Twenty-first century plant biology: impacts of the Arabidopsis genome on plant biology and agriculture.

In the late 1980s and early 1990s, Arabidopsis (Arabidopsis thaliana) rapidly emerged as a model system for plant biology due to the ease of genetic approaches to study development, physiology, and gene function coupled with a highly collaborative community. Arabidopsis’s position as the premiere model plant system was cemented in the early 1990s when the EST project commenced at Michigan State University (Newman et al., 1994). This was the first such effort in plants and it seeded production of large-scale sequence and functional genomics resources for Arabidopsis that to this day are unmatched in any other plant species. While the EST project propelled Arabidopsis research into the genomics era, it was the foresight of leaders in the plant biology community to “...identify all of the genes by any means, and to determine the complete sequence of the Arabidopsis genome before the year 2000” (http://www.arabidopsis.org/portals/masc/ Long_range_plan_1990.pdf). The resulting coordinated international genome sequence effort, the Arabidopsis Genome Initiative, laid the foundations for transition of Arabidopsis from a genetic to a genomic model system. This culminated in the publication of the high-quality genome sequence of the Columbia (Col-0) accession (Arabidopsis Genome Initiative, 2000). While there are gaps in highly repetitive lowcomplexity regions of what is now termed the reference genome, the quality of the Col-0 genome sequence is, and for the foreseeable future will remain, the highest quality plant genome sequence. When coupled with its manually curated annotation, the sequence data makes Arabidopsis the gold standard for all plant genomes. Starting in 1998, Cereon Genomics LLC (a wholly owned subsidiary of Monsanto Co.) produced a lowdepth shotgun sequence of the Landsberg erecta genome using Sanger sequencing technology (Jander et al., 2002), providing an early look at the genes of a flowering plant. For the community, access to both the Col-0 and Landsberg erecta genome sequences revealed an unprecedented number of polymorphisms between these landraces, enabling more than 100 published map-based cloning studies. To our knowledge, it also provided the community with the first example of how high-throughput sequencing of an accession or cultivar related to a high-quality reference sequence makes the initial sequence even more valuable (Rounsley and Last, 2010). Next-generation sequencing technologies permit high-throughput sequencing at greatly reduced costs and sequencing of accessions is now feasible at an enormous scale. The plan to analyze genome-wide sequence variation in 1,001 accessions of Arabidopsis (Weigel and Mott, 2009) is well under way with nearly 100 completed genomes as of early 2010 (http:// www.1001genomes.org/). This pioneering effort will result in a deep understanding of genetic variability within a species and permit analysis of genome evolution and population biology. This illustrates how Arabidopsis research continues to be at the forefront of defining approaches that will revolutionize our understanding of economically important plant processes and plant species. Gene expression states are affected by DNA and chromatin protein modification. While standard genome DNA sequence alone cannot directly report these decorations, these epigenetic states can be assessed at the single nucleotide level using next-generation sequencing approaches, and descriptive studies on the Arabidopsis epigenome are emerging (Lister et al., 2008). This information enables studies of biological problems that are unique to plants such as epigenetic imprinting in the triploid endosperm and the diploid embryo of the seed. Examination of methylation states revealed imprinting arose through targeted methylation of genic regions due to nearby transposable element insertion (Gehring et al., 2009). While the Arabidopsis genome has relatively few transposable elements, other genomes such as maize (Zea mays) and wheat (Triticum aestivum) have large numbers of these and other repetitive sequences and it will be fascinating to examine the molecular details of imprinting in these agronomic species.