A Genome-Wide Association Screen for Genes Affecting Leaf Trichome Development and Epidermal Metal Accumulation in Arabidopsis

. 2025 May ; 48 (5) : 3708-3734. [epub] 20250115

Jazyk angličtina Země Spojené státy americké Médium print-electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid39812181

Grantová podpora
The initial stages of this work have been supported by the Austrian Science Fund, Charles University, CSF/GACR/FWF project GF16-34887L, the formin mutant verification experiments by the CSF/GACR 22-33471S grant, and the finalization of this report by the project TowArds Next GENeration Crops, reg. no. CZ.02.01.01/00/22_008/0004581 of the ERDF Programme Johannes Amos Comenius.

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.

Zobrazit více v PubMed

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

Alonso‐Díaz, A. , Satbhai S. B., de Pedro‐Jové R., 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. 10.1093/jxb/eraa610. PubMed DOI PMC

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

Arteaga, N. , Méndez‐Vigo B., Fuster‐Pons A., 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. 10.1111/pce.14308. PubMed DOI PMC

Barboza, L. , Effgen S., Alonso‐Blanco C., 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. 10.1073/pnas.1314979110. PubMed DOI PMC

Basu, D. , Le J., El‐Essal S. E. D., 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. 10.1105/tpc.104.027987. PubMed DOI PMC

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

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

Bezvoda, R. 2023. “AraPheno Study: Trichome_development_epidermis_metal_traits.” 10.21958/study:126. DOI

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

Bischoff, V. , Nita S., Neumetzler L., 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. 10.1104/pp.110.153320. PubMed DOI PMC

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

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

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

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

Cifrová, P. , Oulehlová D., Kollárová E., 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. 10.3389/fpls.2020.00148. PubMed DOI PMC

Crowell, D. N. , Huizinga D. H., Deem A. K., Trobaugh C., Denton R., and Sen S. E.. 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. 10.1111/j.1365-313X.2007.03091.x. PubMed DOI

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

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

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

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

Donaldson, L. 2020. “Autofluorescence in Plants.” Molecules 25, no. 10: 2393. 10.3390/molecules25102393. PubMed DOI PMC

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

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

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

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

Gloss, A. D. , Vergnol A., Morton T. C., Laurin P. J., Roux F., and Bergelson J.. 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. 10.1098/rstb.2020.0512. PubMed DOI PMC

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

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

Hammer, Ø. , Harper D. A. T., and Ryan P. D.. 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. , Li Y., Yang Z., Wang C., Zhang Y., and Wang B.. 2022. “Molecular Mechanisms of Plant Trichome Development.” Frontiers in Plant Science 13: 910228. 10.3389/fpls.2022.910228. PubMed DOI PMC

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

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

Hauser, M. T. , Harr B., and Schlötterer C.. 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. 10.1093/oxfordjournals.molbev.a003963. PubMed DOI

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

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

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

Huebbers, J. W. , Büttgen K., Leissing F., 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. 10.1186/s13007-021-00836-0. PubMed DOI PMC

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

Hwang, I. S. , Choi D. S., Kim N. H., Kim D. S., and Hwang B. K.. 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. 10.1111/nph.12521. PubMed DOI

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

Ichino, T. , Maeda K., Hara‐Nishimura I., and Shimada T.. 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. 10.1093/jxb/eraa147. PubMed DOI PMC

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

Ilgenfritz, H. , Bouyer D., Schnittger A., 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. 10.1104/pp.014209. PubMed DOI PMC

Jakoby, M. J. , Falkenhan D., Mader M. T., 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. 10.1104/pp.108.126979. PubMed DOI PMC

Jin, S. , Zhang S., Liu Y., 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. 10.1186/s12870-020-02675-y. PubMed DOI PMC

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

Kim, H. , Kwon H., Kim S., 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. 10.1093/pcp/pcw061. PubMed DOI

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

Kriticos, D. J. , Webber B. L., Leriche A., 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. 10.1111/j.2041-210X.2011.00134.x. DOI

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

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

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

Larsen, P. B. , Cancel J., Rounds M., and Ochoa V.. 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. 10.1007/s00425-006-0452-4. PubMed DOI

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

Leonhardt, N. , Kwak J. M., Robert N., Waner D., Leonhardt G., and Schroeder J. I.. 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. 10.1105/tpc.019000. PubMed DOI PMC

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

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

Li, Z. , Wang P., You C., 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. 10.1111/nph.16468. PubMed DOI

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

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

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

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

Long, Z. , Tu M., Xu Y., 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. 10.1093/jxb/erad047. PubMed DOI

Mahjoob, M. M. M. , Kamal N. M., Gorafi Y. S. A., and Tsujimoto H.. 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. 10.1038/s41598-022-21713-3. PubMed DOI PMC

Mathur, J. , Spielhofer P., Kost B., and Chua N. H.. 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. 10.1242/dev.126.24.5559. PubMed DOI

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

Oulehlová, D. , Kollárová E., Cifrová P., Pejchar P., Žárský V., and Cvrčková F.. 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. 10.1093/pcp/pcz102. PubMed DOI

Parsons, H. T. , Christiansen K., Knierim B., 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. 10.1104/pp.111.193151. PubMed DOI PMC

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

Peco, J. D. , Higueras P., Campos J. A., Olmedilla A., Romero‐Puertas M. C., and Sandalio L. M.. 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. 10.1016/j.chemosphere.2020.127721. PubMed DOI

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

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

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

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

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

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

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

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

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

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

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

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

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

Sato, Y. , Shimizu‐Inatsugi R., Yamazaki M., Shimizu K. K., and Nagano A. J.. 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. 10.1186/s12870-019-1705-2. PubMed DOI PMC

Schapire, A. L. , Voigt B., Jasik J., 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. 10.1105/tpc.108.063859. PubMed DOI PMC

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

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

Scutenaire, J. , Deragon J. M., Jean V., 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. 10.1105/tpc.17.00854. PubMed DOI PMC

Seregin, I. V. , and Ivanov V. B.. 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. , Vilhjálmsson B. J., Horton M. W., et al. 2012. “GWAPP: A Web Application for Genome‐Wide Association Mapping in Arabidopsis.” Plant Cell 24, no. 12: 4793–4805. 10.1105/tpc.112.108068. PubMed DOI PMC

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

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

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

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

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

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

Szklarczyk, D. , Kirsch R., Koutrouli M., 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. 10.1093/nar/gkac1000. PubMed DOI PMC

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

Togninalli, M. , Seren Ü., Freudenthal J. A., 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. 10.1093/nar/gkz925. PubMed DOI PMC

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

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

Vega‐Muñoz, I. , Herrera‐Estrella A., Martínez‐de la Vega O., and Heil M.. 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. 10.3389/fimmu.2023.1175786. PubMed DOI PMC

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

Wang, X. , Miao Y., Cai Y., 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. 10.1111/pbi.13532. PubMed DOI PMC

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

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

Wienkoop, S. , Zoeller D., Ebert B., 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. 10.1016/j.phytochem.2004.03.026. PubMed DOI

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

Xia, K. , Sun H. X., Li J., 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. 10.1016/j.devcel.2022.04.011. PubMed DOI

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

Xuan, L. , Yan T., Lu L., 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. 10.1111/pce.13694. PubMed DOI

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

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

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

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

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

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. 10.1371/journal.pone.0025830. PubMed DOI PMC

Zeng, L. , Zhu T., Gao Y., 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. 10.1016/j.ecoenv.2017.01.023. PubMed DOI

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. 10.4161/cc.8.20.9674. PubMed DOI

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

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

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

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...