To identify novel genes engaged in plant epidermal development, we characterized the phenotypic variability of rosette leaf epidermis of 310 sequenced Arabidopsis thaliana accessions, focusing on trichome shape and distribution, compositional characteristics of the trichome cell wall, and histologically detectable metal ion distribution. Some of these traits correlated with cLimate parameters of our accession's locations of origin, suggesting environmental selection. A novel metal deposition pattern in stomatal guard cells was observed in some accessions. Subsequent GWAS analysis identified 1546 loci with protein sequence-altering SNPs associated with one or more traits, including 5 genes with previously reported relevant mutant phenotypes and 80 additional genes with known or predicted roles in relevant developmental and cellular processes. Some candidates, including GFS9/TT9, exhibited environmentally correlated allele distribution. Several large gene famiLies, namely DUF674, DUF784, DUF1262, DUF1985, DUF3741, cytochrome P450, receptor-Like kinases, Cys/His-rich C1 domain proteins and formins were overrepresented among the candidates for various traits, suggesting epidermal development-related functions. A possible participation of formins in guard cell metal deposition was supported by observations in available loss of function mutants. Screening of candidate gene lists against the STRING interactome database uncovered several predominantly nuclear protein interaction networks with possible novel roles in epidermal development.

Department of Experimental Plant Biology Faculty of Sciences Charles University Prague Czechia

Gregor Mendel Institute Vienna Austria

Institute of Experimental Botany Czech Academy of Sciences Prague Czechia

Plant Molecular and Cellular Biology Laboratory and Integrative Biology Laboratory Salk Institute for Biological Studies La Jolla California USA

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Alonso‐Blanco, C., J. Andrade, C. Becker, et al. 2016. “1,135 Genomes Reveal the Global Pattern of Polymorphism in Arabidopsis thaliana.” Cell 166, no. 2: 481–491. https://doi.org/10.1016/j.cell.2016.05.063.

Alonso‐Díaz, A., S. B. Satbhai, R. de Pedro‐Jové, et al. 2021. “A Genome‐Wide Association Study Reveals Cytokinin as a Major Component in the Root Defense Responses Against Ralstonia solanacearum.” Journal of Experimental Botany 72, no. 7: 2727–2740. https://doi.org/10.1093/jxb/eraa610.

Ambrose, J. C., T. Shoji, A. M. Kotzer, J. A. Pighin, and G. O. Wasteneys. 2007. “The Arabidopsis Clasp Gene Encodes a Microtubule‐Associated Protein Involved in Cell Expansion and Division.” Plant Cell 19, no. 9: 2763–2775. https://doi.org/10.1105/tpc.107.053777.

Arteaga, N., B. Méndez‐Vigo, A. Fuster‐Pons, et al. 2022. “Differential Environmental and Genomic Architectures Shape the Natural Diversity for Trichome Patterning and Morphology in Different Arabidopsis Organs.” Plant, Cell & Environment 45, no. 10: 3018–3035. https://doi.org/10.1111/pce.14308.

Barboza, L., S. Effgen, C. Alonso‐Blanco, et al. 2013. “Arabidopsis Semidwarfs Evolved From Independent Mutations in GA20ox1, Ortholog to Green Revolution Dwarf Alleles in Rice and Barley.” Proceedings of the National Academy of Sciences 110, no. 39: 15818–15823. https://doi.org/10.1073/pnas.1314979110.

Basu, D., J. Le, S. E. D. El‐Essal, et al. 2005. “DISTORTED3/SCAR2 Is a Putative Arabidopsis Wave Complex Subunit That Activates the Arp2/3 Complex and Is Required for Epidermal Morphogenesis.” Plant Cell 17, no. 2: 502–524. https://doi.org/10.1105/tpc.104.027987.

Bates, G. W., D. M. Rosenthal, J. Sun, et al. 2012. “A Comparative Study of the Arabidopsis thaliana Guard‐Cell Transcriptome and Its Modulation by Sucrose.” PLoS One 7, no. 11: e49641. https://doi.org/10.1371/journal.pone.0049641.

Berhin, A., C. Nawrath, and C. Hachez. 2022. “Subtle Interplay Between Trichome Development and Cuticle Formation in Plants.” New Phytologist 233, no. 5: 2036–2046. https://doi.org/10.1111/nph.17827.

Bezvoda, R. 2023. “AraPheno Study: Trichome_development_epidermis_metal_traits.” https://doi.org/10.21958/study:126.

Bhattacharya, A., P. Sood, and V. Citovsky. 2010. “The Roles of Plant Phenolics in Defence and Communication During Agrobacterium and Rhizobium Infection.” Molecular Plant Pathology 11, no. 5: 705–719. https://doi.org/10.1111/j.1364-3703.2010.00625.x.

Bischoff, V., S. Nita, L. Neumetzler, et al. 2010. “Trichome Birefringence and Its Homolog AT5G01360 Encode Plant‐Specific DUF231 Proteins Required for Cellulose Biosynthesis in Arabidopsis.” Plant Physiology 153, no. 2: 590–602. https://doi.org/10.1104/pp.110.153320.

Brachi, B., G. P. Morris, and J. O. Borevitz. 2011. “Genome‐Wide Association Studies in Plants: The Missing Heritability Is in the Field.” Genome Biology 12, no. 10: 232. https://doi.org/10.1186/gb-2011-12-10-232.

Brocker, C., M. Vasiliou, S. Carpenter, et al. 2013. “Aldehyde Dehydrogenase (ALDH) Superfamily in Plants: Gene Nomenclature and Comparative Genomics.” Planta 237, no. 1: 189–210. https://doi.org/10.1007/s00425-012-1749-0.

Camoirano, A., A. L. Arce, F. D. Ariel, A. L. Alem, D. H. Gonzalez, and I. L. Viola. 2020. “Class I TCP Transcription Factors Regulate Trichome Branching and Cuticle Development in Arabidopsis.” Journal of Experimental Botany 71, no. 18: 5438–5453. https://doi.org/10.1093/jxb/eraa257.

Cheng, C. Y., V. Krishnakumar, A. P. Chan, F. Thibaud‐Nissen, S. Schobel, and C. D. Town. 2017. “Araport11: A Complete Reannotation of the Arabidopsis thaliana Reference Genome.” Plant Journal 89, no. 4: 789–804. https://doi.org/10.1111/tpj.13415.

Cifrová, P., D. Oulehlová, E. Kollárová, et al. 2020. “Division of Labor Between Two Actin Nucleators—The Formin FH1 and the ARP2/3 Complex—in Arabidopsis Epidermal Cell Morphogenesis.” Frontiers in Plant Science 11: 148. https://doi.org/10.3389/fpls.2020.00148.

Crowell, D. N., D. H. Huizinga, A. K. Deem, C. Trobaugh, R. Denton, and S. E. Sen. 2007. “Arabidopsis thaliana Plants Possess a Specific Farnesylcysteine Lyase That Is Involved in Detoxification and Recycling of Farnesylcysteine.” Plant Journal 50, no. 5: 839–847. https://doi.org/10.1111/j.1365-313X.2007.03091.x.

Cvrčková, F., R. Ghosh, and H. Kočová. 2024. “Transmembrane Formins as Active Cargoes of Membrane Trafficking.” Journal of Experimental Botany 75, no. 12: 3668–3684. https://doi.org/10.1093/jxb/erae078.

Cvrčková, F., M. Grunt, R. Bezvoda, et al. 2012. “Evolution of the Land Plant Exocyst Complexes.” Frontiers in Plant Science 3: 159. https://doi.org/10.3389/fpls.2012.00159.

De Storme, N., and D. Geelen. 2020. “High Temperatures Alter Cross‐Over Distribution and Induce Male Meiotic Restitution in Arabidopsis thaliana.” Communications Biology 3, no. 1: 187. https://doi.org/10.1038/s42003-020-0897-1.

Dettmer, J., A. Hong‐Hermesdorf, Y. D. Stierhof, and K. Schumacher. 2006. “Vacuolar H+‐Atpase Activity Is Required for Endocytic and Secretory Trafficking in Arabidopsis.” Plant Cell 18, no. 3: 715–730. https://doi.org/10.1105/tpc.105.037978.

Donaldson, L. 2020. “Autofluorescence in Plants.” Molecules 25, no. 10: 2393. https://doi.org/10.3390/molecules25102393.

Eggers, R., A. Jammer, S. Jha, et al. 2021. “The Scope of Flavin‐Dependent Reactions and Processes in the Model Plant Arabidopsis thaliana.” Phytochemistry 189: 112822. https://doi.org/10.1016/j.phytochem.2021.112822.

Fendrych, M., L. Synek, T. Pečenková, et al. 2010. “The Arabidopsis Exocyst Complex Is Involved in Cytokinesis and Cell Plate Maturation.” Plant Cell 22, no. 9: 3053–3065. https://doi.org/10.1105/tpc.110.074351.

Frederickson, C. 2003. “Imaging Zinc: Old and New Tools.” Science's STKE: Signal Transduction Knowledge Environment 2003, no. 182: 18. https://doi.org/10.1126/stke.2003.182.pe18.

Gao, W., C. Guo, J. Hu, J. Dong, and L. H. Zhou. 2021. “Mature Trichome Is the Earliest Sequestration Site of Cd Ions in Arabidopsis thaliana Leaves.” Heliyon 7, no. 7: e07501. https://doi.org/10.1016/j.heliyon.2021.e07501.

Gloss, A. D., A. Vergnol, T. C. Morton, P. J. Laurin, F. Roux, and J. Bergelson. 2022. “Genome‐Wide Association Mapping Within a Local Arabidopsis thaliana Population More Fully Reveals the Genetic Architecture for Defensive Metabolite Diversity.” Philosophical Transactions of the Royal Society of London, Series B: Biological Sciences 377, no. 1855: 20200512. https://doi.org/10.1098/rstb.2020.0512.

Google. 2024. “ChromeDriver.” Chrome for Developers. https://chromedriver.chromium.org/.

Guo, C., J. Hu, W. Gao, et al. 2022. “Mechanosensation Triggers Enhanced Heavy Metal Ion Uptake by Non‐Glandular Trichomes.” Journal of Hazardous Materials 426: 127983. https://doi.org/10.1016/j.jhazmat.2021.127983.

Hammer, Ø., D. A. T. Harper, and P. D. Ryan. 2001. “Past: Paleontological Statistics Software Package for Education and Data Dnalysis.” Palaeontologia Electronica 4, no. 1: 4. http://palaeo-electronica.org/2001_1/past/issue1_01.htm.

Han, G., Y. Li, Z. Yang, C. Wang, Y. Zhang, and B. Wang. 2022. “Molecular Mechanisms of Plant Trichome Development.” Frontiers in Plant Science 13: 910228. https://doi.org/10.3389/fpls.2022.910228.

Harada, E., J. A. Kim, A. J. Meyer, R. Hell, S. Clemens, and Y. E. Choi. 2010. “Expression Profiling of Tobacco Leaf Trichomes Identifies Genes for Biotic and Abiotic Stresses.” Plant & Cell Physiology 51, no. 10: 1627–1637. https://doi.org/10.1093/pcp/pcq118.

Hauser, M. T. 2014. “Molecular Basis of Natural Variation and Environmental Control of Trichome Patterning.” Frontiers in Plant Science 5: 320. https://doi.org/10.3389/fpls.2014.00320.

Hauser, M. T., B. Harr, and C. Schlötterer. 2001. “Trichome Distribution in Arabidopsis thaliana and Its Close Relative Arabidopsis lyrata: Molecular Analysis of the Candidate Gene GLABROUS1.” Molecular Biology and Evolution 18, no. 9: 1754–1763. https://doi.org/10.1093/oxfordjournals.molbev.a003963.

Hegelund, J. N., T. P. Jahn, L. Baekgaard, M. G. Palmgren, and J. K. Schjoerring. 2010. “Transmembrane Nine Proteins in Yeast and Arabidopsis Affect Cellular Metal Contents Without Changing Vacuolar Morphology.” Physiologia Plantarum 140, no. 4: 355–367. https://doi.org/10.1111/j.1399-3054.2010.01404.x.

Hilscher, J., C. Schlötterer, and M. T. Hauser. 2009. “A Single Amino Acid Replacement in ETC2 Shapes Trichome Patterning in Natural Arabidopsis Populations.” Current Biology 19, no. 20: 1747–1751. https://doi.org/10.1016/j.cub.2009.08.057.

Horton, M. W., N. Bodenhausen, K. Beilsmith, et al. 2014. “Genome‐Wide Association Study of Arabidopsis thaliana Leaf Microbial Community.” Nature Communications 5: 5320. https://doi.org/10.1038/ncomms6320.

Huebbers, J. W., K. Büttgen, F. Leissing, et al. 2022. “An Advanced Method for the Release, Enrichment and Purification of High‐Quality Arabidopsis thaliana Rosette Leaf Trichomes Enables Profound Insights Into the Trichome Proteome.” Plant Methods 18, no. 1: 12. https://doi.org/10.1186/s13007-021-00836-0.

Huebbers, J. W., M. Mantz, R. Panstruga, and P. F. Huesgen. 2023. “Proteomics Dataset on Detached and Purified Arabidopsis thaliana Rosette Leaf Trichomes.” Data in Brief 46: 108897. https://doi.org/10.1016/j.dib.2023.108897.

Hwang, I. S., D. S. Choi, N. H. Kim, D. S. Kim, and B. K. Hwang. 2014. “The Pepper Cysteine/Histidine‐Rich DC1 Domain Protein CaDC1 Binds Both RNA and DNA and Is Required for Plant Cell Death and Defense Response.” New Phytologist 201, no. 2: 518–530. https://doi.org/10.1111/nph.12521.

Ichino, T., K. Fuji, H. Ueda, et al. 2014. “GFS9/TT9 Contributes to Intracellular Membrane Trafficking and Flavonoid Accumulation in Arabidopsis thaliana.” Plant Journal 80, no. 3: 410–423. https://doi.org/10.1111/tpj.12637.

Ichino, T., K. Maeda, I. Hara‐Nishimura, and T. Shimada. 2020. “Arabidopsis Echidna Protein Is Involved in Seed Coloration, Protein Trafficking to Vacuoles, and Vacuolar Biogenesis.” Journal of Experimental Botany 71, no. 14: 3999–4009. https://doi.org/10.1093/jxb/eraa147.

Igisch, C. P., C. Miège, and Y. Jaillais. 2022. “Cell Shape: A ROP Regulatory Tug‐of‐War in Pavement Cell Morphogenesis.” Current Biology 32, no. 3: R116–R118. https://doi.org/10.1016/j.cub.2021.12.028.

Ilgenfritz, H., D. Bouyer, A. Schnittger, et al. 2003. “The Arabidopsis STICHEL Gene Is a Regulator of Trichome Branch Number and Encodes a Novel Protein.” Plant Physiology 131, no. 2: 643–655. https://doi.org/10.1104/pp.014209.

Jakoby, M. J., D. Falkenhan, M. T. Mader, et al. 2008. “Transcriptional Profiling of Mature Arabidopsis Trichomes Reveals That NOECK Encodes the MIXTA‐Like Transcriptional Regulator Myb106.” Plant Physiology 148, no. 3: 1583–1602. https://doi.org/10.1104/pp.108.126979.

Jin, S., S. Zhang, Y. Liu, et al. 2020. “A Combination of Genome‐Wide Association Study and Transcriptome Analysis in Leaf Epidermis Identifies Candidate Genes Involved in Cuticular Wax Biosynthesis in Brassica napus.” BMC Plant Biology 20, no. 1: 458. https://doi.org/10.1186/s12870-020-02675-y.

Kannangara, R., C. Branigan, Y. Liu, et al. 2007. “The Transcription Factor WIN1/SHN1 Regulates Cutin Biosynthesis in Arabidopsis thaliana.” Plant Cell 19, no. 4: 1278–1294. https://doi.org/10.1105/tpc.106.047076.

Kim, H., H. Kwon, S. Kim, et al. 2016. “Synaptotagmin 1 Negatively Controls the Two Distinct Immune Secretory Pathways to Powdery Mildew Fungi in Arabidopsis.” Plant & Cell Physiology 57, no. 6: 1133–1141. https://doi.org/10.1093/pcp/pcw061.

Kollárová, E., A. Baquero Forero, and F. Cvrčková. 2021. “The Arabidopsis thaliana Class Ii Formin FH13 Modulates Pollen Tube Growth.” Frontiers in Plant Science 12: 599961. https://doi.org/10.3389/fpls.2021.599961.

Kriticos, D. J., B. L. Webber, A. Leriche, et al. 2012. “Climond: Global High‐Resolution Historical and Future Scenario Climate Surfaces for Bioclimatic Modelling.” Methods in Ecology and Evolution 3, no. 1: 53–64. https://doi.org/10.1111/j.2041-210X.2011.00134.x.

Kulich, I., Z. Vojtíková, M. Glanc, J. Ortmannová, S. Rasmann, and V. Žárský. 2015. “Cell Wall Maturation of Arabidopsis Trichomes Is Dependent on Exocyst Subunit EXO70H4 and Involves Callose Deposition.” Plant Physiology 168, no. 1: 120–131. https://doi.org/10.1104/pp.15.00112.

Kulich, I., Z. Vojtíková, P. Sabol, et al. 2018. “Exocyst Subunit EXO70H4 Has a Specific Role in Callose Synthase Secretion and Silica Accumulation.” Plant Physiology 176, no. 3: 2040–2051. https://doi.org/10.1104/pp.17.01693.

Kuroda, H., N. Takahashi, H. Shimada, M. Seki, K. Shinozaki, and M. Matsui. 2002. “Classification and Expression Analysis of Arabidopsis F‐Box‐Containing Protein Genes.” Plant & Cell Physiology 43, no. 10: 1073–1085. https://doi.org/10.1093/pcp/pcf151.

Larsen, P. B., J. Cancel, M. Rounds, and V. Ochoa. 2007. “Arabidopsis ALS1 Encodes a Root Tip and Stele Localized Half Type ABC Transporter Required for Root Growth in an Aluminum Toxic Environment.” Planta 225, no. 6: 1447–1458. https://doi.org/10.1007/s00425-006-0452-4.

Lee, J. H., and T. T. Paull. 2021. “Cellular Functions of the Protein Kinase Atm and Their Relevance to Human Disease.” Nature Reviews Molecular Cell Biology 22, no. 12: 796–814. https://doi.org/10.1038/s41580-021-00394-2.

Leonhardt, N., J. M. Kwak, N. Robert, D. Waner, G. Leonhardt, and J. I. Schroeder. 2004. “Microarray Expression Analyses of Arabidopsis Guard Cells and Isolation of a Recessive Abscisic Acid Hypersensitive Protein Phosphatase 2C Mutant[W].” Plant Cell 16, no. 3: 596–615. https://doi.org/10.1105/tpc.019000.

Levy, A., J. Y. Zheng, and S. G. Lazarowitz. 2015. “Synaptotagmin SYTA Forms ER‐Plasma Membrane Junctions That Are Recruited to Plasmodesmata for Plant Virus Movement.” Current Biology 25, no. 15: 2018–2025. https://doi.org/10.1016/j.cub.2015.06.015.

Li, Y., Y. Shen, C. Cai, et al. 2010. “The Type II Arabidopsis formin14 Interacts With Microtubules and Microfilaments to Regulate Cell Division.” Plant Cell 22, no. 8: 2710–2726. https://doi.org/10.1105/tpc.110.075507.

Li, Z., P. Wang, C. You, et al. 2020. “Combined GWAS and eQTL Analysis Uncovers a Genetic Regulatory Network Orchestrating the Initiation of Secondary Cell Wall Development in Cotton.” New Phytologist 226, no. 6: 1738–1752. https://doi.org/10.1111/nph.16468.

Lin, W., and Z. Yang. 2020. “Unlocking the Mechanisms Behind the Formation of Interlocking Pavement Cells.” Current Opinion in Plant Biology 57: 142–154. https://doi.org/10.1016/j.pbi.2020.09.002.

Liu, E., C. P. MacMillan, T. Shafee, et al. 2020. “Fasciclin‐Like Arabinogalactan‐Protein 16 (FLA16) Is Required for Stem Development in Arabidopsis.” Frontiers in Plant Science 11: 615392. https://doi.org/10.3389/fpls.2020.615392.

Liu, S., J. Jiao, T. J. Lu, F. Xu, B. G. Pickard, and G. M. Genin. 2017. “Arabidopsis Leaf Trichomes as Acoustic Antennae.” Biophysical Journal 113, no. 9: 2068–2076. https://doi.org/10.1016/j.bpj.2017.07.035.

Liu, S., F. Jobert, Z. Rahneshan, S. M. Doyle, and S. Robert. 2021. “Solving the Puzzle of Shape Regulation in Plant Epidermal Pavement Cells.” Annual Review of Plant Biology 72: 525–550. https://doi.org/10.1146/annurev-arplant-080720-081920.

Long, Z., M. Tu, Y. Xu, et al. 2023. “Genome‐Wide‐Association Study and Transcriptome Analysis Reveal the Genetic Basis Controlling the Formation of Leaf Wax in Brassica napus.” Journal of Experimental Botany 74, no. 8: 2726–2739. https://doi.org/10.1093/jxb/erad047.

Mahjoob, M. M. M., N. M. Kamal, Y. S. A. Gorafi, and H. Tsujimoto. 2022. “Genome‐Wide Association Study Reveals Distinct Genetic Associations Related to Leaf Hair Density in Two Lineages of Wheat‐Wild Relative Aegilops tauschii.” Scientific Reports 12, no. 1: 17486. https://doi.org/10.1038/s41598-022-21713-3.

Mathur, J., P. Spielhofer, B. Kost, and N. H. Chua. 1999. “The Actin Cytoskeleton Is Required to Elaborate and Maintain Spatial Patterning During Trichome Cell Morphogenesis in Arabidopsis thaliana.” Development 126, no. 24: 5559–5568. https://doi.org/10.1242/dev.126.24.5559.

Mitsuda, N., K. Enami, M. Nakata, K. Takeyasu, and M. H. Sato. 2001. “Novel Type Arabidopsis thaliana H(+)‐PPase Is Localized to the Golgi Apparatus.” FEBS Letters 488, no. 1–2: 29–33. https://doi.org/10.1016/s0014-5793(00)02400-5.

Oulehlová, D., E. Kollárová, P. Cifrová, P. Pejchar, V. Žárský, and F. Cvrčková. 2019. “Arabidopsis Class I Formin FH1 Relocates Between Membrane Compartments During Root Cell Ontogeny and Associates With Plasmodesmata.” Plant & Cell Physiology 60, no. 8: 1855–1870. https://doi.org/10.1093/pcp/pcz102.

Parsons, H. T., K. Christiansen, B. Knierim, et al. 2012. “Isolation and Proteomic Characterization of the Arabidopsis Golgi Defines Functional and Novel Components Involved in Plant Cell Wall Biosynthesis.” Plant Physiology 159, no. 1: 12–26. https://doi.org/10.1104/pp.111.193151.

Pasha, A., S. Subramaniam, A. Cleary, et al. 2020. “Araport Lives: An Updated Framework for Arabidopsis Bioinformatics.” Plant Cell 32, no. 9: 2683–2686. https://doi.org/10.1105/tpc.20.00358.

Peco, J. D., P. Higueras, J. A. Campos, A. Olmedilla, M. C. Romero‐Puertas, and L. M. Sandalio. 2020. “Deciphering Lead Tolerance Mechanisms in a Population of the Plant Species Biscutella auriculata L. From a Mining Area: Accumulation Strategies and Antioxidant Defenses.” Chemosphere 261: 127721. https://doi.org/10.1016/j.chemosphere.2020.127721.

Pietra, S., A. Gustavsson, C. Kiefer, et al. 2013. “Arabidopsis SABRE and CLASP Interact to Stabilize Cell Division Plane Orientation and Planar Polarity.” Nature Communications 4: 2779. https://doi.org/10.1038/ncomms3779.

Python Software Foundation. 2024. “Python.” https://www.python.org/.

Python Visualisation. 2024. “Folium.” https://python-visualization.github.io/folium/latest/.

Qu, J., D. Bonte, and M. L. Vandegehuchte. 2022. “Phenotypic and Genotypic Divergence of Plant‐Herbivore Interactions Along an Urbanization Gradient.” Evolutionary Applications 15, no. 5: 865–877. https://doi.org/10.1111/eva.13376.

Radua, J., A. Albajes‐Elsagirre, and L. Fortea 2024. “FDR Online Calculator.” Seed‐Based d Mapping. https://www.sdmproject.com/utilities/?show=FDR.

Reback, J., jbrockmendel, W. McKinney, et al. 2021. “Pandas‐Dev/Pandas: Pandas 1.3.5 (v. 1.3.5).” Zenodo. https://doi.org/10.5281/zenodo.5774815.

Reiser, L., E. Bakker, S. Subramaniam, et al. 2024. “The Arabidopsis Information Resource in 2024.” Genetics 227, no. 1: iyae027. https://doi.org/10.1093/genetics/iyae027.

Reynoud, N., J. Petit, C. Bres, et al. 2021. “The Complex Architecture of Plant Cuticles and Its Relation to Multiple Biological Functions.” Frontiers in Plant Science 12: 782773. https://doi.org/10.3389/fpls.2021.782773.

Ricachenevsky, F. K., T. Punshon, D. E. Salt, J. P. Fett, and M. L. Guerinot. 2021. “Arabidopsis thaliana Zinc Accumulation in Leaf Trichomes Is Correlated With Zinc Concentration in Leaves.” Scientific Reports 11, no. 1: 5278. https://doi.org/10.1038/s41598-021-84508-y.

Ristova, D., M. Giovannetti, K. Metesch, and W. Busch. 2018. “Natural Genetic Variation Shapes Root System Responses to Phytohormones in Arabidopsis.” Plant Journal: for Cell and Molecular Biology 96, no. 2: 468–481. https://doi.org/10.1111/tpj.14034.

Rosero, A., D. Oulehlová, L. Stillerová, et al. 2016. “Arabidopsis FH1 Formin Affects Cotyledon Pavement Cell Shape by Modulating Cytoskeleton Dynamics.” Plant & Cell Physiology 57, no. 3: 488–504. https://doi.org/10.1093/pcp/pcv209.

Rosero, A., V. Žárský, and F. Cvrčková. 2013. “AtFH1 Formin Mutation Affects Actin Filament and Microtubule Dynamics in Arabidopsis thaliana.” Journal of Experimental Botany 64, no. 2: 585–597. https://doi.org/10.1093/jxb/ers351.

Sapala, A., A. Runions, A. L. Routier‐Kierzkowska, et al. 2018. “Why Plants Make Puzzle Cells, and How Their Shape Emerges.” eLife 7: e32794. https://doi.org/10.7554/eLife.32794.

Sato, Y., R. Shimizu‐Inatsugi, M. Yamazaki, K. K. Shimizu, and A. J. Nagano. 2019. “Plant Trichomes and a Single Gene GLABRA1 Contribute to Insect Community Composition on Field‐Grown Arabidopsis thaliana.” BMC Plant Biology 19, no. 1: 163. https://doi.org/10.1186/s12870-019-1705-2.

Schapire, A. L., B. Voigt, J. Jasik, et al. 2008. “Arabidopsis Synaptotagmin 1 Is Required for the Maintenance of Plasma Membrane Integrity and Cell Viability.” Plant Cell 20, no. 12: 3374–3388. https://doi.org/10.1105/tpc.108.063859.

Schindelin, J., I. Arganda‐Carreras, E. Frise, et al. 2012. “Fiji: An Open‐Source Platform for Biological‐Image Analysis.” Nature Methods 9, no. 7: 676–682. https://doi.org/10.1038/nmeth.2019.

Schober, P., C. Boer, and L. A. Schwarte. 2018. “Correlation Coefficients: Appropriate Use and Interpretation.” Anesthesia & Analgesia 126, no. 5: 1763–1768. https://doi.org/10.1213/ANE.0000000000002864.

Scutenaire, J., J. M. Deragon, V. Jean, et al. 2018. “The Yth Domain Protein ECT2 Is an M6A Reader Required for Normal Trichome Branching in Arabidopsis.” Plant Cell 30, no. 5: 986–1005. https://doi.org/10.1105/tpc.17.00854.

Seregin, I. V., and V. B. Ivanov. 1997. “Histochemical Investigation of Cadmium and Lead Distribution in Plants.” Russian Journal of Plant Physiology 44, no. 6: 791–796. https://www.researchgate.net/publication/279705125_Histochemical_Investigation_of_Cadmium_and_Lead_Distribution_in_Plants.

Seren, Ü. 2015. “The GWA‐Portal Resource for Phenotypes and GWAS Studies.” https://gwas.gmi.oeaw.ac.at/.

Seren, Ü., B. J. Vilhjálmsson, M. W. Horton, et al. 2012. “GWAPP: A Web Application for Genome‐Wide Association Mapping in Arabidopsis.” Plant Cell 24, no. 12: 4793–4805. https://doi.org/10.1105/tpc.112.108068.

Shi, C., and H. Liu. 2021. “How Plants Protect Themselves From Ultraviolet‐B Radiation Stress.” Plant Physiology 187, no. 3: 1096–1103. https://doi.org/10.1093/plphys/kiab245.

Slovak, R., C. Göschl, Ü. Seren, and W. Busch. 2015. “Genome‐Wide Association Mapping in Plants Exemplified for Root Growth in Arabidopsis thaliana.” Methods in Molecular Biology 1284: 343–357. https://doi.org/10.1007/978-1-4939-2444-8_17.

Srivastava, R. K., P. Pandey, R. Rajpoot, A. Rani, and R. S. Dubey. 2014. “Cadmium and Lead Interactive Effects on Oxidative Stress and Antioxidative Responses in Rice Seedlings.” Protoplasma 251, no. 5: 1047–1065. https://doi.org/10.1007/s00709-014-0614-3.

Stagroom, J. 2024. “Chi‐Square Test Calculator.” Social Science Statistics. https://www.socscistatistics.com/tests/chisquare2/default2.aspx.

Suh, M. C., A. L. Samuels, R. Jetter, et al. 2005. “Cuticular Lipid Composition, Surface Structure, and Gene Expression in Arabidopsis Stem Epidermis.” Plant Physiology 139, no. 4: 1649–1665. https://doi.org/10.1104/pp.105.070805.

Symonds, V. V., G. Hatlestad, and A. M. Lloyd. 2011. “Natural Allelic Variation Defines a Role for ATMYC1: Trichome Cell Fate Determination.” PLoS Genetics 7, no. 6: e1002069. https://doi.org/10.1371/journal.pgen.1002069.

Szklarczyk, D., R. Kirsch, M. Koutrouli, et al. 2023. “The STRING Database in 2023: Protein‐Protein Association Networks and Functional Enrichment Analyses for Any Sequenced Genome of Interest.” Nucleic Acids Research 51, no. D1: D638–D646. https://doi.org/10.1093/nar/gkac1000.

Szymanski, D. B. 2005. “Breaking the WAVE Complex: The Point of Arabidopsis Trichomes.” Current Opinion in Plant Biology 8, no. 1: 103–112. https://doi.org/10.1016/j.pbi.2004.11.004.

Togninalli, M., Ü. Seren, J. A. Freudenthal, et al. 2020. “Arapheno and the AraGWAS Catalog 2020: A Major Database Update Including RNA‐Seq and Knockout Mutation Data for Arabidopsis thaliana.” Nucleic Acids Research 48, no. D1: 1063. https://doi.org/10.1093/nar/gkz925.

Torii, K. U. 2021. “Stomatal Development in the Context of Epidermal Tissues.” Annals of Botany 128, no. 2: 137–148. https://doi.org/10.1093/aob/mcab052.

Vasavada, N. 2016. “Fisher Test of Exact Count Data.” Online Web Statistical Calculators. https://astatsa.com/FisherTest.

Vega‐Muñoz, I., A. Herrera‐Estrella, O. Martínez‐de la Vega, and M. Heil. 2023. “ATM and ATR, Two Central Players of the Dna Damage Response, Are Involved in the Induction of Systemic Acquired Resistance by Extracellular DNA, but Not the Plant Wound Response.” Frontiers in Immunology 14: 1175786. https://doi.org/10.3389/fimmu.2023.1175786.

Vukašinović, N., and V. Žárský. 2016. “Tethering Complexes in the Arabidopsis Endomembrane System.” Frontiers in Cell and Developmental Biology 4: 46. https://doi.org/10.3389/fcell.2016.00046.

Wang, X., Y. Miao, Y. Cai, et al. 2021. “Large‐Fragment Insertion Activates Gene Gafz (Ga08G0121) and Is Associated With the Fuzz and Trichome Reduction in Cotton (Gossypium arboreum).” Plant Biotechnology Journal 19, no. 6: 1110–1124. https://doi.org/10.1111/pbi.13532.

Waskom, M. 2021. “Seaborn: Statistical Data Visualization.” Journal of Open Source Software 6, no. 60: 3021. https://doi.org/10.21105/joss.03021.

Wei, L. H., P. Song, Y. Wang, et al. 2018. “The M6A Reader ECT2 Controls Trichome Morphology by Affecting mRNA Stability in Arabidopsis.” Plant Cell 30, no. 5: 968–985. https://doi.org/10.1105/tpc.17.00934.

Wienkoop, S., D. Zoeller, B. Ebert, et al. 2004. “Cell‐Specific Protein Profiling in Arabidopsis thaliana Trichomes: Identification of Trichome‐Located Proteins Involved in Sulfur Metabolism and Detoxification.” Phytochemistry 65, no. 11: 1641–1649. https://doi.org/10.1016/j.phytochem.2004.03.026.

Wu, Y., Q. Xun, Y. Guo, et al. 2016. “Genome‐Wide Expression Pattern Analyses of the Arabidopsis Leucine‐Rich Repeat Receptor‐Like Kinases.” Molecular Plant 9, no. 2: 289–300. https://doi.org/10.1016/j.molp.2015.12.011.

Xia, K., H. X. Sun, J. Li, et al. 2022. “The Single‐Cell Stereo‐Seq Reveals Region‐Specific Cell Subtypes and Transcriptome Profiling in Arabidopsis Leaves.” Developmental Cell 57, no. 10: 1299–1310.e4. https://doi.org/10.1016/j.devcel.2022.04.011.

Xu, J. J., X. Fang, C. Y. Li, et al. 2018. “Characterization of Arabidopsis thaliana Hydroxyphenylpyruvate Reductases in the Tyrosine Conversion Pathway.” Frontiers in Plant Science 9: 1305. https://doi.org/10.3389/fpls.2018.01305.

Xuan, L., T. Yan, L. Lu, et al. 2020. “Genome‐Wide Association Study Reveals New Genes Involved in Leaf Trichome Formation in Polyploid Oilseed Rape (Brassica napus L.).” Plant, Cell & Environment 43, no. 3: 675–691. https://doi.org/10.1111/pce.13694.

Yaashikaa, P. R., P. S. Kumar, S. Jeevanantham, and R. Saravanan. 2022. “A Review on Bioremediation Approach for Heavy Metal Detoxification and Accumulation in Plants.” Environmental Pollution 301: 119035. https://doi.org/10.1016/j.envpol.2022.119035.

Yamazaki, T., Y. Kawamura, A. Minami, and M. Uemura. 2008. “Calcium‐Dependent Freezing Tolerance in Arabidopsis Involves Membrane Resealing via Synaptotagmin SYT1.” Plant Cell 20, no. 12: 3389–3404. https://doi.org/10.1105/tpc.108.062679.

Yan, H., D. C. Haak, S. Li, L. Huang, and A. Bombarely. 2022. “Exploring Transposable Element‐Based Markers to Identify Allelic Variations Underlying Agronomic Traits in Rice.” Plant Communications 3, no. 3: 100270. https://doi.org/10.1016/j.xplc.2021.100270.

Yates, A. D., J. Allen, R. M. Amode, et al. 2022. “Ensembl Genomes 2022: An Expanding Genome Resource for Non‐Vertebrates.” Nucleic Acids Research 50, no. D1: D996–D1003. https://doi.org/10.1093/nar/gkab1007.

Yengo, L., S. Vedantam, E. Marouli, et al. 2022. “A Saturated Map of Common Genetic Variants Associated With Human Height.” Nature 610, no. 7933: 704–712. https://doi.org/10.1038/s41586-022-05275-y.

Yuan, D. S. 2011. “Dithizone Staining of Intracellular Zinc: An Unexpected and Versatile Counterscreen for Auxotrophic Marker Genes in Saccharomyces cerevisiae.” PLoS One 6, no. 10: e25830. https://doi.org/10.1371/journal.pone.0025830.

Zeng, L., T. Zhu, Y. Gao, et al. 2017. “Effects of Ca Addition on the Uptake, Translocation, and Distribution of Cd in Arabidopsis thaliana.” Ecotoxicology and Environmental Safety 139: 228–237. https://doi.org/10.1016/j.ecoenv.2017.01.023.

Zhang, D. 2009. “Homology between DUF784, DUF1278 Domains and the Plant Prolamin Superfamily Typifies Evolutionary Changes of Disulfide Bonding Patterns.” Cell Cycle 8, no. 20: 3428–3430. https://doi.org/10.4161/cc.8.20.9674.

Zhao, Z., W. Zhang, B. A. Stanley, and S. M. Assmann. 2008. “Functional Proteomics of Arabidopsis thaliana Guard Cells Uncovers New Stomatal Signaling Pathways.” Plant Cell 20, no. 12: 3210–3226. https://doi.org/10.1105/tpc.108.063263.

Zhou, L. H., S. B. Liu, P. F. Wang, et al. 2017. “The Arabidopsis Trichome Is an Active Mechanosensory Switch.” Plant, Cell & Environment 40, no. 5: 611–621. https://doi.org/10.1111/pce.12728.

Zuch, D. T., S. M. Doyle, M. Majda, R. S. Smith, S. Robert, and K. U. Torii. 2022. “Cell Biology of the Leaf Epidermis: Fate Specification, Morphogenesis, and Coordination.” Plant Cell 34, no. 1: 209–227. https://doi.org/10.1093/plcell/koab250.