History of research on Arabidopsis thaliana

A. thaliana was first described by Johannes Thal, and later renamed in his honor.[17] (See the Taxonomy section of the main article.) Friedrich Laibach outlined why A. thaliana might be a good experimental system in 1943 and collected a large number of natural accessions.[5][10][11][17] George Rédei pioneered the use of A. thaliana for fundamental studies, completing the first chemical mutagenesis screens[4] and writing an influential review in 1975.[5] Rédei distributed the standard laboratory accessions ‘Columbia-0’ and ‘Landsberg erecta’.[14]

Gerhard Röbbelen organized the first International Arabidopsis Symposium in 1965.[11] Röbbelen also started the 'Arabidopsis Information Service', a newsletter for sharing information in the community.[19] This newsletter was maintained by A.R. Kranz starting in 1974, and was published until 1990.[11]

As molecular biology methods progressed, many investigators sought to focus community effort on common model plant species. Researchers in the laboratory of Elliot Meyerowitz showed that A. thaliana genome is relatively small and nonrepetitive,[20] which was an important advantage for early molecular methods.[11] Meyerowitz and colleagues also made important contributions to development of the ABC model of flower development via genetic analysis of floral homeotic mutants.[21][22][23] Meyerowitz and Chris R. Somerville were later awarded the Balzan Prize for their work developing A. thaliana as a model.[24] Notable researchers such Gerald Fink and Frederick M. Ausubel were persuaded to adopt A. thaliana as a model, including for the study of host-microbe interactions.[25][7] Pioneering A. thaliana studies have used its natural filamentous pathogen Hyaloperonospora arabidopsidis, the model plant-pathogenic bacterium Pseudomonas syringae, and many other microbes.[15]

Development of a genetic map based on visible and molecular genetic markers facilitated map-based cloning of mutant loci from classical "forward genetic" screens.[11][13] Growing amounts of DNA sequence data facilitated development and application of such molecular markers.[26][27] Descriptions of the first successful map-based cloning projects were published in 1992.[28]

A. thaliana can be genetically transformed using Agrobacterium tumefaciens; transformation was first reported in 1986.[29] Later work showed that transgenic seed can be obtained by simply dipping flowers into a suitable bacterial suspension. The invention/discovery of this 'floral dip' method[30] made A. thaliana arguably the most easily transformed multicellular organism, and has been essential to many subsequent investigations.[11] Efficient transformation facilitated insertional mutagenesis[31] as described further below.

The plant homeodomain finger is so named due to its discovery in an Arabidopsis homeodomain. In 1993 Schindler et al discovered the PHD finger in the protein HAT3.1. It has since proven to be important to chromatin in a wide variety of taxa.[32]

A series of meetings led to an ambitious long-term NSF-funded initiative to determine the function of every A. thaliana gene by the year 2010.[41][42] The rationale for this project was to combine new high-throughput technologies with systematic gene-family-wide studies and community resources to accelerate progress beyond what was possible via piecemeal single-laboratory studies.

DNA microarray technology was rapidly adopted for A. thaliana research and led to the development of "atlases" of gene expression in different tissues and under different conditions. The A. thaliana genome sequence, low-cost Sanger sequencing, and ease of transformation facilated genome-wide mutagenesis, yielding collections of sequence-indexed transposon mutant and (especially) T-DNA mutant lines.[43][44] The ease and speed of ordering mutant seed from stock centers dramatically accelerated "reverse genetic" study of many gene families; the Arabidopsis Biological Resource Center and the Nottingham Arabidopsis Stock Centre were important in this regard, and information on stock availability was integrated into The Arabidopsis Information Resource database.[18]

A. thaliana quickly became an important model for the study of plant small RNAs. The argonaute1 mutant, named for its resemblance to an Argonauta octopuses,[45] was the namesake for the Argonaute protein family central to silencing.[12] Forward genetic screens focused on vegetative phase change uncovered many genes controlling small RNA biogenesis. Multiple groups identified mutations in the DICER-LIKE1 gene (encoding the main DICER protein controlling microRNA biogenesis in plants) that cause strong developmental defects.[46] A. thaliana became an important model for RNA-directed DNA methylation (transcriptional silencing), partly because many A. thaliana methylation mutants are viable, which is not the case for several model animals (in which such mutations cause lethality).[12]

As the NSF 2010 project neared completion, there was a perceived decrease in funding agency interest in A. thaliana, evidenced by the cessation of USDA funding for A. thaliana research and the end of NSF funding for the TAIR database.[47] This trend coincided with the progress of the (US NSF-supported) National Plant Genome Initiative, which began in 1998 and put an increased emphasis on crops. Draft genome sequence for rice were published in 2002[48][49] and followed by publications for sorghum[50] and maize[51] in 2009. The draft genome of Brachypodium distachyon, a short-statured model grass (Poaceae) was published in 2010.[52]

Nevertheless, A. thaliana remained a popular model, and 13 prominent American A. thaliana geneticists were selected as investigators of the prestigious Howard Hughes Medical Institute and Gordon and Betty Moore Foundation in 2011:[53][54] Philip Benfey, Dominique Bergmann, Simon Chan, Xuemei Chen, Jeff Dangl, Xinnian Dong, Joseph R. Ecker, Mark Estelle, Sheng Yang He, Robert Martienssen, Elliot Meyerowitz, Craig Pikaard, and Keiko Torii. (Also selected were wheat geneticist Jorge Dubcovsky and photosynthesis researcher Krishna Niyogi, who has extensively used A. thaliana along with the alga Chlamydomonas reinhardtii.[55]) Prior to this, a handful of A. thaliana geneticists had become HHMI investigators: Joanne Chory (1997),[56] Daphne Preuss (2000-2006),[57] and Steve Jacobsen (2005).[58]

A. thaliana continues to be the subject of intense study using new technologies such as high-throughput sequencing. Mapping of mutations from forward screens is increasingly done with direct genome sequencing, combined in some cases with bulked segregant analysis or backcrossing.[59] A. thaliana is a premier model for studies of the plant microbiome and natural genetic variation,[12][16][17] including genome-wide association studies. Short RNA-guided DNA editing with CRISPR tools has been applied to A. thaliana since at least 2013.[60]

• Electronic Arabidopsis Information Service (AIS) archive
• The Arabidopsis book online
• 1001 Genomes Project site