- 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.
- Morgan, EJ, Čertner, M, Lučanová, M, Kubíková, K, Marhold, K, Kolář, F et al. (2020) Niche similarity in diploid-autotetraploid contact zones of Arabidopsis arenosa across spatial scales. Am J Bot :. doi: 10.1002/ajb2.1534. PubMed PMID:32974906 .
- Szopiński, M, Sitko, K, Rusinowski, S, Zieleźnik-Rusinowska, P, Corso, M, Rostański, A et al. (2020) Different strategies of Cd tolerance and accumulation in Arabidopsis halleri and Arabidopsis arenosa. Plant Cell Environ :. doi: 10.1111/pce.13883. PubMed PMID:32890409 .
- Seear, PJ, France, MG, Gregory, CL, Heavens, D, Schmickl, R, Yant, L et al. (2020) A novel allele of ASY3 is associated with greater meiotic stability in autotetraploid Arabidopsis lyrata. PLoS Genet 16:e1008900. doi: 10.1371/journal.pgen.1008900. PubMed PMID:32667955 PubMed Central PMC7392332.
- Morgan, C, Zhang, H, Henry, CE, Franklin, FCH, Bomblies, K (2020) Derived alleles of two axis proteins affect meiotic traits in autotetraploid Arabidopsis arenosa. Proc Natl Acad Sci U S A 117:8980-8988. doi: 10.1073/pnas.1919459117. PubMed PMID:32273390 PubMed Central PMC7183234.
- Baduel, P, Quadrana, L, Hunter, B, Bomblies, K, Colot, V (2019) Relaxed purifying selection in autopolyploids drives transposable element over-accumulation which provides variants for local adaptation. Nat Commun 10:5818. doi: 10.1038/s41467-019-13730-0. PubMed PMID:31862875 PubMed Central PMC6925279.
- Marburger, S, Monnahan, P, Seear, PJ, Martin, SH, Koch, J, Paajanen, P et al. (2019) Interspecific introgression mediates adaptation to whole genome duplication. Nat Commun 10:5218. doi: 10.1038/s41467-019-13159-5. PubMed PMID:31740675 PubMed Central PMC6861236.
- Morgan, C, Wegel, E (2020) Cytological Characterization of Arabidopsis arenosa Polyploids by SIM. Methods Mol Biol 2061:37-46. doi: 10.1007/978-1-4939-9818-0_4. PubMed PMID:31583651 .
- Bjerkan, KN, Hornslien, KS, Johannessen, IM, Krabberød, AK, van Ekelenburg, YS, Kalantarian, M et al. (2020) Genetic variation and temperature affects hybrid barriers during interspecific hybridization. Plant J 101:122-140. 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 124:255-268. doi: 10.1093/aob/mcz070. PubMed PMID:31185073 PubMed Central PMC6758580.
- 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.
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- 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 .
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