CMS-G from Beta vulgaris ssp. maritima is maintained in natural populations despite containing an atypical cytochrome c oxidase

Abstract

While mitochondrial mutants of the respiratory machinery are rare and often lethal, cytoplasmic male sterility (CMS), a mitochondrially inherited trait that results in pollen abortion, is frequently encountered in wild populations. It generates a breeding system called gynodioecy. In ssp., a gynodioecious species, we found CMS-G to be widespread across the distribution range of the species. Despite the sequencing of the mitochondrial genome of CMS-G, the mitochondrial sterilizing factor causing CMS-G is still unknown. By characterizing biochemically CMS-G, we found that the expression of several mitochondrial proteins is altered in CMS-G plants. In particular, Cox1, a core subunit of the cytochrome oxidase (complex IV), is larger but can still assemble into complex IV. However, the CMS-G-specific complex IV was only detected as a stabilized dimer. We did not observe any alteration of the affinity of complex IV for cytochrome; however, in CMS-G, complex IV capacity is reduced. Our results show that CMS-G is maintained in many natural populations despite being associated with an atypical complex IV. We suggest that the modified complex IV could incur the associated cost predicted by theoretical models to maintain gynodioecy in wild populations.

Structural insights into the assembly and the function of the plant oxidative phosphorylation system

“…Moreover, although supercomplexes containing CIII 2 and CIV are usually weakly detected, they seem abundant in mistletoe that lacks CI (Senkler et al ., 2018) and Beta vulgaris ssp. maritima (Meyer et al ., 2018).…”

Two cytoplasmic male sterility phenotypes in beet (Beta vulgaris L.): implications of their simultaneous onset and divergent paths

“…Wild beets with G cytoplasm inhabit the Atlantic coast from France to Morocco (Meyer et al 2018), suggesting that the tness penalty rendered by the G cytoplasm is limited. As repeated backcrossing was successful, G cytoplasm does not affect female reproductive organs.…”

“…Mitochondrial morphology contrasts between the meiosis and the tetrad stages in both G-and Owen CMS. Therefore, the S-orf of the G cytoplasm (likely the variant cox1 with an NH 2terminal extension; Meyer et al (2018)) and the S-orf of the Owen cytoplasm (preSatp6) may simultaneously induce male sterility. During anther development, the demand for mitochondrial activity is apparently high in beet as N mitochondria are electron-dense, an indication of activated mitochondria (Sche er 1999) (Figs.…”

“…In addition, this wild beet mitochondrial genome has another defect unique to this mitochondrial type, namely a missense mutation in the translational initiation codon of cox1 that adds an NH 2 -terminal extension (Darraq et al 2011). A fusion protein of COXI with the extension was detected (Meyer et al 2018). Unlike Owen mitochondria, the atp6 in this mitochondrial type is identical to that of the N mitochondrial line (Darraq et al 2011).…”

The mitochondrialorf117Shagene desynchronizes pollen development and causes pollen abortion in the Arabidopsis Sha CMS

“…In the vast majority of cases, CMSs used in agriculture rely on naturally occurring mitochondrial CMS genes, most often cryptic in the species, subspecies, or cultivar of origin. Studies to identify CMS-causing genes and understand the mechanism(s) of pollen abortion have been conducted mainly in cultivated plants, but also in Mimulus (Case and Willis, 2008), Silene (Stone et al ., 2017), and wild beet (Meyer et al ., 2018). Mitochondrial CMS genes have been identified in more than 30 CMSs in approximately 20 species (reviewed by Chen & Liu (2014), Toriyama (2021), Xu et al .…”