Male Sterility-Inducing Mitochondrial Genomes: How Do They Differ?

Abstract

Twenty-nine mitochondrial genomes from 19 angiosperm species have been completely sequenced and have been found to vary in genome size and gene content. Seven of these mitochondrial genomes are known to induce cytoplasmic male sterility (CMS), and thus can be utilized for hybrid seed production or the prevention of pollen dispersal. Genome rearrangement frequently is observed in male sterility (MS)-inducing mitochondria, but it also occurs as part of the normal inter- or intraspecific variation in male fertile (MF) mitochondria. Sequence analyses have revealed that the repertoire of genuine genes is indistinguishable between MS-inducing and MF mitochondria. Deleterious mutations appear to be rare in MS-inducing mitochondria, which may be consistent with the lack of systemic manifestation of CMS. On the other hand, several nucleotide substitutions remain to be investigated for their potential mild effects. Various mitochondrial open reading frames (ORFs) are associated with CMS (CMS-ORFs). There are some common but not strict features shared by CMS-ORFs such as their uniqueness to the CMS mitochondrial genome, their association with genes for ATPase subunits, and the hydrophobic nature of their putative translation products. It should be noted that some CMS-ORFs do not satisfy all of these criteria, and ORFs that satisfy these criteria are not necessarily associated with CMS. Therefore, it is difficult to infer the capability of MS induction of mitochondrial genomes solely from their nucleotide sequences. Morphological, physiological, and molecular biological studies suggest that multiple mechanisms cause CMS. Nuclear genes that suppress CMS have been identified. Post-transcriptional suppression of CMS-ORFs mediated by a certain class of RNA binding proteins (pentatrico peptide repeat proteins) is the predominant mechanism of fertility restoration. On the other hand, CMS suppression that is not associated with post-transcriptional suppression of CMS-ORFs has also been reported, suggesting that various types of gene products are involved in fertility restoration.

Keywords:

• cytoplasmic male sterility
• fertility restorer gene
• nuclear– mitochondrial interaction
• mitochondrial genome
• plant mitochondria

ACKNOWLEDGMENTS

The authors wish to thank Dr. Françoise Budar for reviewing the manuscript, and Dr. Sally Mackenzie, Dr. Kinya Toriyama and Dr. Tomohiko Kazama for providing valuable information. This work was supported in part by Grants-in-Aid for Scientific Research from the Ministry of Education, Culture, Sports, Science, and Technology and the Program for Promotion of Basic and Applied Research for Innovation in Bio-oriented Industry (BRAIN).

Referee: Dr. Françoise Budar, INRA, Station de Genetique et d’Amelioration des Plantes, 78026 Versailles, France.

This review is dedicated to the memory of Dr. Toshiro Kinoshita.

Notes

1. After acceptance of the manuscript, the following mitochondrial sequences have been available: Mung bean, HM367685, Alverson et al., Plosone 2011, 6: e16404 wild beets, FP885845, FQ014226, and FQ378026, Darraq et al., Genome Biology and Evolution doi: 10:1093/gbe/evr042.