Interactions of Mitochondrial and Nuclear Genes That Affect Male Gametophyte Development

Abstract

Apart from their agronomic importance in hybrid seed production, mutations that encode cytoplasmic male sterility (CMS) provide a means to probe the role of the mitochondrion in reproductive development. Fertility restorers are examples of nuclear genes that affect cytoplasmic gene expression, and their identification can illuminate the interactions between the two genomes. In this review, we consider what is known about the nature of mutant mitochondrial loci that disrupt pollen development, focusing on their creation through recombination events that have often involved ATP synthase subunit genes. We also discuss how the mutant mitochondrial genes' function or expression is affected by the presence of nuclear fertility restorers and the information gained about these nuclear genes through recent map-based cloning efforts. We also describe the evidence that mitochondrial gene expression can affect the function of nuclear gene products that control floral development. In natural plant populations, the most widespread manifestation of disturbed mitochondrial–nuclear interaction is altered floral development, particularly the loss of the male gametophyte. A substantial fraction of species exhibit populations that include both hermaphroditic (male-fertile) and functional female (male-sterile) individuals, a situation termed gynodioecy by Darwin (discussed by Budar and Pelletier, 2001; Charlesworth, 2002). Although the genetics of the male sterility has not yet been determined in many known gynodioecious species (reviewed by Kaul, 1988), a typical finding is cytoplasmic inheritance of male sterility and restoration of fertility by one or more nuclear alleles. Although non-Mendelian traits in plants could be encoded by either cytoplasmic genome, in all cases to date in which such a sterility-encoding gene has been identified in an organelle, the mitochondrion was the location of the mutation that disrupts pollen development. CMS forces outcrossing; however, the potential advantage of outcrossing does not appear to explain completely the success of the gynodioecious reproductive strategy. Quite possibly, the selective advantages and disadvantages of a mixture of female and hermaphroditic plants may vary between individual genera (Kaul, 1988; Budar et al., 2003). For some species, there is sound evidence that female plants produce more seeds, perhaps because of reduced energetic investment in male floral organs. Indeed, in many species, CMS halts pollen development at a very early developmental stage, potentially saving considerable output of resources. However, no increase in seed set in females has been detected in some species. Furthermore, in other species, the disruption occurs late in development, after considerable energy has been expended. Such a finding raises the question of whether cytoplasmic genes that confer male sterility may somehow confer a survival advantage to individuals, so that more CMS plants reproduce, even if individuals do not produce more seeds. The potential adaptive value of gynodioecy and its impact on the population structure and evolution of species remain topics for further inquiry (recently reviewed by Charlesworth, 2002; Budar et al., 2003; Saur Jacobs and Wade, 2003). Understanding the nature of CMS-encoding cytoplasmic genomes and the nuclear genes that suppress male sterility may be instructive in creating models for the maintenance of the balance of female and hermaphroditic plants in natural plant populations. In addition to the naturally occurring CMS that has been observed in wild plant populations, the trait has been synthesized a of in which the nuclear of one species has been the cytoplasmic of The of pollen development that a of is termed male Quite the finding of CMS after from the of cytoplasmic genes expression is by nuclear genes in the species. However, there also is evidence that the of can be perhaps creating cytoplasmic a of in cytoplasmic and (reviewed by and CMS individuals that and also have after individuals often are plant populations in and are detected The of CMS and fertility restoration have been by plant to hybrid of a of species and seed from a plant from For species in which the is a or a the of does not the or value of the hybrid and the of pollen may even be or seed is the from a hybrid however, the presence of a nuclear fertility is to confer on the hybrid on the for species, the of these genes are to of or The of CMS-encoding and fertility restorers a in plant Furthermore, to the of genes can the to for hybrid the that encode an is to cytoplasmic genomes in and CMS a the has not been between two often may and have no is is to CMS and are of that have from known CMS such to the of of and is to in or events have been A for mitochondrial is to the of a the In most species, and mitochondrial genomes are and both are through the has a means to the of and and to mitochondrial genomes (reviewed by of between CMS and has that fertility does not the In a