Higher plant mitochondria

Over the past 20 years, researchers investigating the mitochondria of plants have been astonished by the phenomenal variation these organelles display relative to their mammalian and fungal counterparts. Plant mitochondria have evolved distinct strategies for genome maintenance, genetic decoding, gene regulation, and organelle segregation. Their physiological and biochemical functions have similarly evolved to meet the specific demands of photosynthetic organisms “rooted” in place. Unfortunately, making sense of the great number of variations inherent to plant mitochondria has been a slow process. This has been made more difficult by the fact that geneticists and biochemists have traditionally formed two distinct and often poorly communicating research groups in mitochondrial biology. The productive merging of these two bodies of information has begun only recently. With this review, we attempt to provide perspective to the recent developments in this field and their implications for our understanding of organellar biogenesis and mitochondrial integration into whole-plant physiology. Mitochondrial genomes encode only a fraction of the genetic information required for their biogenesis and function; the vast majority is nuclear derived. Consequently, it can be assumed that the large number of unique genetic and biochemical features displayed in plant mitochondria arose in the context of a nuclear–mitochondrial coevolution particular to the plant kingdom. Plant mitochondria are compelled to coordinate gene functions with other organelles, including plastids. Likewise, tissues demanding high rates of metabolism during reproduction and fruiting, or in the case of nitrogen fixation, requiring low oxygen concentrations, represent processes peculiar to plants. Due to an inability to mobilize so as to avoid environmental stresses, plants have evolved unique adaptations to stress, some of which involve the mitochondrion. For some species, these unusual evolutionary demands may have been exacerbated by thousands of years of genetic manipulation by breeders. Given this perspective, it is not so surprising that nuclear–mitochondrial interactions within the plant kingdom are highly specialized and unusual. Organelles communicate by means of essential polypeptides and bidirectional information flow, allowing for organogenesis and responses to the environment. In plants, regulatory models from bacterial energy transduction have been extended to photosynthesis in plastids (Allen, 1993; Allen et al., 1995), including regulation by redox poise (Escoubas et al., 1995) and translation of the chloroplast-encoded proteins (Danon and Mayfield, 1994; Yohn et al., 1996). Similarly, yeast has served as an excellent model system for nuclear–mitochondrial interaction (reviewed in Poyton and McEwen, 1996). In studies concerning plant mitochondrial– nuclear interaction—where a third powerful organelle, the chloroplast, is present—we have basic genetic paradigms such as cytoplasmic male sterility (CMS), nonchromosomal stripe mutations, and nuclear mutations affecting heritable phenotypes. However, a dynamic model for plant mitochondrial–nuclear interaction, one differentially responding to environmental and growth challenges, has not risen above a rudimentary level. Such model systems will likely be crucial to the in-depth investigation of mitochondrial integration with overall plant cellular processes. In this review, we describe the current understanding of specialized genetic and biochemical features unique to plant mitochondria. We also address the more speculative but exciting aspects of interorganellar interaction, namely, the recent efforts to identify molecules mediating nuclear–mitochondrial and plastid–mitochondrial communication.