Arabidopsis variegation mutants.

Variegation mutants have been defined as “any plant that develops patches of different colors in its vegetative parts” (Kirk and Tilney-Bassett, 1978). Some of the most common variegations have green and white (or yellow) sectors in normally-green tissues and organs of the plant. Whereas cells in the green sectors typically contain normal-appearing chloroplasts, cells in the white (or yellow) sectors contain plastids that are deficient in chlorophyll and/or carotenoid pigments. These plastids appear to be blocked at various steps of chloroplast biogenesis because they frequently lack organized internal membrane structures and/or contain only rudimentary lamellae. Despite their widespread occurrence, relatively few variegations have been characterized at the molecular level. Variegation mutants have played a prominent role in the history of genetics (reviewed by Granick, 1955; Kirk and Tilney-Bassett, 1978). As a notable example, the finding that transmission of the variegation trait does not always obey Mendel's laws led to the discovery of non-Mendelian inheritance in the early 1900's. Whereas variegations have long been associated with differences in plastid form and function, it was not possible to gain insight into the molecular basis of this phenomenon until the 1960's and early 1970's, when compelling molecular evidence was presented that mitochondria and chloroplasts contain their own DNA and protein synthesis systems, and that organellar proteins are the products of genes in the chloroplast and mitochondrion, as well as the nucleus (reviewed by Bogorad, 1981). Nuclear-organelle interactions Nuclear DNA-encoded proteins that are destined for chloroplasts and mitochondria are translated as precursors on 80S ribosomes in the cytosol and transported into the organelle post-translationally, whereas proteins encoded in the mitochondrial and plastid genomes are translated on prokaryotic-like 70S ribosomes in the organelle itself (reviewed by Goldschmidt-Clermont, 1998; Leon et al., 1998). Mitochondria and plastids are derived from prokaryotic endosymbionts, and during the process of symbiogenesis most of the genes of the symbiont were lost or transferred to the host genome (Gray, 1992; Doolittle, 1998; Cavalier-Smith, 2000). For instance, current-day plastid genomes in higher plants code for less than 100 of the estimated 1900 to 2500 proteins in a typical chloroplast (Abdallah et al., 2000; Martin and Herrmann, 1998). Plastid and mitochondrial genomes are polyploid, and in higher plant cells they are dispersed among many plastids and mitochondria. For example, a typical mesophyll cell contains from 1,000 to 10,000 identical plastid DNAs distributed among 100 or more chloroplasts (Bendich, 1987). It is thought that the dispersal of genes for plastid and mitochondrial proteins between two different compartments was the central driving force that led to the evolution of mechanisms that integrate nuclear and organellar gene expression (reviewed by Bogorad, 1981). A contributing factor might also have been the vast disparity in copy number between genes in the nuclear and organellar compartments. Much of the regulatory traffic between the nucleus and the organelle is anterograde, i.e., from the nucleus to the organelle, in the form of nuclear gene products that control the transcription and translation of mitochondrial and plastid genes (reviewed by Goldschmidt-Clermont, 1998; Leon et al., 1998). Yet, much of this traffic is also retrograde, i.e., from the organelle to the nucleus (reviewed by Oelmuller, 1989; Taylor, 1989; Mayfield, 1990; Susek and Chory, 1992; Gray et al., 1995; Hess et al., 1997; Rodermel, 2001). Perhaps the best understood examples of retrograde trafficking in plants involve the transcriptional regulation of nuclear genes for photosynthetic proteins by plastid-to-nucleus signaling mechanisms initiated by a variety of “plastid signals” (reviewed by Rodermel, 2001). The plastid signals identified to date are intermediates or by-products of photosynthetic metabolism. Yet, poorly understood retrograde signals also control the expression of nuclear genes for a number of non-plastid proteins (reviewed by Oelmuller, 1989; Barak et al., 2001), as well as the transcription of mitochondrial genes, cell differentiation and leaf morphogenesis (reviewed by Hess et al., 1997; Hedtke et al., 1999; Rodermel, 2001). Consequently, plastid-to-nucleus signaling plays a central role in coordinating gene expression in the nucleus, plastid and mitochondrion, and in integrating pathways of cellular metabolism and development. Presumably, there is crosstalk between retrograde signaling and other signal transduction pathways (e.g., light, hormones, sugars, developmental factors) that also play a role in coordinating nuclear and organelle gene expression (e.g., Neff et al., 2000; Oswald et al., 2001).