Arabidopsis: A rich harvest 10 years after completion of the genome sequence

The year 2010 marks the 10th anniversary of the publication of the fully assembled Arabidopsis nuclear genome DNA sequence (The Arabidopsis Genome Initiative, 2000). On this occasion, we at The Plant Journal wish to offer an opportunity to look back and highlight some of the numerous accomplishments in plant science, and beyond, that the availability of the first plant nuclear genome DNA sequence has spawned. As a result of the effort by many, we are providing the scientific community with this Special Issue that is freely available online at the Wiley-Blackwell web site (http://www.theplantjournal.com). We the Editors of this Special Issue, Peter McCourt and Christoph Benning, as many of our friends and colleagues, have been fortunate enough to witness up close the emergence of Arabidopsis from an obscure experimental system to become the predominant plant model over the past decade. Speaking only for The Plant Journal, of more than 3000 articles published during the past decade, a large fraction mention Arabidopsis or deal with discoveries made in this plant. Many will agree with us in humbly stating that we greatly benefited from the visionary effort of giants before us who in their respective countries made the sequencing of the Arabidopsis genome possible and convinced themselves and the general public that the cost would be worth it. Indeed, obtaining the first assembled genome of a plant and the development of 'omics' tools facilitated the exploration of gene function in Arabidopsis from individual genes to nearly all of its genes in parallel, a process that is still ongoing. National funding agencies wisely continued to make it possible to explore the Arabidopsis genome on a grand scale during the past decade, and enabled scientists and the public at large to reap the benefits of a substantial investment of resources into obtaining the genomic sequence. As the exploration of the Arabidopsis genome is a truly international effort, the national agencies in many countries deserve to be acknowledged, and a sampling can be found in the acknowledgements to each of the articles in this Special Issue. In addition, private companies have greatly contributed to the available public resources, for example by providing a second Arabidopsis genomic sequence from a different ecotype, thereby facilitating the development of genetic markers and the mapping of genes. As a result of this decade of prolific research, we can say without hesitation that most of the genes of Arabidopsis as we know them today have been investigated at some level more than once, and that a vast array of data and materials has been produced and made accessible through scientific community resources such as TAIR (The Arabidopsis Information Resource; http://www.arabidopsis.org) or various stock centers in many countries. Of course, this does not mean that we know for certain the function of all genes in every cell of the plant during all times of its life cycle. In fact, we may not even know all the genes of Arabidopsis, as entire new classes of genes have been discovered during the past decade, for example those encoding different small RNAs. Nevertheless, as will become clear when reading the different articles in this Special Issue, hardly any area of plant biology has not made sweeping progress due to the availability of the Arabidopsis genome and the emergence of new tools in the post-genomic era. Advancing basic discoveries from the model Arabidopsis to crop plants takes time, and we are just beginning to witness this transition. One of the most rewarding aspects for supporters of Arabidopsis as a model is the fact that discoveries made in Arabidopsis during the past decade have led to the understanding or recognition of molecular processes at work in non-plant organisms, including humans (Jones et al., 2008). Thus, Arabidopsis has now become a model for basic biological discoveries equal to lambda phage, E. coli, Saccharomyces, Drosophila, or Caenorhabditis. In an effort to highlight the specific areas of research to which the exploration of the Arabidopsis genome has contributed, we asked for articles from a diverse and representative group of leading experts of different generations of scientists, some of whom provided touching personal accounts of their experiences working with Arabidopsis. Of course, there are many more areas of research that could have been covered, and many more outstanding colleagues who could have written articles for this Special Issue than we were able to accommodate. Many of these colleagues generously reviewed the articles in this Special Issue, sometimes up to four experts per article, and made many constructive suggestions. We would like to thank all of those who have contributed to achieving the highest possible scientific standard for the articles in this Special Issue, and apologize to all those we could not invite. In the first article, Maarten Koornneef and David Meinke (pp. 909–921) provide a historic overview of the emergence of Arabidopsis as a genetic model. As Maarten and David show, without a sound genetic base, genomics studies are greatly weakened. Steve Rounsley and Rob Last (pp. 922–927) summarize the benefits of having multiple sequences from different ecotypes and describe how genetic mapping has been perfected during the past decade, facilitating forward-genetics (from phenotype-to-genotype) in Arabidopsis. We all remember the trials and tribulations of cloning a gene based solely on a phenotype at the start of the century. Related to this, Ronan O'Malley and Joe Ecker (pp. 928–940) summarize the development of different gene disruption libraries that have paved the path from genomic sequence to gene function by reverse-genetics (from genotype-to-phenotype) in Arabidopsis. These examples clearly show the power of organized genomic resources that have and will continue to revolutionize plant research. For example, one of the most fascinating new areas of basic research that emerged during the past decade is the role of small regulatory RNAs and their metabolism. An article by Xuemei Chen (pp. 941–958) illustrates the crucial contribution of Arabidopsis research to our current mechanistic understanding of the function of small RNAs in the development of plants and beyond. In general, the study of plant development was greatly facilitated by the availability of the Arabidopsis genomic sequence and new powerful cell biological tools developed for this plant. We start with the embryo, where historically much developmental thinking was based on the Nüsslein-Volhard/Wieschaus premise that to understand patterning you must study the embryo (Ingram, 1988). Although this Drosophila paradigm has served a great purpose, as described in the articles by both Gerd Jürgens (De Smet et al., pp. 959–970) and Michel Caboche (North et al., pp 971–981) and their collaborators, plant embryogenesis and late embryonic development have many developmental surprises and differences not found in animals. Next we have an intriguing account from Joanne Chory (pp. 982–991) about the emergence of Arabidopsis as a model to understand light signal transduction. Joanne mentions how she dreamt of identifying all components of a signal transduction pathway by studying Arabidopsis. Although not complete, much of this dream is now becoming a reality, courtesy, in part, of the power of Arabidopsis genomics. Just as light is so important to understanding above-ground plant development, what happens below the ground is just as essential. As Phil Benfey and his colleagues show (pp. 992–1000), roots, because of their well-organized structure, defined cell types, and translucent appearance, have given us insights into fundamental questions of lineage, cellular patterning and differentiation that rival model systems like Caenorhabditis. From contributions on how plant cells know 'what they are' we shift to an aspect of plant biology that is often understudied in other model systems: the integration of environmental signals to drive developmental decisions. Rick Amasino (pp. 1001–1013) summarizes fundamental breakthroughs of how Arabidopsis takes a myriad of environmental cues and turns these into a developmental transition from vegetative to reproductive development. Because it is a terminal developmental event, flower production serves as an excellent model to answer questions on organ identity and formation. As Vivian Irish shows in her review (pp. 1014–1028), mutational analysis began the unraveling of organ formation, but now genomic and cellular tools such as cell-specific markers and confocal imaging enable, in real time, the monitoring and modeling of events in the apical meristem of Arabidopsis. Finally, no area of plant developmental biology has benefited more from Arabidopsis research than the area of plant hormones. Aside from the Giberellic Acid receptor, all the major hormone receptors were identified using Arabidopsis mutants. From these studies, surprising mechanisms of hormone reception in plants came to light during the last decade. Aaron Santner and Mark Estelle (pp. 1029–1040) describe how the binding of several plant hormones to their cognate receptors leads to the degradation of repressors of gene expression. Certainly, many of us initially scratched our heads when Mark and his co-workers discovered defects in components of the ubiquitin/proteasome complex in auxin-response mutants. The sheer complexity of this system was only revealed with the sequencing of the Arabidopsis genome, and understanding the function of individual members of the large gene families involved will keep scientists busy for some time. Plants are exposed to a variety of environmental stresses during their life time. Because plants are sessile and cannot escape, they have developed complex protective responses to a variety of abiotic stresses as described by Takashi Hirayama and Kazuo Shinozaki (pp. 1041–1052). Extensive analysis of the responses of Arabidopsis to pathogens also led to fundamental insights into what Marc Nishimura and Jeff Dangl (pp. 1053–1066) call the 'plant immune system' in their chronology of progress of the field. It is without doubt that discoveries made in the areas of abiotic and biotic stress research in Arabidopsis will translate into higher productivity of crop plants in the near future. To many of the younger generation of students of biology, primary metabolism is the usual staple in biochemistry class. Much of it was discovered during the past century of biochemical exploration. However, most text books of biochemistry refer in their discussion of carbohydrate metabolism to less complex non-photosynthetic organisms than plants. Primary metabolism is at the heart of plant biomass production and, as it turns out, big discoveries were made during the past decade, for example the pathway of starch degradation, by using Arabidopsis as a model. Mark Stitt and his colleagues (pp. 1067–1091) provide a fascinating summary and perspective of how the combination of 'omics' technologies applied to Arabidopsis has led to the beginnings of a more fundamental understanding of the integration of primary metabolism in plants at the systems scale. Prior to the adoption of Arabidopsis as a genetic model, several areas of plant biochemistry were intractable and progress was slow due to the complex nature of the underlying combinatorial chemistry of many classes of natural compounds or due to the fact that the respective enzymes are integral membrane proteins that are difficult to study. Without doubt, those areas include plant lipid metabolism as summarized by James Wallis and John Browse (pp. 1092–1106), and the assembly of cell wall components as discussed by Aaron Liepman and colleagues (pp. 1107–1121). Many biochemical mutants have been isolated by brute-force forward-genetic screening of the chemical composition of Arabidopsis cell extracts, using ever more downscaled multiparallel approaches. These mutants led to the isolation of the respective enzyme-encoding genes, which enabled the production and study of the recombinant proteins. This indirect approach turned out to be a great improvement over the direct identification of fragile or inactive enzymes purified from their native source. However, as many of us want to study native enzymes and their modifications, we find ourselves moving from Arabidopsis to relatives with more readily available tissue mass, a sure sign that Arabidopsis has its limitations when it comes to biochemistry. Moreover, if the goal is to study specific aspects of metabolism, for example carbon partitioning in a starchy storage organ, alternatives to Arabidopsis, such as potato or even rutabaga, start to look attractive. However, even in these cases, Arabidopsis still serves as the reference model providing 'leads', and to which discoveries in other plants will be compared for a long time to come. Indeed, the ever-advancing progress in DNA sequencing technology makes it now possible to obtain genomic information from any living organism at an affordable price, ushering in the era of comparative genomics and metagenomics. Much of the interpretation of these new genomes, such as metabolic reconstruction, will rely on functional data deduced from models such as Arabidopsis. In our own enthusiasm for Arabidopsis it is easy to forget the many fundamental discoveries that were made in plant biology and biochemistry prior to, and despite of, the establishment of Arabidopsis as a model, as some of the reviewers felt compelled to remind the Authors and Editors. We salute and acknowledge all those great women and men who pushed the envelope of plant biology without having the benefits of the Arabidopsis genome. Our goal here was not to give a complete summary of the entire field of plant biology or of all Arabidopsis research ever done, but to provide an accurate account of some of the highlights of discovery made possible by the availability of the Arabidopsis genome sequence in terms that make sense to the expert, the student of biology, and the interested lay person. However, we would like to add that we are also not at the end, or even at the beginning of the end, for Arabidopsis as a system. The recent identification of the ABA receptor by Arabidopsis researchers was picked as 'One of the Top 10 Breakthroughs' in all of science for 2009 (The News Staff, 2009). We believe there are many more of these to come. We are not alone in our assessment. We asked the authors to provide forward-looking perspectives and many are optimistic about the future of Arabidopsis research. Early Arabidopsis research showed the power of single-gene analysis. With the advent of systems biology and bioinfomatics, Arabidopsis will again be a central player in understanding how single genes interact to make a functional plant. It is up to the reader to use this information, for example in interactions with legislators in efforts to help them make decisions that affect public support of plant research, or to educate the next generation of plant biologists. At a more personal level, reading the articles in this Special Issue, many of us simply might enjoy this moment in history and be in awe recognizing the accomplishments of the plant science community at this 10th anniversary of the publication of the Arabidopsis genome.

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