{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T02:01:21Z","timestamp":1760148081480,"version":"build-2065373602"},"reference-count":54,"publisher":"MDPI AG","issue":"4","license":[{"start":{"date-parts":[[2023,3,28]],"date-time":"2023-03-28T00:00:00Z","timestamp":1679961600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001871","name":"Foundation for Science and Technology (FCT) and FEDER funds","doi-asserted-by":"publisher","award":["PTDC\/ASP-PLA\/29779\/2017","UID\/AGR\/04129\/2020"],"award-info":[{"award-number":["PTDC\/ASP-PLA\/29779\/2017","UID\/AGR\/04129\/2020"]}],"id":[{"id":"10.13039\/501100001871","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001871","name":"FCT UNIT LEAF","doi-asserted-by":"publisher","award":["PTDC\/ASP-PLA\/29779\/2017","UID\/AGR\/04129\/2020"],"award-info":[{"award-number":["PTDC\/ASP-PLA\/29779\/2017","UID\/AGR\/04129\/2020"]}],"id":[{"id":"10.13039\/501100001871","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Agronomy"],"abstract":"<jats:p>Coffee, a widely consumed important agricultural product, is mainly produced from two species, Coffea arabica (Arabica coffee) and C. canephora (Robusta coffee). Timor Hybrid (HDT) is a population resulting from a natural cross between C. arabica and C. canephora. HDT derivatives have a high spectrum of resistance to different races of Hemileia vastatrix (Hv), the causal agent of coffee leaf rust. A RNAseq database, obtained from HDT832\/2 leaves inoculated with Hv (Host Resistance) and Uromyces vignae (Uv, Nonhost Resistance), showed the presence of genes implicated in the hypersensitive response and salicylic acid pathway. Hypersensitive Induced Reaction (HIR) gene family, Enhanced Disease Susceptibility1 gene (EDS1), and Phytoalexin Deficient 4 (PAD4) gene are involved in host and nonhost resistance. Relative expression calculated by RT-qPCR was used to confirm and expand the transcriptome analysis. HDTHIR4, HDTEDS1, and HDTPAD4 showed the highest upregulation in response to Hv and Uv inoculation, confirming a similar trend in host and nonhost resistance in HDT. HIR and EDS1\/PAD4 gene families were characterized for the first time in the three available Coffea genomes. HIR genes were quite conserved between Coffea species. Surprisingly, EDS1 and PAD4 genes revealed major differences in gene structure. The PAD4 predicted protein from C. arabica does not include both conserved domains of the EDS1\/PAD4 family, and the EDS1 putative protein from C. canephora includes a formin domain unusual in the same protein family. The variability shown by EDS1\/PAD4 gene family may impact the disease resistance response of Coffea species, which can be surveyed for the gene sequences that will produce a more resistant phenotype.<\/jats:p>","DOI":"10.3390\/agronomy13040992","type":"journal-article","created":{"date-parts":[[2023,3,28]],"date-time":"2023-03-28T02:58:21Z","timestamp":1679972301000},"page":"992","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":3,"title":["Identification of HIR, EDS1 and PAD4 Genes Reveals Differences between Coffea Species That May Impact Disease Resistance"],"prefix":"10.3390","volume":"13","author":[{"given":"S\u00edlvia","family":"Tavares","sequence":"first","affiliation":[{"name":"CIFC\u2014Centro de Investiga\u00e7\u00e3o das Ferrugens do Cafeeiro, Instituto Superior de Agronomia, Universidade de Lisboa, Quinta do Marqu\u00eas, 2784-505 Oeiras, Portugal"},{"name":"LEAF\u2014Linking Landscape, Environment, Agriculture and Food Research Center, Associated Laboratory TERRA, Instituto Superior de Agronomia, Universidade de Lisboa, Tapada da Ajuda, 1349-017 Lisboa, Portugal"},{"name":"Department of Plant and Environmental Sciences, Copenhagen Plant Science Center, University of Copenhagen, 1871 Frederiksberg C, Denmark"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9007-0082","authenticated-orcid":false,"given":"Helena","family":"Azinheira","sequence":"additional","affiliation":[{"name":"CIFC\u2014Centro de Investiga\u00e7\u00e3o das Ferrugens do Cafeeiro, Instituto Superior de Agronomia, Universidade de Lisboa, Quinta do Marqu\u00eas, 2784-505 Oeiras, Portugal"},{"name":"LEAF\u2014Linking Landscape, Environment, Agriculture and Food Research Center, Associated Laboratory TERRA, Instituto Superior de Agronomia, Universidade de Lisboa, Tapada da Ajuda, 1349-017 Lisboa, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8807-567X","authenticated-orcid":false,"given":"Javier","family":"Valverde","sequence":"additional","affiliation":[{"name":"CIBIO, InBIO\u2014Research Network in Biodiversity and Evolutionary Biology, University of Porto, Campus Agr\u00e1rio de Vair\u00e3o, 4485-661 Vair\u00e3o, Portugal"},{"name":"Estaci\u00f3n Biol\u00f3gica de Do\u00f1ana, Consejo Superior de Investigaciones Cient\u00edficas (CSIC), Avenida Am\u00e9rico Vespucio 26, Isla de La Cartuja, 41092 Sevilla, Spain"}]},{"given":"A. Jesus","family":"Mu\u00f1oz-Pajares","sequence":"additional","affiliation":[{"name":"CIBIO, InBIO\u2014Research Network in Biodiversity and Evolutionary Biology, University of Porto, Campus Agr\u00e1rio de Vair\u00e3o, 4485-661 Vair\u00e3o, Portugal"},{"name":"Department of Genetics, Faculty of Sciences, University of Granada, 18071 Granada, Spain"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6694-7502","authenticated-orcid":false,"given":"Pedro","family":"Talhinhas","sequence":"additional","affiliation":[{"name":"LEAF\u2014Linking Landscape, Environment, Agriculture and Food Research Center, Associated Laboratory TERRA, Instituto Superior de Agronomia, Universidade de Lisboa, Tapada da Ajuda, 1349-017 Lisboa, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1628-7128","authenticated-orcid":false,"given":"Maria do C\u00e9u","family":"Silva","sequence":"additional","affiliation":[{"name":"CIFC\u2014Centro de Investiga\u00e7\u00e3o das Ferrugens do Cafeeiro, Instituto Superior de Agronomia, Universidade de Lisboa, Quinta do Marqu\u00eas, 2784-505 Oeiras, Portugal"},{"name":"LEAF\u2014Linking Landscape, Environment, Agriculture and Food Research Center, Associated Laboratory TERRA, Instituto Superior de Agronomia, Universidade de Lisboa, Tapada da Ajuda, 1349-017 Lisboa, Portugal"}]}],"member":"1968","published-online":{"date-parts":[[2023,3,28]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","unstructured":"Maghuly, F., Jankowicz-Cieslak, J., and Souleymane, B. (2020). Improving coffee species for pathogen resistance. CAB Rev., 15.","DOI":"10.1079\/PAVSNNR202015009"},{"key":"ref_2","doi-asserted-by":"crossref","unstructured":"Silva, M.d.C., Guerra-Guimar\u00e3es, L., Diniz, I., Loureiro, A., Azinheira, H., Pereira, A.P., Tavares, S., Batista, D., and V\u00e1rzea, V. (2022). An overview of the mechanisms involved in coffee-Hemileia vastatrix interactions: Plant and Pathogen Perspectives. Agronomy, 12.","DOI":"10.3390\/agronomy12020326"},{"key":"ref_3","first-page":"587","article-title":"Coffee rust regains foothold. researchers marshal technology in bid to thwart fungal outbreak in Central America","volume":"493","author":"Cressy","year":"2013","journal-title":"Nature"},{"key":"ref_4","unstructured":"Sieff, K. (Washington Post, 2019). The migration problem is a coffee problem, Washington Post."},{"key":"ref_5","first-page":"199","article-title":"Principles and practice of coffee breeding for resistance to rust and other diseases","volume":"4","author":"Bettencourt","year":"1988","journal-title":"Coffee Agron."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"153","DOI":"10.1007\/s10681-018-2231-2","article-title":"The H\u00edbrido de Timor germplasm: Identification of molecular diversity and resistance sources to coffee berry disease and leaf rust","volume":"214","author":"Silva","year":"2018","journal-title":"Euphytica"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"141","DOI":"10.1007\/s10658-011-9925-9","article-title":"Cellular and molecular analyses of coffee resistance to Hemileia vastatrix and nonhost resistance to Uromyces vignae in the resistance-donor genotype HDT832\/2","volume":"133","author":"Diniz","year":"2012","journal-title":"Eur. J. Plant Pathol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"1039","DOI":"10.1111\/mpp.12512","article-title":"The coffee leaf rust pathogen Hemileia vastatrix: One and a half centuries around the tropics","volume":"18","author":"Talhinhas","year":"2017","journal-title":"Mol. Plant Pathol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"109","DOI":"10.1146\/annurev-phyto-080516-035649","article-title":"From chaos to harmony: Responses and signaling upon microbial pattern recognition","volume":"55","author":"Yu","year":"2017","journal-title":"Annu. Rev. Phytopathol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"243","DOI":"10.1146\/annurev-phyto-080417-045817","article-title":"Structural, functional, and genomic diversity of plant NLR proteins: An evolved resource for rational engineering of plant immunity","volume":"56","author":"Monteiro","year":"2018","journal-title":"Annu. Rev. Phytopathol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"1253","DOI":"10.1094\/MPMI-06-20-0161-CR","article-title":"What is the molecular basis of nonhost resistance?","volume":"33","author":"Panstruga","year":"2020","journal-title":"Mol. Plant Microbe Interact."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1297","DOI":"10.1074\/jbc.M110.211615","article-title":"Physical association of Arabidopsis hypersensitive induced reaction proteins (HIRs) with the immune receptor RPS2","volume":"286","author":"Qi","year":"2011","journal-title":"J. Biol. Chem."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"681","DOI":"10.1023\/A:1005949304445","article-title":"Cloning of tobacco genes that elicit the hypersensitive response","volume":"36","author":"Karrer","year":"1998","journal-title":"Plant Mol. Biol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"273","DOI":"10.1007\/s00299-012-1361-6","article-title":"Wheat hypersensitive-induced reaction genes TaHIR1 and TaHIR3 are involved in response to stripe rust fungus infection and abiotic stresses","volume":"32","author":"Duan","year":"2013","journal-title":"Plant Cell Rep."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"314","DOI":"10.1007\/s11105-012-0504-9","article-title":"Characterization of a Hypersensitive Response-Induced gene TaHIR3 from wheat leaves infected with leaf rust","volume":"31","author":"Yu","year":"2012","journal-title":"Plant Mol. Biol. Rep."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"1094","DOI":"10.1007\/s00122-003-1351-8","article-title":"Barley putative hypersensitive induced reaction genes: Genetic mapping, sequence analyses and differential expression in disease lesion mimic mutants","volume":"107","author":"Rostoks","year":"2003","journal-title":"Theor. Appl. Genet."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"783","DOI":"10.1111\/tpj.14271","article-title":"The Hypersensitive Induced Reaction 3 (HIR3) Gene Contributes to Plant Basal Resistance via an EDS1 and Salicylic Acid-Dependent Pathway","volume":"98","author":"Li","year":"2019","journal-title":"Plant J."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"102039","DOI":"10.1016\/j.pbi.2021.102039","article-title":"EDS1 signalling: At the nexus of intracellular and surface receptor immunity","volume":"62","author":"Dongus","year":"2021","journal-title":"Curr. Opin. Plant Biol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"107","DOI":"10.1111\/j.1469-8137.2011.03675.x","article-title":"Different roles of enhanced disease susceptibility 1 (EDS1) bound to and dissociated from phytoalexin deficient 4 (PAD4) in Arabidopsis immunity","volume":"191","author":"Rietz","year":"2011","journal-title":"New Phytol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"619","DOI":"10.1016\/j.chom.2013.11.006","article-title":"Structural basis for signaling by exclusive EDS1 heteromeric complexes with SAG101 or PAD4 in plant innate immunity","volume":"14","author":"Wagner","year":"2013","journal-title":"Cell Host Microbe"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"1181","DOI":"10.1126\/science.1255274","article-title":"The coffee genome provides insight into the convergent evolution of caffeine biosynthesis","volume":"345","author":"Denoeud","year":"2014","journal-title":"Science"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"1093","DOI":"10.1016\/j.funbio.2015.08.008","article-title":"A method for obtaining RNA from Hemileia vastatrix appressoria produced in planta, suitable for transcriptomic analyses","volume":"119","author":"Loureiro","year":"2015","journal-title":"Fungal Biol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"79","DOI":"10.1086\/314113","article-title":"Cytochemical aspects of the plant-rust fungus interface during the compatible interaction Coffea arabica (cv. Caturra)-Hemileia vastatrix (race III)","volume":"160","author":"Silva","year":"1999","journal-title":"Int. J. Plant Sci."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"169","DOI":"10.1006\/pmpp.2002.0389","article-title":"Hypersensitive cell death and post-haustorial defence responses arrest the orange rust (Hemileia vastatrix) growth in resistant coffee leaves","volume":"60","author":"Silva","year":"2002","journal-title":"Physiol. Mol. Plant Pathol."},{"key":"ref_25","doi-asserted-by":"crossref","unstructured":"Vega-Arregu\u00edn, J.C., Ibarra-Laclette, E., Jim\u00e9nez-Moraila, B., Mart\u00ednez, O., Vielle-Calzada, J.P., Herrera-Estrella, L., and Herrera-Estrella, A. (2009). Deep Sampling of the Palomero Maize Transcriptome by a High Throughput Strategy of Pyrosequencing. BMC Genom., 10.","DOI":"10.1186\/1471-2164-10-299"},{"key":"ref_26","unstructured":"Sambrook, J., and Russell, D.W. (2001). Molecular Cloning: A Laboratory Manual, Cold Spring Harbor Laboratory."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1007\/s11103-012-9885-2","article-title":"miRDeepFinder: A miRNA analysis tool for deep sequencing of plant small RNAs","volume":"80","author":"Xie","year":"2012","journal-title":"Plant Mol. Biol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"62","DOI":"10.1016\/S0304-3940(02)01423-4","article-title":"Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data","volume":"339","author":"Ramakers","year":"2003","journal-title":"Neurosci. Lett."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"e45","DOI":"10.1093\/nar\/29.9.e45","article-title":"A new mathematical model for relative quantification in real-time RT-PCR","volume":"29","author":"Pfaffl","year":"2001","journal-title":"Nucleic Acids Res."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"205","DOI":"10.1006\/jmbi.2000.4042","article-title":"T-coffee: A novel method for fast and accurate multiple sequence alignment","volume":"302","author":"Notredame","year":"2000","journal-title":"J. Mol. Biol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"D200","DOI":"10.1093\/nar\/gkw1129","article-title":"CDD\/SPARCLE: Functional classification of proteins via subfamily domain architectures","volume":"45","author":"Bo","year":"2017","journal-title":"Nucleic Acids Res."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"W429","DOI":"10.1093\/nar\/gkm256","article-title":"Advantages of combined transmembrane topology and signal peptide prediction-the Phobius web server","volume":"35","author":"Krogh","year":"2007","journal-title":"Nucleic Acids Res."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"W202","DOI":"10.1093\/nar\/gkp335","article-title":"MEME Suite: Tools for motif discovery and searching","volume":"37","author":"Bailey","year":"2009","journal-title":"Nucleic Acids Res."},{"key":"ref_34","first-page":"275","article-title":"The rapid generation of mutation data matrices from protein sequences","volume":"8","author":"Jones","year":"1992","journal-title":"Comput. Appl. Biosci."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"1870","DOI":"10.1093\/molbev\/msw054","article-title":"MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets","volume":"33","author":"Kumar","year":"2016","journal-title":"Mol. Biol. Evol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"10","DOI":"10.14806\/ej.17.1.200","article-title":"Cutadapt removes adapter sequences from high-throughput sequencing reads","volume":"17","author":"Martin","year":"2011","journal-title":"EMBnet J."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"1754","DOI":"10.1093\/bioinformatics\/btp324","article-title":"Fast and Accurate Short Read Alignment with Burrows-Wheeler Transform","volume":"25","author":"Li","year":"2009","journal-title":"Bioinformatics"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"343","DOI":"10.1007\/s00018-005-5434-3","article-title":"Ancient origin of reggie (flotillin), reggie-like, and other lipid-raft proteins: Convergent evolution of the SPFH domain","volume":"63","author":"Stuermer","year":"2006","journal-title":"Cell. Mol. Life Sci."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"201","DOI":"10.1016\/j.bbamcr.2008.09.015","article-title":"Plant formins: Diverse isoforms and unique molecular mechanism","volume":"1803","author":"Blanchoin","year":"2010","journal-title":"Biochim. Biophys. Acta"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"4642","DOI":"10.1038\/s41598-020-61216-7","article-title":"A single polyploidization event at the origin of the tetraploid genome of Coffea arabica is responsible for the extremely low genetic variation in wild and cultivated germplasm","volume":"10","author":"Scalabrin","year":"2020","journal-title":"Sci. Rep."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"68","DOI":"10.1094\/MPMI-02-10-0030","article-title":"The hypersensitive induced reaction and leucine-rich repeat proteins regulate plant cell death associated with disease and plant immunity","volume":"24","author":"Choi","year":"2011","journal-title":"Mol. Plant-Microbe Interact."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"1311","DOI":"10.1111\/nph.16208","article-title":"Geminivirus C4 antagonizes the HIR1-mediated hypersensitive response by inhibiting the HIR1 self-interaction and promoting degradation of the protein","volume":"225","author":"Mei","year":"2020","journal-title":"New Phytol."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"772","DOI":"10.1038\/s41467-019-08783-0","article-title":"An EDS1 heterodimer signalling surface enforces timely reprogramming of immunity genes in Arabidopsis","volume":"10","author":"Bhandari","year":"2019","journal-title":"Nat. Commun."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"1802","DOI":"10.1111\/nph.14302","article-title":"A core function of EDS1 with PAD4 is to protect the salicylic acid defense sector in Arabidopsis immunity","volume":"213","author":"Cui","year":"2017","journal-title":"New Phytol."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"1037","DOI":"10.1007\/s00425-010-1107-z","article-title":"A functional EDS1 ortholog is differentially regulated in powdery mildew resistant and susceptible grapevines and complements an Arabidopsis eds1 mutant","volume":"231","author":"Gao","year":"2010","journal-title":"Planta"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"381","DOI":"10.1007\/s11103-014-0235-4","article-title":"Functions of EDS1-like and PAD4 genes in grapevine defenses against powdery mildew","volume":"86","author":"Gao","year":"2014","journal-title":"Plant Mol. Biol."},{"key":"ref_47","doi-asserted-by":"crossref","unstructured":"Garcia, A.V., Blanvillain-Baufume, S., Huibers, R.P., Wiermer, M., Li, G., Gobbato, E., Rietz, S., and Parker, J.E. (2010). Balanced nuclear and cytoplasmic activities of EDS1 are required for a complete plant innate immune response. PLoS Pathog., 6.","DOI":"10.1371\/journal.ppat.1000970"},{"key":"ref_48","first-page":"153","article-title":"EDS1-interacting J protein 1 is an essential negative regulator of plant innate immunity in Arabidopsis","volume":"33","author":"Liu","year":"2021","journal-title":"Plant Cell"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"1071","DOI":"10.1104\/pp.104.055665","article-title":"Cloning and functional characterization of a formin-like protein (AtFH8) from Arabidopsis","volume":"138","author":"Yi","year":"2005","journal-title":"Plant Physiol."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"529","DOI":"10.1111\/j.1469-8137.2005.01582.x","article-title":"Arabidopsis group Ie formins localize to specific cell membrane domains, interact with actin-binding proteins and cause defects in cell expansion upon aberrant expression","volume":"168","author":"Deeks","year":"2005","journal-title":"New Phytol."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"299","DOI":"10.1111\/jipb.12445","article-title":"From filaments to function: The role of the plant actin cytoskeleton in pathogen perception, signaling and immunity","volume":"58","author":"Porter","year":"2016","journal-title":"J. Integr. Plant Biol."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"253","DOI":"10.1146\/annurev-phyto-010820-012840","article-title":"Origins and immunity networking functions of EDS1 family proteins","volume":"58","author":"Lapin","year":"2020","journal-title":"Annu. Rev. Phytopathol."},{"key":"ref_53","doi-asserted-by":"crossref","unstructured":"Bernacki, M.J., Czarnocka, W., Szechynska-Hebda, M., Mittler, R., and Karpinski, S. (2019). Biotechnological potential of LSD1, EDS1, and PAD4 in the improvement of crops and industrial plants. Plants, 8.","DOI":"10.3390\/plants8080290"},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"527","DOI":"10.1007\/s00299-015-1901-y","article-title":"PAD4, LSD1 and EDS1 regulate drought tolerance, plant biomass production, and cell wall properties","volume":"35","author":"Czarnocka","year":"2016","journal-title":"Plant Cell Rep."}],"container-title":["Agronomy"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2073-4395\/13\/4\/992\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T19:04:32Z","timestamp":1760123072000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2073-4395\/13\/4\/992"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,3,28]]},"references-count":54,"journal-issue":{"issue":"4","published-online":{"date-parts":[[2023,4]]}},"alternative-id":["agronomy13040992"],"URL":"https:\/\/doi.org\/10.3390\/agronomy13040992","relation":{},"ISSN":["2073-4395"],"issn-type":[{"type":"electronic","value":"2073-4395"}],"subject":[],"published":{"date-parts":[[2023,3,28]]}}}