September 30, 2020
Mitochondria are the cellular site of critical pathways for bioenergetics and central metabolism. They are also an important source biosynthetic intermediates and cellular signaling molecules.While mitochondria carry a genome essential to these functions, the coordinate action of over2,000 nuclear genes is also required. In the seed plants, mitochondrial-nuclear genome interactions are exemplified by the mitochondria-encoded cytoplasmic male sterility (CMS)trait, which can be reversed by nuclear restorer-of-fertility genes. Many, independently evolved CMS systems have been studied to gain insights into these genetic interactions. Among these,the S type of CMS (CMS-S) in maize is unique in that a mitochondria-encoded pollen collapse phenotype can be reversed by multiple, independent, nuclear restorer-of-fertility lethal (rfl)mutations that also condition a homozygous-lethal seed phenotype. The molecular and cellular features of these phenotypes were investigated to understand mitochondrial contributions to maize reproduction. CMS-S pollen collapse was characterized by features typical of mitochondria-signaled programmed cell death in animals. Rescue of CMS-S pollen, surprisingly,occurred by limiting pollen mitochondrial gene expression. A collection of rfl mutations was developed in a Mutator (Mu) transposon background and two rfl mutations were shown to disrupted nuclear genes encoding mitochondrial ribosomal proteins. These mutations reduced the accumulation of mitochondria-encoded respiratory proteins in CMS-S rfl pollen to less than 25% of normal (N) cytoplasm controls. While CMS-S rfl pollen can effect fertilization in the absence of competition from non-mutant pollen, 75-95% of pollinations were accomplished by pollen carrying the non-mutant (+) allele in crosses of N-cytoplasm rfl /+ pollen parents. Maize pollen function is therefore flexible with respect to requirements for cytochrome pathway respiration, but fertility is enhanced in the presence of a wild-type cytochrome pathway. Light microscopy revealed early developmental arrest of rfl mutant embryos and endosperms compared to wild-type siblings, consistent with more stringent requirements for cytochrome pathway respiration during maize seed development.