History of research on Arabidopsis thaliana

Arabidopsis thaliana is a first class model organism and the single most important species for fundamental research in plant molecular genetics.

A. thaliana was the first plant for which a high-quality reference genome sequence was determined (see below), and a worldwide research community has developed many other genetic resources and tools. The experimental advantages of A. thaliana have enabled many important discoveries.[1][2][3][4] These advantages have been extensively reviewed,[5][6][7][8][9][10][11][12] as has its role in fundamental discoveries about the plant immune system,[13] natural variation,[14][15] and other areas.[16]

Early history

A. thaliana was first described by Johannes Thal, and later renamed in his honor.[15] (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][15] 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]

Gerhard Röbbelen organized the first International Arabidopsis Symposium in 1965.[10] Röbbelen also started the 'Arabidopsis Information Service', a newsletter for sharing information in the community.[17] This newsletter was maintained by A.R. Kranz starting in 1974, and was published until 1990.[10]

Adoption as the premiere model plant species for molecular genetics

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,[18] which was an important advantage for early molecular methods.[10] Meyerowitz and colleagues also made important contributions to development of the ABC model of flower development via genetic analysis of floral homeotic mutants.[19][20][21] 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.[22][7] Pioneering A. thaliana studies have used its natural filamentous pathogen Hyaloperonospora arabidopsidis, the model plant-pathogenic bacterium Pseudomonas syringae, and many other microbes.[13]

Development of a genetic map based on visible and molecular genetic markers facilitated map-based cloning of mutant loci from classical "forward genetic" screens.[10][12] Growing amounts of DNA sequence data facilitated development and application of such molecular markers.[23][24] Descriptions of the first successful map-based cloning projects were published in 1992.[25]

A. thaliana can be genetically transformed using Agrobacterium tumefaciens; transgenic seed can be obtained by simply dipping flowers into a suitable bacterial suspension. The invention/discovery of this 'floral dip' method[26] made A. thaliana arguably the most easily transformed multicellular organism, and has been essential to many subsequent investigations.[10] Efficient transformation facilitated insertional mutagenesis[27] as described further below.

Genome project

An international consortium began sequencing and assembly of a draft genome for A. thaliana in 1990.[8] This work paralleled the Human Genome Project and related projects for other model organisms, and built on efforts to sequence expressed sequence tags from A. thaliana.[28][29] Descriptions of the sequences of chromosomes 4 and 2 were published in 1999,[30][31] and the project was completed in 2000.[32][33][34][35] This represented the first reference genome for a flowering plant and facilitated comparative genomics.

2010 project

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.[36][37] 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, and 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.[38][39] 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.[16]

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,[40] was the namesake for the Argonaute protein family central to silencing.[11] Forward genetic screens focused on vegetative phase change uncovered many genes controlling small RNA biogenesis. A. thaliana became an important model for RNA-directed RNA 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).[11]

Post-2010 project developments

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, the end of NSF funding for The Arabidopsis Information Resource database,[41] and the rise of new genome-sequence-enabled model plant species (including crops). Nevertheless, A. thaliana remains a popular model, and continues to be the subject of intense study using new technologies such as high-throughput short-read sequencing. Mapping of mutations from forward screens is increasingly done with direct genome sequencing, combined in some cases with bulked segregant analysis or backcrossing.[42] A. thaliana is a premier model for studies of natural genetic variation,[11][14][15] including genome-wide association studies. Short RNA-guided DNA editing with CRISPR tools has been applied to A. thaliana since at least 2013.[43]

References

  1. ↑ Nicholas Wade (1999). "Geneticists tap secrets of 'the weed'". New York Times.
  2. ↑ Andrew Pollack (2000). "First complete plant genetic sequence is determined". New York Times.
  3. ↑ Pennisi, Elizabeth (2000-10-06). "Arabidopsis comes of age". Science. 290 (5489): 32–35. doi:10.1126/science.290.5489.32. ISSN 0036-8075. PMID 11183143. Retrieved 2017-10-28.
  4. 1 2 Potter, Erik (2014). "From Apathy to Apogee". MIZZOU Magazine. Retrieved 2014-08-22.
  5. 1 2 3 Redei, G P (1975-12-01). "Arabidopsis as a genetic tool". Annual Review of Genetics. 9 (1): 111–127. doi:10.1146/annurev.ge.09.120175.000551. ISSN 0066-4197. Retrieved 2017-10-03.
  6. ↑ Estelle, M. A.; Somerville, Chris R. (1986). "The mutants of Arabidopsis". Trends in Genetics. 2: 89–93. Retrieved 2016-08-30.
  7. 1 2 Fink, Gerald R. (1998-06-01). "Anatomy of a Revolution". Genetics. 149 (2): 473–477. ISSN 0016-6731. PMID 9611166. Retrieved 2017-10-22.
  8. 1 2 Meinke, David W.; Cherry, J. Michael; Dean, Caroline; Rounsley, Steven D.; Koornneef, Maarten (1998-10-23). "Arabidopsis thaliana: A Model Plant for Genome Analysis". Science. 282 (5389): 662–682. doi:10.1126/science.282.5389.662. ISSN 0036-8075. PMID 9784120. Retrieved 2017-10-22.
  9. ↑ Somerville, Chris; Somerville, Shauna (1999-07-16). "Plant functional genomics". Science. 285 (5426): 380–383. doi:10.1126/science.285.5426.380. ISSN 0036-8075. PMID 10411495. Retrieved 2017-12-22.
  10. 1 2 3 4 5 6 7 Somerville, Chris; Koornneef, Maarten (2002). "A fortunate choice: the history of Arabidopsis as a model plant". Nature Reviews Genetics. 3 (11): 883–889. doi:10.1038/nrg927. ISSN 1471-0056. Retrieved 2014-11-05.
  11. 1 2 3 4 Jones, Alan M.; Chory, Joanne; Dangl, Jeffery L.; Estelle, Mark; Jacobsen, Steven E.; Meyerowitz, Elliot M.; Nordborg, Magnus; Weigel, Detlef (2008-06-13). "The impact of Arabidopsis on human health: diversifying our portfolio". Cell. 133 (6): 939–943. doi:10.1016/j.cell.2008.05.040. ISSN 0092-8674. Retrieved 2015-06-09.
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  15. 1 2 3 4 Krämer, Ute (2015-03-25). "Planting molecular functions in an ecological context with Arabidopsis thaliana". eLife. 4: –06100. doi:10.7554/eLife.06100. ISSN 2050-084X. PMID 25807084. Retrieved 2017-04-20.
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