In this study, we aimed to systematically assess the frequency at which potentially deleterious phenotypes appear in natural populations of the outcrossing model plant Arabidopsis arenosa, and to establish their underlying genetics. For this purpose, we collected seeds from wild A. arenosa populations and screened over 2,500 plants for unusual phenotypes in the greenhouse. We repeatedly found plants with obvious phenotypic defects, such as small stature and necrotic or chlorotic leaves, among first-generation progeny of wild A. arenosa plants. Such abnormal plants were present in about 10% of maternal sibships, with multiple plants with similar phenotypes in each of these sibships, pointing to a genetic basis of the observed defects. A combination of transcriptome profiling, linkage mapping and genome-wide runs of homozygosity patterns using a newly assembled reference genome indicated a range of underlying genetic architectures associated with phenotypic abnormalities. This included evidence for homozygosity of certain genomic regions, consistent with alleles that are identical by descent being responsible for these defects. Our observations suggest that deleterious alleles with different genetic architectures are segregating at appreciable frequencies in wild A. arenosa populations.

Catalent 73614 Schorndorf Germany

Department of Botany Faculty of Science Charles University 128 01 Prague Czech Republic

Department of Molecular Biology Max Planck Institute for Biology 72076 Tübingen Germany

Department of Plant Developmental Biology Wageningen University and Research 6708 PB Wageningen Netherlands

Institute of Plant Breeding University of Hohenheim 70599 Stuttgart Germany

KWS Saat 37574 Einbeck Germany

The MAMA AI 100 00 Prague Czech Republic

The Sainsbury Laboratory Norwich NR4 7UH UK

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Al-Shehbaz IA, O’Kane SL Jr. 2002. Taxonomy and phylogeny of Arabidopsis (Brassicaceae). Arabidopsis Book. 1:e0001. doi:10.1199/tab.0001. PubMed DOI PMC

Ashktorab H, Cohen RJ. 1992. Facile isolation of genomic DNA from filamentous fungi. Biotechniques. 13(2):198–200. PubMed

Baldwin SJ, Schoen DJ. 2019. Inbreeding depression is difficult to purge in self-incompatible populations of Leavenworthia alabamica. New Phytol. 224(3):1330–1338. doi:10.1111/nph.15963. PubMed DOI

Barragan AC, Collenberg M, Wang J, Lee RRQ, Cher WY, Rabanal FA, Ashkenazy H, Weigel D, Chae E. 2020. A truncated singleton NLR causes hybrid necrosis in Arabidopsis thaliana. Mol Biol Evol. 38(2):557–574. doi:10.1093/molbev/msaa245. PubMed DOI PMC

Barrett SC, Charlesworth D. 1991. Effects of a change in the level of inbreeding on the genetic load. Nature. 352(6335):522–524. doi:10.1038/352522a0. PubMed DOI

Barrett RDH, Schluter D. 2008. Adaptation from standing genetic variation. Trends Ecol Evol. 23(1):38–44. doi:10.1016/j.tree.2007.09.008. PubMed DOI

Bomblies K, Lempe J, Epple P, Warthmann N, Lanz C, Dangl JL, Weigel D. 2007. Autoimmune response as a mechanism for a Dobzhansky-Muller-type incompatibility syndrome in plants. PLoS Biol. 5(9):e236. doi:10.1371/journal.pbio.0050236. PubMed DOI PMC

Bosse M, Megens H-J, Derks MFL, de Cara ÁMR, Groenen MAM. 2019. Deleterious alleles in the context of domestication, inbreeding, and selection. Evol Appl. 12(1):6–17. doi:10.1111/eva.12691. PubMed DOI PMC

Broman KW, Wu H, Sen S, Churchill GA. 2003. R/qtl: QTL mapping in experimental crosses. Bioinformatics. 19(7):889–890. doi:10.1093/bioinformatics/btg112. PubMed DOI

Brown KE, Kelly JK. 2020. Severe inbreeding depression is predicted by the “rare allele load” in Mimulus guttatus. Evolution. 74(3):587–596. doi:10.1111/evo.13876. PubMed DOI

Catchen J, Hohenlohe PA, Bassham S, Amores A, Cresko WA. 2013. Stacks: an analysis tool set for population genomics. Mol Ecol. 22(11):3124–3140. doi:10.1111/mec.12354. PubMed DOI PMC

Chae E, Bomblies K, Kim S-T, Karelina D, Zaidem M, Ossowski S, Martín-Pizarro C, Laitinen RAE, Rowan BA, Tenenboim H, et al. . 2014. Species-wide genetic incompatibility analysis identifies immune genes as hot spots of deleterious epistasis. Cell. 159(6):1341–1351. doi:10.1016/j.cell.2014.10.049. PubMed DOI PMC

Charlesworth D, Charlesworth B. 1987. Inbreeding depression and its evolutionary consequences. Annu Rev Ecol Syst. 18(1):237–268. doi:10.1146/annurev.es.18.110187.001321. DOI

Charlesworth B, Charlesworth D. 1999. The genetic basis of inbreeding depression. Genet Res. 74(3):329–340. doi:10.1017/s0016672399004152. PubMed DOI

Charlesworth D, Willis JH. 2009. The genetics of inbreeding depression. Nat Rev Genet. 10(11):783–796. doi:10.1038/nrg2664. PubMed DOI

Chin C-S, Peluso P, Sedlazeck FJ, Nattestad M, Concepcion GT, Clum A, Dunn C, O’Malley R, Figueroa-Balderas R, Morales-Cruz A, et al. . 2016. Phased diploid genome assembly with single-molecule real-time sequencing. Nat Methods. 13(12):1050–1054. doi:10.1038/nmeth.4035. PubMed DOI PMC

Cingolani P, Platts A, Wang LL, Coon M, Nguyen T, Wang L, Land SJ, Lu X, Ruden DM. 2012. A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3. Fly (Austin). 6(2):80–92. doi:10.4161/fly.19695. PubMed DOI PMC

Clamp M, Cuff J, Searle SM, Barton GJ. 2004. The Jalview Java alignment editor. Bioinformatics. 20(3):426–427. doi:10.1093/bioinformatics/btg430. PubMed DOI

Clo J, Kolár F. 2022. Inbreeding depression in polyploid species: a meta-analysis. Biol Lett. 18(12):20220477. doi:10.1098/rsbl.2022.0477. PubMed DOI PMC

Crow JF. 1991. Why is Mendelian segregation so exact? Bioessays. 13(6):305–312. doi:10.1002/bies.950130609. PubMed DOI

Crow J, Kimura M. 1970. An introduction to population genetics theory. https://www.cabdirect.org/cabdirect/abstract/19710105376

Danecek P, Auton A, Abecasis G, Albers CA, Banks E, DePristo MA, Handsaker RE, Lunter G, Marth GT, Sherry ST, et al. . 2011. The variant call format and VCFtools. Bioinformatics. 27(15):2156–2158. doi:10.1093/bioinformatics/btr330. PubMed DOI PMC

Dixit SP, Singh S, Ganguly I, Bhatia AK, Sharma A, Kumar NA, Dang AK, Jayakumar S. 2020. Genome-wide runs of homozygosity revealed selection signatures in bos indicus. Front Genet. 11:92. doi:10.3389/fgene.2020.00092. PubMed DOI PMC

Do C, Waples RS, Peel D, Macbeth GM, Tillett BJ, Ovenden JR. 2014. Neestimator v2: re-implementation of software for the estimation of contemporary effective population size (Ne) from genetic data. Mol Ecol Resour. 14(1):209–214. doi:10.1111/1755-0998.12157. PubMed DOI

Doyle JJ, Doyle JL. 1987. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemistry. https://worldveg.tind.io/record/33886/

Dukić M, Bomblies K. 2022. Male and female recombination landscapes of diploid Arabidopsis arenosa. Genetics. 220(3):iyab236. doi:10.1093/genetics/iyab236. PubMed DOI PMC

Edgar RC. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32(5):1792–1797. doi:10.1093/nar/gkh340. PubMed DOI PMC

Emms DM, Kelly S. 2019. OrthoFinder: phylogenetic orthology inference for comparative genomics. Genome Biol. 20(1):238. doi:10.1186/s13059-019-1832-y. PubMed DOI PMC

Fisher RA. 1949. Theory of Inbreeding. London: Oliver and Boyd.

Flynn JM, Hubley R, Goubert C, Rosen J, Clark AG, Feschotte C, Smit AF. 2020. RepeatModeler2 for automated genomic discovery of transposable element families. Proc Natl Acad Sci U S A. 117(17):9451–9457. doi:10.1073/pnas.1921046117. PubMed DOI PMC

Gaudeul M, Stenøien HK, Agren J. 2007. Landscape structure, clonal propagation, and genetic diversity in Scandinavian populations of Arabidopsis lyrata (Brassicaceae). Am J Bot. 94(7):1146–1155. doi:10.3732/ajb.94.7.1146. PubMed DOI

Gieroń Ż, Sitko K, Małkowski E. 2021. The different faces of Arabidopsis arenosa—a plant Species for a special purpose. Plants. 10(7):1342. doi:10.3390/plants10071342. PubMed DOI PMC

Gurevich A, Saveliev V, Vyahhi N, Tesler G. 2013. QUAST: quality assessment tool for genome assemblies. Bioinformatics. 29(8):1072–1075. doi:10.1093/bioinformatics/btt086. PubMed DOI PMC

Haddrill PR, Halligan DL, Tomaras D, Charlesworth B. 2007. Reduced efficacy of selection in regions of the Drosophila genome that lack crossing over. Genome Biol. 8(2):R18. doi:10.1186/gb-2007-8-2-r18. PubMed DOI PMC

Hämälä T, Savolainen O. 2019. Genomic patterns of local adaptation under gene flow in Arabidopsis lyrata. Mol Biol Evol. 36(11):2557–2571. doi:10.1093/molbev/msz149. PubMed DOI

Hill WG, Robertson A. 1966. The effect of linkage on limits to artificial selection. Genet Res. 8(3):269–294. doi:10.1017/s0016672300010156. PubMed DOI

Hu TT, Pattyn P, Bakker EG, Cao J, Cheng J-F, Clark RM, Fahlgren N, Fawcett JA, Grimwood J, Gundlach H, et al. . 2011. The Arabidopsis lyrata genome sequence and the basis of rapid genome size change. Nat Genet. 43(5):476–481. doi:10.1038/ng.807. PubMed DOI PMC

Huang S, Kang M, Xu A. 2017. HaploMerger2: rebuilding both haploid sub-assemblies from high-heterozygosity diploid genome assembly. Bioinformatics. 33(16):2577–2579. doi:10.1093/bioinformatics/btx220. PubMed DOI PMC

Husband BC, Schemske DW. 1996. Evolution of the magnitude and timing of inbreeding depression in plants. Evolution. 50(1):54–70. doi:10.2307/2410780. PubMed DOI

Johnson NA. 2010. Hybrid incompatibility genes: remnants of a genomic battlefield? Trends Genet. 26(7):317–325. doi:10.1016/j.tig.2010.04.005. PubMed DOI

Kahle D, Wickham H. 2013. ggmap: spatial visualization with ggplot2. R J. 5(1):144–161. doi:10.32614/RJ-2013-014. DOI

Khan MA, Elias I, Sjölund E, Nylander K, Guimera RV, Schobesberger R, Schmitzberger P, Lagergren J, Arvestad L. 2013. Fastphylo: fast tools for phylogenetics. BMC Bioinformatics. 14(1):334. doi:10.1186/1471-2105-14-334. PubMed DOI PMC

Kim D, Langmead B, Salzberg SL. 2015. HISAT: a fast spliced aligner with low memory requirements. Nat Methods. 12(4):357–360. doi:10.1038/nmeth.3317. PubMed DOI PMC

Koch MA. 2019. The plant model system Arabidopsis set in an evolutionary, systematic, and spatio-temporal context. J Exp Bot. 70(1):55–67. doi:10.1093/jxb/ery340. PubMed DOI

Kolár F, Fuxová G, Záveská E, Nagano AJ, Hyklová L, Lucanová M, Kudoh H, Marhold K. 2016. Northern glacial refugia and altitudinal niche divergence shape genome-wide differentiation in the emerging plant model Arabidopsis arenosa. Mol Ecol. 25(16):3929–3949. doi:10.1111/mec.13721. PubMed DOI

Kumar S, Deng CH, Hunt M, Kirk C, Wiedow C, Rowan D, Wu J, Brewer L. 2020. Homozygosity mapping reveals population history and trait architecture in self-incompatible pear (Pyrus spp.). Front Plant Sci. 11:590846. doi:10.3389/fpls.2020.590846. PubMed DOI PMC

Lande R, Schemske DW, Schultz ST. 1994. High inbreeding depression, selective interference among loci, and the threshold selfing rate for purging recessive lethal mutations. Evolution. 48(4):965–978. doi:10.2307/2410359. PubMed DOI

Langmead B, Salzberg SL. 2012. Fast gapped-read alignment with Bowtie 2. Nat Methods. 9(4):357–359. doi:10.1038/nmeth.1923. PubMed DOI PMC

Larsson A. 2014. AliView: a fast and lightweight alignment viewer and editor for large datasets. Bioinformatics. 30(22):3276–3278. doi:10.1093/bioinformatics/btu531. PubMed DOI PMC

Lencz T, Lambert C, DeRosse P, Burdick KE, Morgan TV, Kane JM, Kucherlapati R, Malhotra AK. 2007. Runs of homozygosity reveal highly penetrant recessive loci in schizophrenia. Proc Natl Acad Sci U S A. 104(50):19942–19947. doi:10.1073/pnas.0710021104. PubMed DOI PMC

Li H. 2013. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. arXiv [q-bioGN]. http://arxiv.org/abs/1303.3997, preprint: not peer reviewed.

Li B, Dewey CN. 2011. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics. 12(1):323. doi:10.1186/1471-2105-12-323. PubMed DOI PMC

Li L, Weigel D. 2021. One hundred years of hybrid necrosis: hybrid autoimmunity as a window into the mechanisms and evolution of plant–pathogen interactions. Annu Rev Phytopathol. 59(1):213–237. doi:10.1146/annurev-phyto-020620-114826. PubMed DOI

Lindholm AK, Dyer KA, Firman RC, Fishman L, Forstmeier W, Holman L, Johannesson H, Knief U, Kokko H, Larracuente AM, et al. . 2016. The ecology and evolutionary dynamics of meiotic drive. Trends Ecol Evol. 31(4):315–326. doi:10.1016/j.tree.2016.02.001. PubMed DOI

Linthorst J, Hulsman M, Holstege H, Reinders M. 2015. Scalable multi whole-genome alignment using recursive exact matching. bioRxiv. [accessed 2020 May 15]:022715. 10.1101/022715, preprint: not peer reviewed. DOI

Lloyd DG, Schoen DJ. 1992. Self- and cross-fertilization in plants. I. Functional dimensions. Int J Plant Sci. 153(3, Part 1):358–369. doi:10.1086/297040. DOI

Love MI, Huber W, Anders S. 2014. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15(12):550. doi:10.1186/s13059-014-0550-8. PubMed DOI PMC

Lynch M. 1991. The genetic interpretation of inbreeding depression and outbreeding depression. Evolution. 45(3):622–629. doi:10.2307/2409915. PubMed DOI

Lynch M. 2010. Evolution of the mutation rate. Trends Genet. 26(8):345–352. doi:10.1016/j.tig.2010.05.003. PubMed DOI PMC

McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, Garimella K, Altshuler D, Gabriel S, Daly M, et al. . 2010. The genome analysis toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20(9):1297–1303. doi:10.1101/gr.107524.110. PubMed DOI PMC

Menzel M, Sletvold N, Ågren J, Hansson B. 2015. Inbreeding affects gene expression differently in two self-incompatible Arabidopsis lyrata populations with similar levels of inbreeding depression. Mol Biol Evol. 32(8):2036–2047. doi:10.1093/molbev/msv086. PubMed DOI PMC

Moyle LC, Jewell CP, Kostyun JL. 2014. Fertile approaches to dissecting mechanisms of premating and postmating prezygotic reproductive isolation. Curr Opin Plant Biol. 18:16–23. doi:10.1016/j.pbi.2013.12.005. PubMed DOI

Papadopoulou GV, Maedicke A, Grosser K, van Dam NM, Martínez-Medina A. 2018. Defence signalling marker gene responses to hormonal elicitation differ between roots and shoots. AoB Plants. 10(3):ly031. doi:10.1093/aobpla/ply031. PubMed DOI PMC

Patterson N, Price AL, Reich D. 2006. Population structure and eigenanalysis. PLoS Genet. 2(12):e190. doi:10.1371/journal.pgen.0020190. PubMed DOI PMC

Pavan S, Delvento C, Mazzeo R, Ricciardi F. 2021. Almond diversity and homozygosity define structure, kinship, inbreeding, and linkage disequilibrium in cultivated germplasm, and reveal genomic associations with nut and seed weight. Horticulture. doi:10.1038/s41438-020-00447-1/6446605. PubMed DOI PMC

Peripolli E, Munari DP, Silva MVGB, Lima ALF, Irgang R, Baldi F. 2017. Runs of homozygosity: current knowledge and applications in livestock. Anim Genet. 48(3):255–271. doi:10.1111/age.12526. PubMed DOI

Perlman RL. 2005. Why disease persists: an evolutionary nosology. Med Health Care Philos. 8(3):343–350. doi:10.1007/s11019-005-2655-z. PubMed DOI

Picelli S, Björklund AK, Reinius B, Sagasser S, Winberg G, Sandberg R. 2014. Tn5 transposase and tagmentation procedures for massively scaled sequencing projects. Genome Res. 24(12):2033–2040. doi:10.1101/gr.177881.114. PubMed DOI PMC

Postel Z, Touzet P. 2020. Cytonuclear genetic incompatibilities in plant speciation. Plants. 9(4):487. doi:10.3390/plants9040487. PubMed DOI PMC

Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MAR, Bender D, Maller J, Sklar P, de Bakker PIW, Daly MJ, et al. . 2007. PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet. 81(3):559–575. doi:10.1086/519795. PubMed DOI PMC

Rambaut A. FigTree v1. 4.http://tree.bio.ed.ac.uk/software/figtree2012.

Remington DL, O’Malley DM. 2000. Evaluation of major genetic loci contributing to inbreeding depression for survival and early growth in a selfed family of Pinus taeda. Evolution. 54(5):1580–1589. doi:10.1111/j.0014-3820.2000.tb00703.x. PubMed DOI

Renaut S, Rieseberg LH. 2015. The accumulation of deleterious mutations as a consequence of domestication and improvement in sunflowers and other Compositae crops. Mol Biol Evol. 32(9):2273–2283. doi:10.1093/molbev/msv106. PubMed DOI

Rieseberg LH, Willis JH. 2007. Plant speciation. Science. 317(5840):910–914. doi:10.1126/science.1137729. PubMed DOI PMC

Rodgers-Melnick E, Bradbury PJ, Elshire RJ, Glaubitz JC, Acharya CB, Mitchell SE, Li C, Li Y, Buckler ES. 2015. Recombination in diverse maize is stable, predictable, and associated with genetic load. Proc Natl Acad Sci U S A. 112(12):3823–3828. doi:10.1073/pnas.1413864112. PubMed DOI PMC

Rowan BA, Seymour DK, Chae E, Lundberg DS, Weigel D. 2017. Methods for genotyping-by-sequencing. Methods Mol Biol. 1492:221–242. doi:10.1007/978-1-4939-6442-0_16. PubMed DOI

Sams AJ, Boyko AR. 2019. Fine-scale resolution of runs of homozygosity reveal patterns of inbreeding and substantial overlap with recessive disease genotypes in domestic dogs. G3 (Bethesda). 9(1):117–123. doi:10.1534/g3.118.200836. PubMed DOI PMC

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(8):e42691. doi:10.1371/journal.pone.0042691. PubMed DOI PMC

Simão FA, Waterhouse RM, Ioannidis P, Kriventseva EV, Zdobnov EM. 2015. BUSCO: assessing genome assembly and annotation completeness with single copy orthologs. Bioinformatics. 31(19):3210–3212. doi:10.1093/bioinformatics/btv351. PubMed DOI

Stanke M, Schöffmann O, Morgenstern B, Waack S. 2006. Gene prediction in eukaryotes with a generalized hidden Markov model that uses hints from external sources. BMC Bioinformatics. 7(1):62. doi:10.1186/1471-2105-7-62. PubMed DOI PMC

Supek F, Bošnjak M, Škunca N, Šmuc T. 2011. REVIGO summarizes and visualizes long lists of gene ontology terms. PLoS One. 6(7):e21800. doi:10.1371/journal.pone.0021800. PubMed DOI PMC

Talebi R, Szmatoła T, Mészáros G, Qanbari S. 2020. Runs of homozygosity in modern chicken revealed by sequence data. G3 (Bethesda). 10(12):4615–4623. doi:10.1534/g3.120.401860. PubMed DOI PMC

Taylor DR, Ingvarsson PK. 2003. Common features of segregation distortion in plants and animals. Genetica. 117(1):27–35. doi:10.1023/A:1022308414864. PubMed DOI

Tian T, Liu Y, Yan H, You Q, Yi X, Du Z, Xu W, Su Z. 2017. agriGO v2.0: a GO analysis toolkit for the agricultural community. Nucleic Acids Res. 45(W1):W122–W129. doi:10.1093/nar/gkx382. PubMed DOI PMC

van Wersch R, Li X, Zhang Y. 2016. Mighty dwarfs: Arabidopsis autoimmune mutants and their usages in genetic dissection of plant immunity. Front Plant Sci. 7:1717. doi:10.3389/fpls.2016.01717. PubMed DOI PMC

Venkataraman S, Badar U, Shoeb E, Hashim G, AbouHaidar M, Hefferon K. 2021. An inside look into biological miniatures: molecular mechanisms of viroids. Int J Mol Sci. 22(6):2795. doi:10.3390/ijms22062795. PubMed DOI PMC

Walker BJ, Abeel T, Shea T, Priest M, Abouelliel A, Sakthikumar S, Cuomo CA, Zeng Q, Wortman J, Young SK, et al. . 2014. Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS One. 9(11):e112963. doi:10.1371/journal.pone.0112963. PubMed DOI PMC

Weiß CL, Pais M, Cano LM, Kamoun S, Burbano HA. 2018. Nquire: a statistical framework for ploidy estimation using next generation sequencing. BMC Bioinformatics. 19(1):122. doi:10.1186/s12859-018-2128-z. PubMed DOI PMC

Wickham H. 2009. Ggplot2: Elegant Graphics for Data Analysis. 2nd ed. New York (NY): Springer Publishing Company.

Willis JH. 1992. Genetic analysis of inbreeding depression caused by chlorophyll-deficient lethals in Mimulus guttatus. Heredity (Edinb). 69(6):562–572. doi:10.1038/hdy.1992.172. DOI

Winn AA, Elle E, Kalisz S, Cheptou P-O, Eckert CG, Goodwillie C, Johnston MO, Moeller DA, Ree RH, Sargent RD, et al. . 2011. Analysis of inbreeding depression in mixed-mating plants provides evidence for selective interference and stable mixed mating. Evolution. 65(12):3339–3359. doi:10.1111/j.1558-5646.2011.01462.x. PubMed DOI

Wright SI, Ness RW, Foxe JP, Barrett SCH. 2008. Genomic consequences of outcrossing and selfing in plants. Int J Plant Sci. 169(1):105–118. doi:10.1086/523366. DOI

Yaffe H, Buxdorf K, Shapira I, Ein-Gedi S, Moyal-Ben Zvi M, Fridman E, Moshelion M, Levy M. 2012. LogSpin: a simple, economical, and fast method for RNA isolation from infected or healthy plants and other eukaryotic tissues. BMC Res Notes. 5(1):45. doi:10.1186/1756-0500-5-45. PubMed DOI PMC

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 DOI

Zanders SE, Unckless RL. 2019. Fertility costs of meiotic drivers. Curr Biol. 29(11):R512–R520. doi:10.1016/j.cub.2019.03.046. PubMed DOI PMC

Zhang C, Wang P, Tang D, Yang Z, Lu F, Qi J, Tawari NR, Shang Y, Li C, Huang S. 2019. The genetic basis of inbreeding depression in potato. Nat Genet. 51(3):374–378. doi:10.1038/s41588-018-0319-1. PubMed DOI

Complementing model species with model clades

Phytochromes mediate germination inhibition under red, far-red, and white light in Aethionema arabicum