Conservation and innovation in plant signaling pathways

In this brief survey, we have highlighted just a few examples where we can begin to trace the origins of novelty in the evolution of plant signaling pathways. The source materials derive from some expected sources, such as the progenitor of the chloroplast genome and genes inherited from the common ancestor of all eukaryotes, but also include a surprising number of novel genes of unknown origin. While the mechanisms that allow evolution of new functions for old genes are presumably similar in eukaryotes, there may be qualitative differences at that level as well. For example, is the creation of novelty through gene duplication and diversification more common in plants than in animals? In animals, examples of evolution through gene duplication are balanced by examples where single genes have evolved more complex regulation. That the Arabidopsis genome should have nearly twice the gene number of Drosophila, an organism that is arguably more complex, is intriguing. One possibility is that plant genomes have a higher level of functional redundancy overall. If so, a smaller fraction of gene disruptions in plants will have discernable phenotypes relative to other eukaryotes. Time will tell as we accumulate more data from gene knockout experiments in plants. Alternatively, functional complexity may be partitioned differently in plant genomes such that a larger number of less complex genes are used to span an equivalent set of functions that can be provided by a smaller number of more complex genes in animals.Plant evolution might favor a path of deploying a larger number of differentially regulated simple genes rather than a smaller number of more complex genes for a couple of reasons. First, polyploidy and aneuploidy are better tolerated in plants than in higher animals allowing more frequent wholesale duplication events. As illustrated by the history of the maize genome, polyploid genomes relax to genetic diploidy fairly rapidly, but in the process create a large number of partially redundant paralogous genes, many of which can be distinguished phenotypically (Gaut and Doebley 1997xDNA sequence evidence for the segmental allotetraploid origin of maize. Gaut, B.S and Doebley, J.F. Proc. Natl. Acad. Sci. USA. 1997; 94: 6809–6814Crossref | PubMed | Scopus (477)See all ReferencesGaut and Doebley 1997). A second possibility is that the capacity to add regulatory complexity to individual plant genes is constrained in some way relative to animals. Upstream regulatory elements in plant genes are rarely located more than 1 kb or so from the transcription start and more often occur within the first 300 nt (roughly the span of two nucleosomes). In Arabidopsis, this compact regulatory structure is enforced by an average gene density of one gene per 4 kb (5xAnalysis of 1.9 Mb of contiguous sequence from chromosome 4 of Arabidopsis thaliana. Bevan, M, Bancroft, I, Bent, E, Love, K, Goodman, H, Dean, C, Bergkamp, R, Dirkse, W, Van Staveren, M, Stiekema, W et al. Nature. 1998; 391: 485–488Crossref | PubMed | Scopus (603)See all References, 50xSequence and analysis of chromosome 2 of the plant Arabidopsis thaliana. Lin, X, Kaul, S, Rounsley, S, Shea, T.P, Benito, M.I, Town, C.D, Fujii, C.Y, Mason, T, Bowman, C.L, Barnstead, M et al. Nature. 1999; 402: 761–768Crossref | PubMed | Scopus (497)See all References). Perhaps, in animals, the unit of duplication can be an enhancer as readily as an entire gene whereas in plants, there is a tendency to duplicate whole genes. However, the features of plant chromatin structure that would impose such a constraint are not obvious.Clearly, these are very early days in the era of comparative functional genomics, and we can look forward to many new insights into the evolution of novelty in eukaryotic signal transduction pathways.‡To whom correspondence should be addressed (e-mail: drm@ufl.edu).