial growth, ORF138 is presumed to produce a certain level of toxicity toward mitochondrial activity in the tapetum of anthers (Duroc et al, 2005).…”

Section: Introductionmentioning

confidence: 99%

“…The ORF138 protein was recently shown to reside in the inner membrane of mitochondria, likely assembled as a homopolymer, but the mechanism by which it interferes with pollen production is still unclear (Grelon et al, 1994;Duroc et al, 2005). Nevertheless, because the expression of orf138 was shown to strongly inhibit bacterial growth, ORF138 is presumed to produce a certain level of toxicity toward mitochondrial activity in the tapetum of anthers (Duroc et al, 2005). Several groups recently succeeded in cloning the Ogura CMS restorer locus, Rfo, in radish by positional cloning (Brown et al, 2003;Desloire et al, 2003;Koizuka et al, 2003).…”

Section: Introductionmentioning

confidence: 99%

Characterization of Raphanus sativus Pentatricopeptide Repeat Proteins Encoded by the Fertility Restorer Locus for Ogura Cytoplasmic Male Sterility

et al. 2008

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Cytoplasmic male sterility is a maternally inherited trait in higher plants that prevents the production of functional pollen. Ogura cytoplasmic male sterility in radish (Raphanus sativus) is regulated by the orf138 mitochondrial locus. Male fertility can be restored when orf138 accumulation is suppressed by the nuclear Rfo locus, which consists of three genes putatively encoding highly similar pentatricopeptide repeat proteins (PPR-A, -B, and -C). We produced transgenic rapeseed (Brassica napus) plants separately expressing PPR-A and PPR-B and demonstrated that both encoded proteins accumulated preferentially in the anthers of young flower buds. Immunodetection of ORF138 showed that, unlike PPR-B, PPR-A had no effect on the synthesis of the sterility protein. Moreover, immunolocalization experiments indicated that complete elimination of ORF138 from the tapetum of anthers correlated with the restoration of fertility. Thus, the primary role of PPR-B in restoring fertility is to inhibit ORF138 synthesis in the tapetum of young anthers. In situ hybridization experiments confirmed, at the cellular level, that PPR-B has no effect on the accumulation of orf138 mRNA. Lastly, immunoprecipitation experiments demonstrated that PPR-B, but not PPR-A, is associated with the orf138 RNA in vivo, linking restoration activity with the ability to directly or indirectly interact with the orf138 RNA. Together, our data support a role for PPR-B in the translational regulation of orf138 mRNA.

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Biochemical and functional characterization of ORF138, a mitochondrial protein responsible for Ogura cytoplasmic male sterility in Brassiceae

Cited by 67 publications

References 48 publications

Cytoplasmic Male Sterility of Rice with Boro II Cytoplasm Is Caused by a Cytotoxic Peptide and Is Restored by Two Related PPR Motif Genes via Distinct Modes of mRNA Silencing

Cytoplasmic Male Sterility of Rice with Boro II Cytoplasm Is Caused by a Cytotoxic Peptide and Is Restored by Two Related PPR Motif Genes via Distinct Modes of mRNA Silencing

The Rf and Rf-like PPR in higher plants, a fast-evolving subclass of PPR genes

Characterization of Raphanus sativus Pentatricopeptide Repeat Proteins Encoded by the Fertility Restorer Locus for Ogura Cytoplasmic Male Sterility

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