Plant Cell, Vol. 13, 5-10, January 2001, Copyright © 2001, American Society of Plant Physiologists
Arabidopsis Genome Conference 2000: How a Small Weed Changed the World
Nancy A. Eckardt
News and Reviews Editor
Participants at the Arabidopsis Genome Conference at Cold Spring Harbor Lab (Dec. 7–10, 2000) celebrated the imminent publication of the complete sequence of the Arabidopsis genome, due for release in the journal Nature the following week (Arabidopsis Genome Initiative 2000 
). This marks a milestone for plant biology that promises to radically change not only the way in which many aspects of plant biology are studied, but also some of our fundamental views about plant—and eukaryotic—development and evolution. Conference organizers Rob Martienssen (Cold Spring Harbor Lab, NY) and Mike Bevan (John Innes Center, Norwich, UK) brought together many of the leading scientists involved in the Arabidopsis Genome Initiative sequencing and ongoing annotation efforts, and many others involved in making use of the genome sequence for functional and comparative genomics studies. Special mention was made honoring the contributions to plant genetics and the genome project of DeLill Nasser, an ardent supporter of plant genetics research and program director for Genetics (1978 to present) and the Arabidopsis Genome Project (1995 to present) at the National Science Foundation. Dr. Nasser, who was unable to attend the meeting due to illness, was honored with a special Plant Genetics Award, presented by Ron Davis (Stanford University, CA) on behalf of the plant science community, in deep gratitude for the friendship and inspiration she has given to plant geneticists for many years.
THE FAR-REACHING VALUE OF THE ARABIDOPSIS GENOME
The genomics era is now in full swing, and it was clear from numerous presentations at the conference that the Arabidopsis genome sequence has already made significant contributions to our understanding of plant biology, and indeed eukaryotic biology, particularly in the areas of evolutionary biology and molecular biology. The far-reaching value of the Arabidopsis genome was underscored in particular in the first and last talks of the conference, given by Plenary Speaker Michael Ashburner (EMBL-EBI Welcome Trust Genome Campus, Hinxton, UK) and Steve Tanksley (Cornell University, Ithaca, NY), respectively.
Ashburner, famous for his model of hormonal regulation of gene activity in flies, described problems with annotation of the Drosophila genome, and the efforts to produce a dynamic, controlled vocabulary for annotating genes with respect to function by the Gene Ontology Consortium (GO). The goal of GO, which is made up of participants of the Drosophila (fruitfly), Saccharomyces (budding yeast), Mus (mouse), Caenorhabditis (nematode), and Arabidopsis genome projects, is to produce a vocabulary to be applied to all eukaryotes that will associate gene products with their molecular functions, biological processes, and cellular components (see http://www.geneontology.org). Ashburner pointed out that a good deal of the annotation of the various eukaryotic genomes is on unsure footing, in other words, it is based on homologies to known proteins and/or gene prediction algorithms, with very little empirical data. We have great depth of information on a limited set of individual genes from classical genetics and single-gene molecular studies, and a great breadth of information from large-scale whole genome analyses, which lack depth; there is the need for great depth as well as breadth of knowledge for the Drosophila as well as Arabidopsis genomes. Arabidopsis currently represents the best annotated multicellular eukaryotic genome. Thus in addition to providing the plant component of the GO, the Arabidopsis genome will give tremendous aid to efforts to improve and extend the annotation of all complex genomes.
Insights into Evolution
Tanksley is interested in how the Arabidopsis genome may be used to shed light on the mechanisms by which plant genomes evolve over long periods of time, as well as to predict genes and markers in tomato and other species. The evolutionary distance between tomato, an asterid species, and Arabidopsis, a rosid, is fairly large; they are estimated to have diverged from a common ancestor between 90 and 150 MYA. This is similar to the estimated time of divergence of the human and mouse genomes, yet we find that comparisons between the human and mouse genomes are quite good and that the mouse is a fairly good model for human and other mammalian systems. Thus, Arabidopsis may prove to be a good model for tomato and other dicot genomes. To identify putative orthologs (genes with high sequence similarity—that is, assumed to have the same or similar function—in different species) between tomato and Arabidopsis, Tanksley's group used the BLAST sequence similarity search program to compare with tomato EST sequences (expressed sequence tags from cDNA clones, representing expressed genes from tomato) to the Arabidopsis genome sequence. Approximately 75% of the tomato ESTs matched sequence in the Arabidopsis genome, and of these, 4% were single copy genes within both genomes and thus good candidates for being true orthologs. These were mapped to the tomato genome and their organization compared with that found in the Arabidopsis genome, and a tomato BAC clone was selected and sequenced for a more detailed sequence comparison over a long region (see Ku et al. 2000 ).
One of the most interesting findings reported by Tanksley was that gene density in the tomato BAC sequence, at approximately one gene or open-reading frame per 6 kb, was similar to that of Arabidopsis, at approximately one gene per 4.5 kb. Arabidopsis has a genome content of 
120 Mb and an estimated 25,500 genes. Because tomato has a genome content of around 950 Mb, a similar gene density would lead us to predict that tomato has around 145,000 genes—more than that estimated for any other eukaryote, including humans! Tomato may turn out to have more genes than Arabidopsis, but 145,000 is an unlikely number. Thus, it may be that in tomato and other large plant genomes, expressed genes are clustered in small portions of the genome, and a significant portion of the genome remains gene-poor. The genomic comparisons further suggested that at least two large-scale genome duplication events (possibly whole genome) occurred in the Arabidopsis lineage near the divergence time of tomato and Arabidopsis. More tomato sequence data is needed to determine if and when similar events occurred in the tomato genome. This conclusion allows the prediction that taxa diverged from a common ancestor with Arabidopsis after the duplication events (such as legumes) will share these duplicated segments with Arabidopsis.
Talks given by Owen White (TIGR, Rockville, MD), Hans-Werner Mewes (Max Planck Institute, Martinsried, Germany), and Curtis Palm (Stanford Genome Technology Center, Stanford University, CA) also included presentation of data suggesting that large regions in all five Arabidopsis chromo-somes have undergone duplication events. According to White and Mewes, an estimated 58 to 60% of the Arabidopsis genome is duplicated. Mewes presented data suggesting that complex rearrangements between chromosomes have occurred multiple times. Palm reported on structural analysis of chromosome 1, suggesting that four large-scale regions were duplicated, each region having a counterpart in the top and bottom arms of the chromosome. Compared with non-plant eukaryotes (Saccharomyces, Drosophila, and Caenorhabditis), Arabidopsis has a high proportion of very closely related genes, which are the apparent product of gene duplication events. This leads many to suspect that redundancy of gene function exists within gene families, which is supported by the evidence that mutations in more than one gene of a gene family are often required to produce a mutant phenotype. However, Ashburner cautioned that redundancy is an often-misused word in genetics, and maintained that true redundancy probably will not exist over the long term in biological systems because there is no way for it to maintained through evolution. Throughout the meeting, others were therefore cautious in their use of the term, and a consensus seemed to arise for the use of "overlapping function" rather than "redundancy."
Centromere Structure and Function
The centromeres of eukaryotic chromosomes are particularly challenging regions for sequencing, because they contain many highly repetitive DNA sequences that are difficult for various chemistries employed in sequencing to "read through." This is true for all of the large-scale eukaryotic genome projects. The Arabidopsis Genome Initiative has made a concerted effort to obtain centromere sequence, and as a result the Arabidopsis genome includes the most extensive centromere sequencing of any of the multicellular eukaryotic genomes to date. The lab of Daphne Preuss (University of Chicago, IL) has made significant contributions to the investigation of centromere structure and function in Arabidopsis (Copenhaver et al. 1999 ). Preuss related that yeast (unicellular eukaryote) centromeres have been well-defined, such that a 120-bp consensus region has been identified on all yeast chromosomes, and her goal is to reach this point for Arabidopsis as well. Arabidopsis centromeres are located somewhere within 1.4- and 1.9-Mb regions on each of the five chromosomes, which contain regions of highly repetitive DNA sequence with some islands of encoded genes. Interestingly, there is evidence that many of these genes are expressed, even though they are highly methylated in young seedlings (it is typically thought that methylation represses gene expression). Furthermore, two of the centromere genes were shown to be expressed only when methylated, because they lost methylation in mature tissues where they were not expressed.
Paul Franz (University of Amsterdam, The Netherlands) presented research on the organization of interphase heterochromatin, which occurs in centromeric regions and in two heterochromatic knobs located on chromosomes 4 and 5 in certain ecotypes of Arabidopsis. Comparison of ecotype Ws with C24, the latter of which lacks the knob on chromosome 4, suggests that the heterochromatic knob resulted from an inversion originating from pericentromeric heterochromatin. Franz also showed spectacular multi-color fluorescent in situ hybridization (FISH) that painted an entire pachytene chromosome with alternating BACs and highlighted euchromatic loops between chromocenters. During interphase, the colocalization of repeats and methylated DNA within the nucleus was disrupted in chromatin remodeling and methyltransferase mutants.
Exploiting Natural Variation in Arabidopsis
The study of natural variation among different ecotypes, or accessions, of Arabidopsis contributes knowledge of evolutionary processes operating in plants, and facilitates the identification of potentially useful genes to target in crop breeding strategies, as discussed by Steve Rounsley (Cereon Genomics, Cambridge, MA), Ben Bowen (Lynx Therapeutics, Hayward, CA), Thomas Mitchell-Olds (Max Planck Institute for Chemical Ecology, Jena, Germany), and Detlef Weigel (Salk Institute, La Jolla, CA). Rounsley reported on the Cereon project to complete whole genome shotgun sequencing of the Arabidopsis Ler ecotype, which will complement the Arabidopsis Genome Initiative project (which has sequenced the Col-0 ecotype), and to identify polymorphisms between the two genomes. They have amassed a large data set totaling 92 Mb of genomic sequence contained within over 50,000 non-overlapping contigs. Mitchell-Olds and Weigel are engaged in efforts to identify loci responsible for quantitative genetic variation among Arabidopsis ecotypes and are testing hypotheses of local adaptation to native environments for ecologically important traits. For example, Weigel, in collaboration with Joanne Chory, reported that hypocotyl length shows quantitative inheritance patterns among Arabidopsis ecotypes. There is good correlation between the latitude of origin and hypocotyl length in plants grown under a given light intensity and quality, and ecotypes originating in more northern latitudes appear to be more sensitive to light in this respect. Weigel showed that it is possible to identify candidate loci for quantitative traits by cluster analysis of phenotypes across ecotypes and known mutants. For example, one ecotype was found to cluster tightly with a phyA mutant with respect to hypocotyl length under a variety of conditions, suggesting that allelic variation at the PHYA locus may control natural variation in this trait. Analysis of the PHYA gene and the encoded protein in this ecotype revealed different properties of the PHYA protein, apparently due to a single missense change relative to standard ecotypes such as Col-0.
PLANT FUNCTIONAL GENOMICS TOOLS AND COMMUNITY SERVICES
Community Services
The scientific community has direct access to the Arabidopsis genome through public databases, such as NCBI (http://www.ncbi.nlm.nih.gov/), and The Arabidopsis Information Resource (TAIR; http://www.arabidopsis.org/). Margarita García-Hernandez and Eva Huala (Stanford University, CA) presented information on the current state of TAIR and future plans for this web-based resource. TAIR has funding from the NSF for five years, beginning in 1999, and will become the major repository in the United States for all Arabidopsis genome data coming from TIGR and other genome centers. TAIR represents the Arabidopsis link to the eukaryotic gene ontology consortium, described above, and will be working on collecting annotation information on cellular components, molecular function, and expression data, all to be integrated into the sequence map viewer. They further hope to develop literature curating tools, enhance the query interface for users to provide feedback and contribute data as well as browse and download information, and provide information and links to the Arabidopsis Biological Resource Center (ABRC) at Ohio State University.
T-DNA and transposon-mediated insertional mutagenesis represent powerful tools for reverse genetics. Several groups have established large collections of T-DNA or transposon insertion lines, collectively giving a reasonable chance of finding a knock-out mutant for any given gene. Michael Sussman (University of Wisconsin, Madison), Jonathan Jones (John Innes Center, Norwich, UK), and Rob Martienssen (Cold Spring Harbor Lab, NY) each presented research on the use of different T-DNA or transposon-tagged lines for reverse genetics projects. Sussman is part of the NSF-funded Arabidopsis Functional Genomics Consortium (AFGC), which has made available to the scientific community more than 60,000 T-DNA- tagged lines and provides a service for identifying and distributing lines carrying insertions that disrupt genes of interest to individual researchers (http://afgc.stanford.edu/). They observed a small but significant bias against T-DNA insertion within genes (ORFs), which means that more lines than originally projected need to be screened to find gene "knock-outs." Sussman described ongoing research of this project to identify and characterize knock-out mutants for many of the 1200 protein kinase genes present in the Arabidopsis genome.
Jones spoke about the Sainsbury lab Arabidopsis transposon insertion (SLAT) lines (Tissier et al. 1999 ; http://www.jic.bbsrc.ac.uk/sainsbury-lab/jonathan-jones/ SINS-database/sins.htm), and research focused on the family of respiratory burst oxidases (Atrboh genes). Insertional mutants in all eight of the Atrboh family members, and various double mutant lines, suggest a variety of hitherto unsuspected roles for active oxygen in plant development, such as in pollen dehiscence and root hair development, in addition to anticipated roles in defense responses. Interestingly, unlike the T-DNA inserts used in Sussman's group, the dSpm transposable element used to create the SLAT lines shows a bias for insertion into genes; most lines sequenced show insertions within 1000 bp downstream of an ATG start site and very few insertions upstream.
Martienssen discussed the creation and use of transposon-tagged lines designed as gene traps (protein-reporter gene fusions that reveal gene expression patterns), enhancer traps (indirect activation of gene by insertion into promoter regions), and secretion traps (targeting of genes that encode secreted proteins). The secretion trap relies on the observation that the GUS protein is inhibited by glycosylation, which occurs in proteins targeted to the endoplasmic reticulum (ER), and glycosylation can by inhibited by treatment with the drug tunicamycin. Thus, the insertion of transposon-tagged GUS into a secreted protein can be detected by screening for transgenic plants that express the GUS reporter only in the presence of tunicamycin. Information on these lines can be found at http://www.cshl.org/genetrap.
Steve Henikoff (Fred Hutchinson Cancer Research Center, Seattle, WA) presented research on the use of traditional chemical mutagenesis and the identification of mutated genes using a process called TILLING (for targeting induced local lesions in genomes), which makes use of gene-specific primers and denaturing HPLC for mutation detection (McCallum et al. 2000 ). In heterozygous lines of interest, the wild-type and mutated alleles, amplified by the same set of primers, will form distinct heteroduplexes that can be detected via denaturing HPLC. An alternate mutation detection technique is based on the celI gene product. CelI incises duplexed DNA precisely 3' to a mismatched base pair, and 90% of mutations induced by the chemical EMS are single base transitions. Thus, celI treatment followed by electrophoretic two-color fragment sizing allows for rapid detection and subsequent sequencing of the gene of interest. Henikoff estimated that this technique could be used to generate more than 500 TILLED mutant gene lines per year in Arabidopsis. The NSF Plant Genome Project has funded Henikoff and collaborator Luca Comai to TILL the Arabidopsis genome and make the lines available to the scientific community through the ABRC.
Notable New Tools
Plenary speaker Michael Snyder (Yale University, New Haven, CT) spoke about tools being used in the large-scale analysis of the yeast genome. Of particular note is a technique to identify all cis targets of various transcription factors using chromatin immunoprecipitation (ChIP) combined with microarray analysis, referred to as the "ChIP chip" method. Chromatin DNA with associated transcription factors is immunoprecipiated from an epitope-tagged transgenic strain and a control non-tagged yeast strain, and the purified DNA labeled with fluorescent markers and hybridized to a array containing DNA corresponding to intergenic regions of the yeast genome. This method was used to identify the targets of key regulators of the G1/S transition in the yeast cell cycle, SWI4 and Mbp1. Snyder also discussed a technique being developed to analyze protein function of all 122 yeast protein kinases in a high through-put fashion. Acrylic chips are laser-etched to create a chip with a 1.4-mm diameter and 300-nL volume micro-wells. The chip surface is activated with a potential kinase substrate, and a different kinase is loaded into every well, allowing all of the 122 kinases to be tested against many different substrates (one substrate per chip) very quickly. They found that 112 of the yeast kinases showed detectable kinase activity; about half recognized many different substrates, while others were quite specific in their choice of substrate.
Michael Sussman (University of Wisconsin) described exciting new research in collaboration with Francesco Cerrina to produce oligonucleotide arrays through a "maskless" chip DNA synthesis technique. This technology, called NimbleChip, makes use of a digital micro-mirror device and a photosensitive substrate hooked up to a DNA synthesizer, and will make possible the production of oligonucleotide arrays at greatly reduced cost relative to conventional photolithographic mask oligonucleotide DNA chips (Singh-Gasson et al. 1999 ).
Wayne Volkmuth (Ceres, Inc., Malibu, CA), Jack Okamuru (Ceres), and Z. Jeffrey Chen (Texas A & M University, College Station, TX) all presented research on analyzing gene expression in a high through-put format using cDNA-AFLP. This technique involves selective PCR amplification of restriction digested cDNA samples, which produce a fingerprint banding pattern on PAGE gels of the cDNAs present in the sample. Chen showed that cDNA-AFLP could be used to distinguish homologous gene transcripts between related Arabidopsis species A. thaliana and A. suecica, which is difficult to accomplish using other methods.
Ben Bowen (Lynx Therapeutics, Hayward, CA) spoke about a transcript profiling method called Massively Parallel Signature Sequencing (MPSS), which involves amplifying cDNAs and attaching them to beads which are used to generate 20-bp signature sequences (Brenner et al. 2000 ). MPSS is a promising method for rapid identification of multiple candidate genes for QTL that control complex traits, and Bowen described the identification of two candidate genes controlling aspects of nitrogen uptake and metabolism.
Finally, Keith Davis (Paradigm Genetics, Research Triangle Park, NC) described a high through-put platform for identifying mutant phenotypes in Arabidopsis. Paradigm has developed an impressive system, consisting of a large, highly controlled physical environment for plant growth and automated data collection, and a well-defined system for monitoring phenotypic variation in all stages of plant growth and collecting data in a high through-put fashion. They propose to use this system to identify subtle mutations influencing growth and development and also plan to make many of these mutants available to the public.
NEW INSIGHTS IN PLANT BIOLOGY
It is difficult to separate the various talks at the meeting into categories such as "new tools" and "new insights," etc., because most of the presentations fall under more than one of these headings. Nonetheless, a variety of presentations represented significant new insights into plant development, plant biochemistry and molecular biology, and plant response to the environment.
Recombination
Greg Copenhaver (University of Chicago, IL) presented research he has conducted in the Preuss lab on the regulation of recombination in Arabidopsis, making use of the quartet mutation, which causes the four products of pollen meiosis to remain attached. He has developed a digital assay for analyzing recombination events, using a post-meiotic, pollen-specific promoter to drive GFP expression. Different GFP colors can be used to mark distinct locations along a chromosome, and the post-meiotic positions of the markers observed in the pollen quartets to follow recombination events. Copenhaver has crossed mutants homozygous for the quartet mutation in the Col-0 and Ler backgrounds to assess recombination between the two ecotypes, giving a genome-wide view of recombination (Copenhaver et al. 1998 ). This is a highly promising area of research for addressing questions about the regulation of recombination.
RNA Stability/Turnover
Pam Green and Rodrigo Gutierrez (Michigan State University, East Lansing) are applying cDNA microarray analysis to the study of RNA stability as an important component of the regulation of gene expression. A set of genes with unstable transcripts (defined as having a half-life of <60 min) was identified by dual hybridization to EST microarrays of samples collected at 0 and 120 min following treatment of plants with the transcription inhibitor cordycepin; the 120-min signal remains high (or equal to 0-min signal) for stable messages but declines relative to the 0 time point for unstable messages, and the half-life may be estimated from the two time points. Cluster analysis indicated that auxin and touch gene expression responses have an important RNA stability component. A specific sequence, called DST, identified from a small auxin up-regulated (SAUR) RNA, was found to cause rapid turnover of RNA transcripts. Green's group has employed a genetic selection method to screen for dst mutants, which were found to be extremely rare. A total of three mutants were identified from screens of 800,000 mutagenized plants, and characterization of these mutants is under way (Johnson et al. 2000 ).
Plant Pathogen and Abiotic Stress Responses
Jeff Dangl (University of North Carolina, Chapel Hill) and Nina Fedoroff (Pennsylvania State University, University Park) both reported on the use of cDNA microarray analysis to investigate plant response to pathogens and abiotic stresses. Dangl's group has used microarray analysis to identify a promoter element, the W box, that has significantly increased distribution in a set of genes that cluster with the PR1 gene under a variety of stress treatments (Maleck et al. 2000 ). The Fedoroff group has identified many novel stress-response-associated genes through PCR-suppression subtractive hybridization, and is using singular value decomposition analysis of microarray data to identify patterns of gene expression underlying stress responses (Holter et al. 2000 ).
Circadian Rhythms
Stacey Harmer (Scripps Research Institute, La Jolla, CA) reported on the use of oligonucleotide (Affymetrix) arrays to investigate circadian clock regulation of gene expression. This group has identified a total of 450 clock-controlled genes involved in regulation of many different processes, including phenylpropanoid biosynthesis, response to chilling stress, and sugar metabolism (Harmer et al. 2000 ). This work enables a genome-wide view of how the eukaryotic circadian clock temporally compartmentalizes physiological pathways to coincide with predictable changes in the environment.
Cytochrome P450s
David Galbraith (University of Arizona, Tucson) spoke about a project using transposon tagging and microarray analysis to investigate the function of the cytochrome P450s in Arabidopsis, a large superfamily with approximately 300 members. A number of mutants have been identified, and functional characterizations are under way. Interesting P450s thus identified include CYP83B1, which is involved in auxin and glucosinolate biosynthesis pathways (see "In This Issue"; Bak et al. 2001 ), and CYP90B1, whose null mutant causes a dwarf phenotype due to a lesion in brassinosteroid biosynthesis.
Auxin Responses
Paul Overvoorde (Plant Gene Expression Center, Albany, CA) described efforts in the Theologis lab to investigate how the plant hormone auxin works, using insertional mutagenesis of AUX/IAA/ARF family genes. A total of 28 AUX/IAA immediate, early auxin response genes have been found in the Arabidopsis genome, which encode short-lived, nuclear-localized proteins that form homo- and heterodimers with family members. These genes are further characterized by a promoter element that is bound by ARF proteins. The ARF gene family contains 22 members, and ARF proteins contain the same dimerization domain found in the AUX/IAA proteins, suggesting that heterodimerization occurs within these two families. A total of 1225 possible combinations exists between all of the different IAA/AUX and ARF proteins, suggesting a mechanism for how auxin may be involved in regulation of many and diverse developmental processes.
Historically, molecular biology (i.e., gene organization and the regulation of transcription and translation), in the minds of many, has been divorced from whole organism biochemistry, physiology, and ecology. Genomics, as the study of how genomes are organized and how they function, is the road to "whole organism molecular biology." Molecular biologists have long realized that however "genes" are defined, they do not act as isolated units, and the important goal is understanding how networks of interacting genes and proteins contribute to the resulting biochemistry and physiology of whole organisms. Until recent times, it has quite simply been impossible to study more than one, two, or perhaps a handful of genes and how they interact at once in complex eukaryotic systems. Plant functional genomics research promises great strides in our understanding of gene interactions, and how overlapping networks of cis- and trans-acting factors regulate developmental processes and plant responses to the environment. Arabidopsis is at the forefront of this exciting era in plant biology.
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