- Photo gallery
- Railway plants
- Heavy metals
- Serpentine soils
- Genomic/transcriptomic resources
- PubMed resources
One of the main reasons for anyone to be working with eXtremeplants is to learn from plants that do stress tolerance well. Understanding the fundamental mechanisms of tolerance can be facilitated using genomic approaches applied to populations where selection is strong and on-going. Such studies can provide insights into the species’ demographic histories. Putatively, these approaches can indicate which traits were/are most important in complex adaptations.
The illusion, of course, is that by studying such plants, generalizable mechanisms will become apparent, and perhaps (but don’t hold your breath), those mechanisms could be transferred to the plants that other people care about, e.g. crops. One could select the target, or model, based on any criteria, but there are several that might make the studies more fruitful. For example, the shorter the evolutionary history of the tolerance phenotype, the more likely that the genomic signal can be separated from the noise. Or, the more variability of tolerance exhibited within a single species, the more likely that tolerance-specific genomic differences can be discerned. Or, the more different specific tolerances expressed by different genotypes are, the greater the likelihood that stress-specific characters can be identified. Of course, if there are genetic/genomic resources already available for the species, that is even better.
Arguably, no species meets all these criteria better than Arabidopsis arenosa. Although it is only a “poorly known relative” of Arabidopsis thaliana, A. arenosa is an excellent model for understanding the mechanisms and effects of repeated genome duplication and hybridization events.[2–5] It is also a model for adaptation because of its distribution throughout Europe in a variety of disturbed area types (mountain slopes, forest margins, roadsides, railroad tracks, river banks and grassy and sandy areas, mine sites), its wide altitudinal range (sea level and up to 2000 m), and its genetic specializations to a wide variety of edaphic conditions. And while its genome has not been sequenced (or has been, but hasn’t been released), the genomes available for A. thaliana and A. lyrata have proven suitable for most comparative studies.
A. arenosa is biennial or short-lived perennial (although some populations are annual) and an obligate outcrosser. Within the species, its tolerance of multiple stresses reflects its high genetic diversity. Different populations, even over small geographic areas, have both diploid and autotetraploid variants. At least one report has identified triploid individuals. The autotetraploid populations are found across Northern and Central Europe while diploids occur in Eastern Europe and along the southern Baltic coast; the two ploidies overlap in the Carpathian Mountains.
Whole-genome duplication or autopolyploidy has often been implicated as contributing to speciation and to the development of novel phenotype variations. There have been a number of studies of the process as it occurred in A. arenosa, the subsequent split into multiple lineages, radiation across the landscape to diverse habitats, and the relationship between tetraploid and diploid genotypes. In at least two cases, selection has apparently acted on an introgressed locus.[6,7]
The original autotetraploid genotype apparently arose from a single diploid population in the Carpathian Mountains, subsequently radiating across Europe and becoming a collection of at least 4 distinct genetic lineages associated with a diversity of geographies and habitats. In the process, a perennial mountain form stabilized associated mainly with rocky outcrops. In the last 200 years, however, a diploid, annual, ruderal form has appeared along railways. Although diploid lineages in general are not limited to rail lines, the plants there are of one genetic lineage, certainly consistent with the obvious migration corridor along the rails.
Acknowledgement – This page was put together by John Cheeseman who offers special thanks to Levi Yant, Kirsten Bomblies, Filip Kolar, Ewa Maria Przedpełska-Wąsowicz and Jouko Lehmuskallio for assistance with the text and photos.
Arabidopsis arenosa riding the rails
One of the more interesting curiosities regarding the distribution and life history of A. arenosa is its distribution along railway beds. Clearly, railway construction and maintenance are major disturbances. In addition, railways are obvious corridors for plant (and animal) migration. But beyond that, railway construction introduces exotic materials which can greatly change the underlying soil properties, creating a novel and specific habitat. For example, the importing of uniform bed materials usually results in a substrate with a higher pH than the adjacent soils, and varying but rather high levels of nutrients. The aberrant nutrient levels seem to go away with time, but the pH difference does not.
Colonization of railways by A. arenosa is clearly a “recent” phenomenon since railways have only been in existence for about 200 years. The arrival of A. arenosa on the lines resulted in a number of phenotypic, genomic and transcriptomic changes in the populatioin that colonized the new habitat. For example, the railway populations are diploid, monocarpic, rapid cycling and do not respond to vernalization. Nearby mountain tetraploids, on the other hand, are perennial, polycarpic, and vernalization responsive. The differences are at least partly due to differences in expression of FLC (Flowering Locus C); railway plants show very low FLC expression associated with their much reduced vernalization response. Plants from the mountains, on the other hand, show transient FLC repression by vernalization.
On her John Innes Center webpage, Kirsten Bomblies proposes that the railway genotype, or at least the most abundant lineage, arose only once and now ranges from Sweden to Southwestern Germany to Central Poland. She does note, however, that there is also one locally abundant “isolated perhaps independent railway colonization that has a distinct phenotype with respect to flowering gene expression (high expression of FLC, despite early flowering). This population is clearly a hybrid between the abundant railway type, and the adjacent mountain type. How it became early flowering despite its high FLC expression, however, remains mysterious.”
Railway and mountain genotypes also vary with respect to differences in the expression of cold and heat stress-responsive genes. These are constitutively expressed in the railway plants – as might be expected given the sometimes very exposed conditions of the lines – and they have higher basal heat and cold tolerance than the mountain plants. [Of course, what is “expected” in plant biology and what actually occurs are not necessarily the same thing.] The gene responsible, LHY, is a circadian clock regulator which also regulates many of the differentially expressed cold- and heat-responsive genes. There are 18 polymorphisms occurring at higher frequency in the railway population, 9 encoding amino acid changes, and all clustered in one small region of the gene. Interestingly, the circadian clock function is not altered while the thermal tolerances are. [KB] Overall, some 20 loci have been implicated as reflecting positive selection associated with weediness (i.e. the ruderal life style) in the railway plants.
At this point, there are only a few folks studying this particular phenomenon, but the promise it holds for understanding evolution as well as stress adaptation warrants continued, and greater, attention.
Arabidopsis arenosa populations show serious heavy metal tolerance
Variations in heavy metal tolerance (i.e. zinc, cadmium and lead) are also demonstrable in A. arenosa. Przedpełska & Wierzbicka examined a number of morphological traits in two diploid population from Poland, one from a zinc-lead waste heap and one from a national park site with low heavy metal content in the soil. The comparisons were done both in the native soils in the field and in a common garden, growth chamber, study. Waste-heap plants are shorter, multi-stemmed and brighter green, and their leaves narrower, thicker and with fewer trichomes. The plants from non-polluted sites, in contrast, are taller but with single flowering stalks. These characteristics are expressed both in the field and in common gardens and they are heritable. Although this study included no analysis of any sub-cellular characteristics (e.g. proteomics, metabolomics, transcriptomics or genomics), the authors interpreted the waste-heap phenology as indicating genetic adaptation to xerothermic as well as heavy metal conditions.
The level of tolerance to heavy metals (zinc, cadmium, and lead) was quantified (at least approximately) by comparing seedling root growth responses. The tolerance of the waste-heap populations to all of the metals is high, and exceeds that of four other predominant plant species growing on the same waste heap (Silene vulgaris, Dianthus carthusianorum, Biscutella laevigata, and Armeria maritima).
At this point, it should be noted that heavy metal tolerance has also been studied to a much greater extent in another Arabidopsis species often compared with A. arenosa, i.e. A. halleri. In that case, many of those studies have emphasized the molecular level. A partial list of A. halleri citations from PubMed can be found here. In both cases, the existence of tolerant and non-tolerant populations portends promise for comparative analysis at the molecular level.
Adaptation to serpentine soils
It is doubtless true that anyone who studies eXtremophytes takes a certain joy in the unique beauty of “their” ecosystem, but also becomes a willing cheerleader for how radically eXtreme it is and, consequently, how amazing their chosen species is.
With respect to A. arenosa, one group of big fans appreciates its outstanding adaptation to serpentine soils. [For a more complete but not overwhelming introduction to such soils, click here.] Arnold et al. tout serpentine barrens as posing “extreme hazards for plant colonists.” Among these, they list dramatically skewed elemental contents (e.g. a high Mg:Ca ratio and low K, N, S and P), phytotoxic levels of heavy metals (especially Ni, but in some places very low levels of Cu and Zn), and drought risk associated with high soil porosity and low canopy cover.
Despite the apparent hostility of the soil, however, the A.arenosa population adapted to a serpentine site has (in comparison to populations from nearby non-serpentine sites), high leaf levels of K and S, low levels of Ni and Mg, low Mg:Ca ratios and “comparatively high” levels of the micronutrients Cu, Zn and Cd.
At the molecular level, 24 autotetraploid individuals from 3 populations have been barcoded and compared using the A. lyrata genome as a reference. Extensive shared variation between the populations suggest either recent colonization of the serpentine site by multiple individuals, or ongoing gene flow between the populations. The results of the study by Arnold et al., however, were not consistent with the latter. Their analyses also contradicted their initial expectation that a single colonization event would be reflected as having been an extreme bottleneck. Modeling of the results indicated a divergence time between the serpentine and closest non-serpentine populations as only about 3,000 generations; i.e. the colonization of the barren was quite recent. This is much lower than the average time it takes to fix rare or intermediate-frequency neutral mutations in a finite population [source].
Overall, some 162 genes have been identified as under selection, covering a broad range of processes. About half of the genes are identified with processes or functions related to the challenges of the barrens (e.g. high Mg tolerance, ion transport, Ca-signaling), and each of the processes is represented by several genes. Some of the top loci are implicated in stress signaling and tolerance, such as early responsive to dehydration stress protein 4 (ERD4) and high expression of osmotically responsive genes 2 (HOS2).
A final interesting result was that some of the alleles under selection appear to have been transferred from diploid A. lyrata. Additionally, 11 genes have distinct alleles associated with the serpentine colonization and indicative of convergent evolution. In all, the gene overlap between the species supports the idea that the adaptations were qualitatively similar despite the fact that A. lyrata is diploid, and A. arenosa is tetraploid.
The genome of Arabidopsis arenosa has apparently been sequenced but as yet there is no assembly or publication associated with it. The sequencing was done at JGI/Berkeley as part of the Arabidopsis Comparative Genomics project, Luca Comai (PI). Raw data are available through NCBI or JGI.
In addition there are 15 other BioProjects listed at NCBI, including an earlier genome sequencing project from Cold Springs Harbor Laboratory. Alas, that project and a number of the others have no publicly available data associated with them. For additional sequencing data availability (BioSamples, Nucleotides, SRAs etc.) at NCBI, click here.
Arabidopsis arenosa is the focus of studies addressing a wide range of topics. Therefore, the list below was generated by a search of PubMed without restriction to any particular level of organization. Additional publications not indexed in PubMed are, of course, not included. Abstracts and/or full text versions can be accessed by clicking doi, PMID or PMC numbers. For a list of all PubMedCentral (PMC) listed publications including A.arenosa, click here. This link takes you to the NCBI site.
- Bjerkan, KN, Hornslien, KS, Johannessen, IM, Krabberød, AK, van Ekelenburg, YS, Kalantarian, M et al. (2019) Genetic variation and temperature affects hybrid barriers during interspecific hybridization. Plant J. :. doi: 10.1111/tpj.14523. PubMed PMID:31487093 .
- Szopiński, M, Sitko, K, Gieroń, Ż, Rusinowski, S, Corso, M, Hermans, C et al. (2019) Toxic Effects of Cd and Zn on the Photosynthetic Apparatus of the Arabidopsis halleri and Arabidopsis arenosa Pseudo-Metallophytes. Front Plant Sci 10:748. doi: 10.3389/fpls.2019.00748. PubMed PMID:31244873 PubMed Central PMC6563759.
- Wos, G, Mořkovská, J, Bohutínská, M, Šrámková, G, Knotek, A, Lučanová, M et al. (2019) Role of ploidy in colonization of alpine habitats in natural populations of Arabidopsis arenosa. Ann. Bot. :. doi: 10.1093/aob/mcz070. PubMed PMID:31185073 .
- Preite, V, Sailer, C, Syllwasschy, L, Bray, S, Ahmadi, H, Krämer, U et al. (2019) Convergent evolution in Arabidopsis halleri and Arabidopsis arenosa on calamine metalliferous soils. Philos. Trans. R. Soc. Lond., B, Biol. Sci. 374:20180243. doi: 10.1098/rstb.2018.0243. PubMed PMID:31154972 PubMed Central PMC6560266.
- Monnahan, P, Kolář, F, Baduel, P, Sailer, C, Koch, J, Horvath, R et al. (2019) Pervasive population genomic consequences of genome duplication in Arabidopsis arenosa. Nat Ecol Evol 3:457-468. doi: 10.1038/s41559-019-0807-4. PubMed PMID:30804518 .
- Molina-Henao, YF, Hopkins, R (2019) Autopolyploid lineage shows climatic niche expansion but not divergence in Arabidopsis arenosa. Am. J. Bot. 106:61-70. doi: 10.1002/ajb2.1212. PubMed PMID:30609009 .
- Rozpądek, P, Nosek, M, Domka, A, Ważny, R, Jędrzejczyk, R, Tokarz, K et al. (2019) Acclimation of the photosynthetic apparatus and alterations in sugar metabolism in response to inoculation with endophytic fungi. Plant Cell Environ. 42:1408-1423. doi: 10.1111/pce.13485. PubMed PMID:30516827 .
- Guggisberg, A, Liu, X, Suter, L, Mansion, G, Fischer, MC, Fior, S et al. (2018) The genomic basis of adaptation to calcareous and siliceous soils in Arabidopsis lyrata. Mol. Ecol. 27:5088-5103. doi: 10.1111/mec.14930. PubMed PMID:30411828 .
- Abeysinghe, JK, Lam, KM, Ng, DW (2019) Differential regulation and interaction of homoeologous WRKY18 and WRKY40 in Arabidopsis allotetraploids and biotic stress responses. Plant J. 97:352-367. doi: 10.1111/tpj.14124. PubMed PMID:30307072 .
- Domka, A, Rozpądek, P, Ważny, R, Turnau, K (2019) Mucor sp.-An endophyte of Brassicaceae capable of surviving in toxic metal-rich sites. J. Basic Microbiol. 59:24-37. doi: 10.1002/jobm.201800406. PubMed PMID:30303545 .
- Borymski, S, Cycoń, M, Beckmann, M, Mur, LAJ, Piotrowska-Seget, Z (2018) Plant Species and Heavy Metals Affect Biodiversity of Microbial Communities Associated With Metal-Tolerant Plants in Metalliferous Soils. Front Microbiol 9:1425. doi: 10.3389/fmicb.2018.01425. PubMed PMID:30061867 PubMed Central PMC6054959.
- Baduel, P, Hunter, B, Yeola, S, Bomblies, K (2018) Genetic basis and evolution of rapid cycling in railway populations of tetraploid Arabidopsis arenosa. PLoS Genet. 14:e1007510. doi: 10.1371/journal.pgen.1007510. PubMed PMID:29975688 PubMed Central PMC6049958.
- Li, L, Liu, B, Deng, X, Zhao, H, Li, H, Xing, S et al. (2018) Evolution of interspecies unilateral incompatibility in the relatives of Arabidopsis thaliana. Mol. Ecol. 27:2742-2753. doi: 10.1111/mec.14707. PubMed PMID:29717521 .
- Novikova, PY, Hohmann, N, Van de Peer, Y (2018) Polyploid Arabidopsis species originated around recent glaciation maxima. Curr. Opin. Plant Biol. 42:8-15. doi: 10.1016/j.pbi.2018.01.005. PubMed PMID:29448159 .
- Hohmann, N, Koch, MA (2017) An Arabidopsis introgression zone studied at high spatio-temporal resolution: interglacial and multiple genetic contact exemplified using whole nuclear and plastid genomes. BMC Genomics 18:810. doi: 10.1186/s12864-017-4220-6. PubMed PMID:29058582 PubMed Central PMC5651623.
- Ng, DW, Chen, HH, Chen, ZJ (2017) Heterologous protein-DNA interactions lead to biased allelic expression of circadian clock genes in interspecific hybrids. Sci Rep 7:45087. doi: 10.1038/srep45087. PubMed PMID:28345627 PubMed Central PMC5366859.
- Lafon-Placette, C, Johannessen, IM, Hornslien, KS, Ali, MF, Bjerkan, KN, Bramsiepe, J et al. (2017) Endosperm-based hybridization barriers explain the pattern of gene flow between Arabidopsis lyrata and Arabidopsis arenosa in Central Europe. Proc. Natl. Acad. Sci. U.S.A. 114:E1027-E1035. doi: 10.1073/pnas.1615123114. PubMed PMID:28115687 PubMed Central PMC5307485.
- Novikova, PY, Tsuchimatsu, T, Simon, S, Nizhynska, V, Voronin, V, Burns, R et al. (2017) Genome Sequencing Reveals the Origin of the Allotetraploid Arabidopsis suecica. Mol. Biol. Evol. 34:957-968. doi: 10.1093/molbev/msw299. PubMed PMID:28087777 PubMed Central PMC5400380.
- Yant, L, Bomblies, K (2017) Genomic studies of adaptive evolution in outcrossing Arabidopsis species. Curr. Opin. Plant Biol. 36:9-14. doi: 10.1016/j.pbi.2016.11.018. PubMed PMID:27988391 .
- Arnold, BJ, Lahner, B, DaCosta, JM, Weisman, CM, Hollister, JD, Salt, DE et al. (2016) Borrowed alleles and convergence in serpentine adaptation. Proc. Natl. Acad. Sci. U.S.A. 113:8320-5. doi: 10.1073/pnas.1600405113. PubMed PMID:27357660 PubMed Central PMC4961121.
- Kolář, F, Fuxová, G, Záveská, E, Nagano, AJ, Hyklová, L, Lučanová, M et al. (2016) Northern glacial refugia and altitudinal niche divergence shape genome-wide differentiation in the emerging plant model Arabidopsis arenosa. Mol. Ecol. 25:3929-49. doi: 10.1111/mec.13721. PubMed PMID:27288974 .
- Baduel, P, Arnold, B, Weisman, CM, Hunter, B, Bomblies, K (2016) Habitat-Associated Life History and Stress-Tolerance Variation in Arabidopsis arenosa. Plant Physiol. 171:437-51. doi: 10.1104/pp.15.01875. PubMed PMID:26941193 PubMed Central PMC4854687.
- Solhaug, EM, Ihinger, J, Jost, M, Gamboa, V, Marchant, B, Bradford, D et al. (2016) Environmental Regulation of Heterosis in the Allopolyploid Arabidopsis suecica. Plant Physiol. 170:2251-63. doi: 10.1104/pp.16.00052. PubMed PMID:26896394 PubMed Central PMC4825151.
- Bomblies, K, Jones, G, Franklin, C, Zickler, D, Kleckner, N (2016) The challenge of evolving stable polyploidy: could an increase in "crossover interference distance" play a central role?. Chromosoma 125:287-300. doi: 10.1007/s00412-015-0571-4. PubMed PMID:26753761 PubMed Central PMC4830878.
- Kirkbride, RC, Yu, HH, Nah, G, Zhang, C, Shi, X, Chen, ZJ et al. (2015) An Epigenetic Role for Disrupted Paternal Gene Expression in Postzygotic Seed Abortion in Arabidopsis Interspecific Hybrids. Mol Plant 8:1766-75. doi: 10.1016/j.molp.2015.09.009. PubMed PMID:26409189 .
- Shi, X, Zhang, C, Ko, DK, Chen, ZJ (2015) Genome-Wide Dosage-Dependent and -Independent Regulation Contributes to Gene Expression and Evolutionary Novelty in Plant Polyploids. Mol. Biol. Evol. 32:2351-66. doi: 10.1093/molbev/msv116. PubMed PMID:25976351 PubMed Central PMC6281156.
- Muir, G, Ruiz-Duarte, P, Hohmann, N, Mable, BK, Novikova, P, Schmickl, R et al. (2015) Exogenous selection rather than cytonuclear incompatibilities shapes asymmetrical fitness of reciprocal Arabidopsis hybrids. Ecol Evol 5:1734-45. doi: 10.1002/ece3.1474. PubMed PMID:25937915 PubMed Central PMC4409420.
- Arnold, B, Kim, ST, Bomblies, K (2015) Single Geographic Origin of a Widespread Autotetraploid Arabidopsis arenosa Lineage Followed by Interploidy Admixture. Mol. Biol. Evol. 32:1382-95. doi: 10.1093/molbev/msv089. PubMed PMID:25862142 .
- Burkart-Waco, D, Ngo, K, Lieberman, M, Comai, L (2015) Perturbation of parentally biased gene expression during interspecific hybridization. PLoS ONE 10:e0117293. doi: 10.1371/journal.pone.0117293. PubMed PMID:25719202 PubMed Central PMC4342222.
- Wright, KM, Arnold, B, Xue, K, Šurinová, M, O'Connell, J, Bomblies, K et al. (2015) Selection on meiosis genes in diploid and tetraploid Arabidopsis arenosa. Mol. Biol. Evol. 32:944-55. doi: 10.1093/molbev/msu398. PubMed PMID:25543117 PubMed Central PMC4379401.
- Hohmann, N, Schmickl, R, Chiang, TY, Lučanová, M, Kolář, F, Marhold, K et al. (2014) Taming the wild: resolving the gene pools of non-model Arabidopsis lineages. BMC Evol. Biol. 14:224. doi: 10.1186/s12862-014-0224-x. PubMed PMID:25344686 PubMed Central PMC4216345.
- Wolf, DE, Steets, JA, Houliston, GJ, Takebayashi, N (2014) Genome size variation and evolution in allotetraploid Arabidopsis kamchatica and its parents, Arabidopsis lyrata and Arabidopsis halleri. AoB Plants 6:. doi: 10.1093/aobpla/plu025. PubMed PMID:24887004 PubMed Central PMC4076644.
- Ng, DW, Shi, X, Nah, G, Chen, ZJ (2014) High-throughput RNA-seq for allelic or locus-specific expression analysis in Arabidopsis-related species, hybrids, and allotetraploids. Methods Mol. Biol. 1112:33-48. doi: 10.1007/978-1-62703-773-0_3. PubMed PMID:24478006 .
- Henry, IM, Dilkes, BP, Tyagi, A, Gao, J, Christensen, B, Comai, L et al. (2014) The BOY NAMED SUE quantitative trait locus confers increased meiotic stability to an adapted natural allopolyploid of Arabidopsis. Plant Cell 26:181-94. doi: 10.1105/tpc.113.120626. PubMed PMID:24464296 PubMed Central PMC3963567.
- Higgins, JD, Wright, KM, Bomblies, K, Franklin, FC (2014) Cytological techniques to analyze meiosis in Arabidopsis arenosa for investigating adaptation to polyploidy. Front Plant Sci 4:546. doi: 10.3389/fpls.2013.00546. PubMed PMID:24427164 PubMed Central PMC3879461.
- Yant, L, Hollister, JD, Wright, KM, Arnold, BJ, Higgins, JD, Franklin, FCH et al. (2013) Meiotic adaptation to genome duplication in Arabidopsis arenosa. Curr. Biol. 23:2151-6. doi: 10.1016/j.cub.2013.08.059. PubMed PMID:24139735 PubMed Central PMC3859316.
- Nadgórska-Socha, A, Ptasiński, B, Kita, A (2013) Heavy metal bioaccumulation and antioxidative responses in Cardaminopsis arenosa and Plantago lanceolata leaves from metalliferous and non-metalliferous sites: a field study. Ecotoxicology 22:1422-34. doi: 10.1007/s10646-013-1129-y. PubMed PMID:24085602 PubMed Central PMC3824952.
- Tian, L, Li, X, Ha, M, Zhang, C, Chen, ZJ (2014) Genetic and epigenetic changes in a genomic region containing MIR172 in Arabidopsis allopolyploids and their progenitors. Heredity (Edinb) 112:207-14. doi: 10.1038/hdy.2013.94. PubMed PMID:24065179 PubMed Central PMC3907107.
- Turisová, I, Štrba, T, Aschenbrenner, Š, Andráš, P (2013) Arabidopsis arenosa (L.) Law. on metalliferous and non-metalliferous sites in central Slovakia. Bull Environ Contam Toxicol 91:469-74. doi: 10.1007/s00128-013-1074-8. PubMed PMID:23912231 .
- Burkart-Waco, D, Ngo, K, Dilkes, B, Josefsson, C, Comai, L (2013) Early disruption of maternal-zygotic interaction and activation of defense-like responses in Arabidopsis interspecific crosses. Plant Cell 25:2037-55. doi: 10.1105/tpc.112.108258. PubMed PMID:23898028 PubMed Central PMC3723611.
- Hollister, JD, Arnold, BJ, Svedin, E, Xue, KS, Dilkes, BP, Bomblies, K et al. (2012) Genetic adaptation associated with genome-doubling in autotetraploid Arabidopsis arenosa. PLoS Genet. 8:e1003093. doi: 10.1371/journal.pgen.1003093. PubMed PMID:23284289 PubMed Central PMC3527224.
- Schmickl, R, Paule, J, Klein, J, Marhold, K, Koch, MA (2012) The evolutionary history of the Arabidopsis arenosa complex: diverse tetraploids mask the Western Carpathian center of species and genetic diversity. PLoS ONE 7:e42691. doi: 10.1371/journal.pone.0042691. PubMed PMID:22880083 PubMed Central PMC3411824.
- Shi, X, Ng, DW, Zhang, C, Comai, L, Ye, W, Chen, ZJ et al. (2012) Cis- and trans-regulatory divergence between progenitor species determines gene-expression novelty in Arabidopsis allopolyploids. Nat Commun 3:950. doi: 10.1038/ncomms1954. PubMed PMID:22805557 .
- Kenderesová, L, Stanová, A, Pavlovkin, J, Durisová, E, Nadubinská, M, Ciamporová, M et al. (2012) Early Zn2+-induced effects on membrane potential account for primary heavy metal susceptibility in tolerant and sensitive Arabidopsis species. Ann. Bot. 110:445-59. doi: 10.1093/aob/mcs111. PubMed PMID:22645116 PubMed Central PMC3394654.
- Pontvianne, F, Blevins, T, Chandrasekhara, C, Feng, W, Stroud, H, Jacobsen, SE et al. (2012) Histone methyltransferases regulating rRNA gene dose and dosage control in Arabidopsis. Genes Dev. 26:945-57. doi: 10.1101/gad.182865.111. PubMed PMID:22549957 PubMed Central PMC3347792.
- Burkart-Waco, D, Josefsson, C, Dilkes, B, Kozloff, N, Torjek, O, Meyer, R et al. (2012) Hybrid incompatibility in Arabidopsis is determined by a multiple-locus genetic network. Plant Physiol. 158:801-12. doi: 10.1104/pp.111.188706. PubMed PMID:22135429 PubMed Central PMC3271768.
- Jørgensen, MH, Ehrich, D, Schmickl, R, Koch, MA, Brysting, AK (2011) Interspecific and interploidal gene flow in Central European Arabidopsis (Brassicaceae). BMC Evol. Biol. 11:346. doi: 10.1186/1471-2148-11-346. PubMed PMID:22126410 PubMed Central PMC3247304.
- Ng, DW, Zhang, C, Miller, M, Shen, Z, Briggs, SP, Chen, ZJ et al. (2012) Proteomic divergence in Arabidopsis autopolyploids and allopolyploids and their progenitors. Heredity (Edinb) 108:419-30. doi: 10.1038/hdy.2011.92. PubMed PMID:22009271 PubMed Central PMC3313054.
- Kim, ED, Chen, ZJ (2011) Unstable transcripts in Arabidopsis allotetraploids are associated with nonadditive gene expression in response to abiotic and biotic stresses. PLoS ONE 6:e24251. doi: 10.1371/journal.pone.0024251. PubMed PMID:21897874 PubMed Central PMC3163679.
- Schmickl, R, Koch, MA (2011) Arabidopsis hybrid speciation processes. Proc. Natl. Acad. Sci. U.S.A. 108:14192-7. doi: 10.1073/pnas.1104212108. PubMed PMID:21825128 PubMed Central PMC3161561.
- Ng, DW, Zhang, C, Miller, M, Palmer, G, Whiteley, M, Tholl, D et al. (2011) cis- and trans-Regulation of miR163 and target genes confers natural variation of secondary metabolites in two Arabidopsis species and their allopolyploids. Plant Cell 23:1729-40. doi: 10.1105/tpc.111.083915. PubMed PMID:21602291 PubMed Central PMC3123960.
- Costa-Nunes, P, Pontes, O, Preuss, SB, Pikaard, CS Extra views on RNA-dependent DNA methylation and MBD6-dependent heterochromatin formation in nucleolar dominance. Nucleus 1:254-9. doi: 10.4161/nucl.1.3.11741. PubMed PMID:21327072 PubMed Central PMC3027031.
- Ha, M, Ng, DW, Li, WH, Chen, ZJ (2011) Coordinated histone modifications are associated with gene expression variation within and between species. Genome Res. 21:590-8. doi: 10.1101/gr.116467.110. PubMed PMID:21324879 PubMed Central PMC3065706.
- Roy, S, Ueda, M, Kadowaki, K, Tsutsumi, N (2010) Different status of the gene for ribosomal protein S16 in the chloroplast genome during evolution of the genus Arabidopsis and closely related species. Genes Genet. Syst. 85:319-26. . PubMed PMID:21317544 .
- Moraes, IC, Lermontova, I, Schubert, I (2011) Recognition of A. thaliana centromeres by heterologous CENH3 requires high similarity to the endogenous protein. Plant Mol. Biol. 75:253-61. doi: 10.1007/s11103-010-9723-3. PubMed PMID:21190064 .
- Chang, PL, Dilkes, BP, McMahon, M, Comai, L, Nuzhdin, SV (2010) Homoeolog-specific retention and use in allotetraploid Arabidopsis suecica depends on parent of origin and network partners. Genome Biol. 11:R125. doi: 10.1186/gb-2010-11-12-r125. PubMed PMID:21182768 PubMed Central PMC3046485.
- Ravi, M, Kwong, PN, Menorca, RM, Valencia, JT, Ramahi, JS, Stewart, JL et al. (2010) The rapidly evolving centromere-specific histone has stringent functional requirements in Arabidopsis thaliana. Genetics 186:461-71. doi: 10.1534/genetics.110.120337. PubMed PMID:20628040 PubMed Central PMC2954480.
- Moison, M, Roux, F, Quadrado, M, Duval, R, Ekovich, M, Lê, DH et al. (2010) Cytoplasmic phylogeny and evidence of cyto-nuclear co-adaptation in Arabidopsis thaliana. Plant J. 63:728-38. doi: 10.1111/j.1365-313X.2010.04275.x. PubMed PMID:20553420 .
- Bomblies, K, Weigel, D (2010) Arabidopsis and relatives as models for the study of genetic and genomic incompatibilities. Philos. Trans. R. Soc. Lond., B, Biol. Sci. 365:1815-23. doi: 10.1098/rstb.2009.0304. PubMed PMID:20439283 PubMed Central PMC2871890.
- Rangwala, SH, Richards, EJ (2010) The structure, organization and radiation of Sadhu non-long terminal repeat retroelements in Arabidopsis species. Mob DNA 1:10. doi: 10.1186/1759-8753-1-10. PubMed PMID:20226007 PubMed Central PMC2848041.
- Carvalho, A, Delgado, M, Barão, A, Frescatada, M, Ribeiro, E, Pikaard, CS et al. (2010) Chromosome and DNA methylation dynamics during meiosis in the autotetraploid Arabidopsis arenosa. Sex. Plant Reprod. 23:29-37. doi: 10.1007/s00497-009-0115-2. PubMed PMID:20165961 .
- Yin, P, Kang, J, He, F, Qu, LJ, Gu, H (2010) The origin of populations of Arabidopsis thaliana in China, based on the chloroplast DNA sequences. BMC Plant Biol. 10:22. doi: 10.1186/1471-2229-10-22. PubMed PMID:20141622 PubMed Central PMC2827422.
- Nah, G, Jeffrey Chen, Z (2010) Tandem duplication of the FLC locus and the origin of a new gene in Arabidopsis related species and their functional implications in allopolyploids. New Phytol. 186:228-38. doi: 10.1111/j.1469-8137.2009.03164.x. PubMed PMID:20100201 .
- Ha, M, Lu, J, Tian, L, Ramachandran, V, Kasschau, KD, Chapman, EJ et al. (2009) Small RNAs serve as a genetic buffer against genomic shock in Arabidopsis interspecific hybrids and allopolyploids. Proc. Natl. Acad. Sci. U.S.A. 106:17835-40. doi: 10.1073/pnas.0907003106. PubMed PMID:19805056 PubMed Central PMC2757398.
- Wright, KM, Pires, JC, Madlung, A (2009) Mitotic instability in resynthesized and natural polyploids of the genus Arabidopsis (Brassicaceae). Am. J. Bot. 96:1656-64. doi: 10.3732/ajb.0800270. PubMed PMID:21622352 .
- Walia, H, Josefsson, C, Dilkes, B, Kirkbride, R, Harada, J, Comai, L et al. (2009) Dosage-dependent deregulation of an AGAMOUS-LIKE gene cluster contributes to interspecific incompatibility. Curr. Biol. 19:1128-32. doi: 10.1016/j.cub.2009.05.068. PubMed PMID:19559614 PubMed Central PMC6754343.
- Yu, Z, Haage, K, Streit, VE, Gierl, A, Ruiz, RA (2009) A large number of tetraploid Arabidopsis thaliana lines, generated by a rapid strategy, reveal high stability of neo-tetraploids during consecutive generations. Theor. Appl. Genet. 118:1107-19. doi: 10.1007/s00122-009-0966-9. PubMed PMID:19205656 .
- Ha, M, Kim, ED, Chen, ZJ (2009) Duplicate genes increase expression diversity in closely related species and allopolyploids. Proc. Natl. Acad. Sci. U.S.A. 106:2295-300. doi: 10.1073/pnas.0807350106. PubMed PMID:19168631 PubMed Central PMC2650150.
- Beaulieu, J, Jean, M, Belzile, F (2009) The allotetraploid Arabidopsis thaliana-Arabidopsis lyrata subsp. petraea as an alternative model system for the study of polyploidy in plants. Mol. Genet. Genomics 281:421-35. doi: 10.1007/s00438-008-0421-7. PubMed PMID:19148683 .
- Ni, Z, Kim, ED, Ha, M, Lackey, E, Liu, J, Zhang, Y et al. (2009) Altered circadian rhythms regulate growth vigour in hybrids and allopolyploids. Nature 457:327-31. doi: 10.1038/nature07523. PubMed PMID:19029881 PubMed Central PMC2679702.
- Hazzouri, KM, Mohajer, A, Dejak, SI, Otto, SP, Wright, SI (2008) Contrasting patterns of transposable-element insertion polymorphism and nucleotide diversity in autotetraploid and allotetraploid Arabidopsis species. Genetics 179:581-92. doi: 10.1534/genetics.107.085761. PubMed PMID:18493073 PubMed Central PMC2390634.
- Chen, M, Ha, M, Lackey, E, Wang, J, Chen, ZJ (2008) RNAi of met1 reduces DNA methylation and induces genome-specific changes in gene expression and centromeric small RNA accumulation in Arabidopsis allopolyploids. Genetics 178:1845-58. doi: 10.1534/genetics.107.086272. PubMed PMID:18430920 PubMed Central PMC2323781.
- Kuang, H, Caldwell, KS, Meyers, BC, Michelmore, RW (2008) Frequent sequence exchanges between homologs of RPP8 in Arabidopsis are not necessarily associated with genomic proximity. Plant J. 54:69-80. doi: 10.1111/j.1365-313X.2008.03408.x. PubMed PMID:18182023 .
- Pontes, O, Lawrence, RJ, Silva, M, Preuss, S, Costa-Nunes, P, Earley, K et al. (2007) Postembryonic establishment of megabase-scale gene silencing in nucleolar dominance. PLoS ONE 2:e1157. doi: 10.1371/journal.pone.0001157. PubMed PMID:17987131 PubMed Central PMC2048576.
- Koch, MA, Matschinger, M (2007) Evolution and genetic differentiation among relatives of Arabidopsis thaliana. Proc. Natl. Acad. Sci. U.S.A. 104:6272-7. doi: 10.1073/pnas.0701338104. PubMed PMID:17404224 PubMed Central PMC1851049.
- Lee, HS, Wang, J, Tian, L, Jiang, H, Black, MA, Madlung, A et al. (2004) Sensitivity of 70-mer oligonucleotides and cDNAs for microarray analysis of gene expression in Arabidopsis and its related species. Plant Biotechnol. J. 2:45-57. doi: 10.1046/j.1467-7652.2003.00048.x. PubMed PMID:17166142 PubMed Central PMC2034503.
- Kawabe, A, Charlesworth, D (2007) Patterns of DNA variation among three centromere satellite families in Arabidopsis halleri and A. lyrata. J. Mol. Evol. 64:237-47. doi: 10.1007/s00239-006-0097-8. PubMed PMID:17160639 .
- Beck, JB, Al-Shehbaz, IA, O'Kane, SL Jr, Schaal, BA (2007) Further insights into the phylogeny of Arabidopsis (Brassicaceae) from nuclear Atmyb2 flanking sequence. Mol. Phylogenet. Evol. 42:122-30. doi: 10.1016/j.ympev.2006.06.011. PubMed PMID:16908202 .
- Clauss, MJ, Koch, MA (2006) Poorly known relatives of Arabidopsis thaliana. Trends Plant Sci. 11:449-59. doi: 10.1016/j.tplants.2006.07.005. PubMed PMID:16893672 .
- Josefsson, C, Dilkes, B, Comai, L (2006) Parent-dependent loss of gene silencing during interspecies hybridization. Curr. Biol. 16:1322-8. doi: 10.1016/j.cub.2006.05.045. PubMed PMID:16824920 .
- Jakobsson, M, Hagenblad, J, Tavaré, S, Säll, T, Halldén, C, Lind-Halldén, C et al. (2006) A unique recent origin of the allotetraploid species Arabidopsis suecica: Evidence from nuclear DNA markers. Mol. Biol. Evol. 23:1217-31. doi: 10.1093/molbev/msk006. PubMed PMID:16549398 .
- Wang, J, Tian, L, Lee, HS, Chen, ZJ (2006) Nonadditive regulation of FRI and FLC loci mediates flowering-time variation in Arabidopsis allopolyploids. Genetics 173:965-74. doi: 10.1534/genetics.106.056580. PubMed PMID:16547097 PubMed Central PMC1526503.
- Hall, AE, Kettler, GC, Preuss, D (2006) Dynamic evolution at pericentromeres. Genome Res. 16:355-64. doi: 10.1101/gr.4399206. PubMed PMID:16461884 PubMed Central PMC1415207.
- Sanyal, A, Jackson, SA (2006) Comparative genomics reveals expansion of the FLC region in the genus Arabidopsis. Mol. Genet. Genomics 275:26-34. doi: 10.1007/s00438-005-0063-y. PubMed PMID:16341708 .
- Wang, J, Tian, L, Lee, HS, Wei, NE, Jiang, H, Watson, B et al. (2006) Genomewide nonadditive gene regulation in Arabidopsis allotetraploids. Genetics 172:507-17. doi: 10.1534/genetics.105.047894. PubMed PMID:16172500 PubMed Central PMC1456178.
- Pontes, O, Neves, N, Silva, M, Lewis, MS, Madlung, A, Comai, L et al. (2004) Chromosomal locus rearrangements are a rapid response to formation of the allotetraploid Arabidopsis suecica genome. Proc. Natl. Acad. Sci. U.S.A. 101:18240-5. doi: 10.1073/pnas.0407258102. PubMed PMID:15604143 PubMed Central PMC539792.
- Kawabe, A, Nasuda, S (2005) Structure and genomic organization of centromeric repeats in Arabidopsis species. Mol. Genet. Genomics 272:593-602. doi: 10.1007/s00438-004-1081-x. PubMed PMID:15586291 .
- Ali, HB, Lysak, MA, Schubert, I (2004) Genomic in situ hybridization in plants with small genomes is feasible and elucidates the chromosomal parentage in interspecific Arabidopsis hybrids. Genome 47:954-60. doi: 10.1139/g04-041. PubMed PMID:15499409 .
- Wang, J, Tian, L, Madlung, A, Lee, HS, Chen, M, Lee, JJ et al. (2004) Stochastic and epigenetic changes of gene expression in Arabidopsis polyploids. Genetics 167:1961-73. doi: 10.1534/genetics.104.027896. PubMed PMID:15342533 PubMed Central PMC1471021.
- Cooper, JL, Henikoff, S (2004) Adaptive evolution of the histone fold domain in centromeric histones. Mol. Biol. Evol. 21:1712-8. doi: 10.1093/molbev/msh179. PubMed PMID:15175412 .
- Fiebig, A, Kimport, R, Preuss, D (2004) Comparisons of pollen coat genes across Brassicaceae species reveal rapid evolution by repeat expansion and diversification. Proc. Natl. Acad. Sci. U.S.A. 101:3286-91. doi: 10.1073/pnas.0305448101. PubMed PMID:14970339 PubMed Central PMC365782.
- Säll, T, Jakobsson, M, Lind-Halldén, C, Halldén, C (2003) Chloroplast DNA indicates a single origin of the allotetraploid Arabidopsis suecica. J. Evol. Biol. 16:1019-29. . PubMed PMID:14635917 .
- Pontes, O, Lawrence, RJ, Neves, N, Silva, M, Lee, JH, Chen, ZJ et al. (2003) Natural variation in nucleolar dominance reveals the relationship between nucleolus organizer chromatin topology and rRNA gene transcription in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 100:11418-23. doi: 10.1073/pnas.1932522100. PubMed PMID:14504406 PubMed Central PMC208772.
- Lawrence, RJ, Pikaard, CS (2003) Transgene-induced RNA interference: a strategy for overcoming gene redundancy in polyploids to generate loss-of-function mutations. Plant J. 36:114-21. doi: 10.1046/j.1365-313x.2003.01857.x. PubMed PMID:12974816 .
- Bushell, C, Spielman, M, Scott, RJ (2003) The basis of natural and artificial postzygotic hybridization barriers in Arabidopsis species. Plant Cell 15:1430-42. doi: 10.1105/tpc.010496. PubMed PMID:12782734 PubMed Central PMC156377.
- Comai, L, Tyagi, AP, Lysak, MA (2003) FISH analysis of meiosis in Arabidopsis allopolyploids. Chromosome Res. 11:217-26. . PubMed PMID:12769289 .
- Lind-Halldén, C, Halldén, C, Säll, T (2002) Genetic variation in Arabidopsis suecica and its parental species A. arenosa and A. thaliana. Hereditas 136:45-50. doi: 10.1034/j.1601-5223.2002.1360107.x. PubMed PMID:12184488 .
- Madlung, A, Masuelli, RW, Watson, B, Reynolds, SH, Davison, J, Comai, L et al. (2002) Remodeling of DNA methylation and phenotypic and transcriptional changes in synthetic Arabidopsis allotetraploids. Plant Physiol. 129:733-46. doi: 10.1104/pp.003095. PubMed PMID:12068115 PubMed Central PMC161697.
- Talbert, PB, Masuelli, R, Tyagi, AP, Comai, L, Henikoff, S (2002) Centromeric localization and adaptive evolution of an Arabidopsis histone H3 variant. Plant Cell 14:1053-66. doi: 10.1105/tpc.010425. PubMed PMID:12034896 PubMed Central PMC150606.
- Lewis, MS, Pikaard, CS (2001) Restricted chromosomal silencing in nucleolar dominance. Proc. Natl. Acad. Sci. U.S.A. 98:14536-40. doi: 10.1073/pnas.251424098. PubMed PMID:11734651 PubMed Central PMC64717.