{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,12]],"date-time":"2026-09-12T02:29:46Z","timestamp":1789180186103,"version":"build-2803163510"},"reference-count":114,"publisher":"MDPI AG","issue":"14","license":[{"start":{"date-parts":[[2026,7,10]],"date-time":"2026-07-10T00:00:00Z","timestamp":1783641600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Plants"],"abstract":"<jats:p>The increasing threat posed by wheat rust diseases caused by Puccinia spp. necessitates the development of resistance strategies that extend beyond conventional race-specific mechanisms. Although recent reviews (2023\u20132025) have emphasized gene discovery and genomic approaches, comparatively less attention has been given to the potential roles of metabolic regulation and micronutrient homeostasis in host\u2013pathogen interactions. Here, we present a narrative synthesis of current evidence and propose a conceptual framework in which induced mutagenesis (ethyl methanesulfonate, EMS, and \u03b3-irradiation) serves as a tool for investigating interactions among redox regulation, iron (Fe) homeostasis, and disease resistance. A key component of this framework is the proposed interplay between reactive oxygen species (ROS) signaling and Fe partitioning. Vacuolar iron transporters (VITs), ferritins, and associated transport networks regulate intracellular Fe distribution and may influence Fe availability at the host\u2013pathogen interface, potentially affecting fungal development and host defense responses. This concept of \u201ciron-withholding immunity\u201d may operate alongside ROS-mediated defense processes, linking metabolism with immune function. Observations from mutant wheat populations are broadly consistent with the hypothesis that these processes may contribute to durable adult-plant resistance (APR), which is characterized by reduced disease development, coordinated defense responses, and relative stability across environments. In some studies, Fe-enriched mutant lines have been associated with enhanced expression of pathogenesis-related genes and the occurrence of combined APR and seedling-resistance phenotypes, suggesting possible links between micronutrient homeostasis and immunity. Integration of high-throughput phenotyping with genotype \u00d7 environment \u00d7 time (G \u00d7 E \u00d7 T) frameworks may further improve our understanding of quantitative resistance and disease-associated traits. Overall, this review highlights the potential importance of nutrient homeostasis, redox regulation, and susceptibility modulation as components of future research aimed at developing climate-resilient and nutritionally improved wheat cultivars.<\/jats:p>","DOI":"10.3390\/plants15142131","type":"journal-article","created":{"date-parts":[[2026,7,10]],"date-time":"2026-07-10T09:46:47Z","timestamp":1783676807000},"page":"2131","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":1,"title":["Beyond R-Genes: Dissecting Metabolic and Nutrient-Driven Wheat Rust Resistance Through Induced Mutagenesis"],"prefix":"10.3390","volume":"15","author":[{"given":"Saule","family":"Kenzhebayeva","sequence":"first","affiliation":[{"name":"Biotechnology Department, Al-Farabi Kazakh National University, Al-Farabi Av. 71, Almaty 050041, Kazakhstan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2284-5077","authenticated-orcid":false,"given":"Alfia","family":"Abekova","sequence":"additional","affiliation":[{"name":"Kazakh Research Institute of Agriculture and Crop Production, Erlepesov Street 1, Almalybak Village, Almaty Region 040909, Kazakhstan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nargul","family":"Omirbekova","sequence":"additional","affiliation":[{"name":"Biotechnology Department, Al-Farabi Kazakh National University, Al-Farabi Av. 71, Almaty 050041, Kazakhstan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sabina","family":"Shoinbekova","sequence":"additional","affiliation":[{"name":"Biotechnology Department, Al-Farabi Kazakh National University, Al-Farabi Av. 71, Almaty 050041, Kazakhstan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Saule","family":"Atabayeva","sequence":"additional","affiliation":[{"name":"Biotechnology Department, Al-Farabi Kazakh National University, Al-Farabi Av. 71, Almaty 050041, Kazakhstan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Gulina","family":"Doktyrbay","sequence":"additional","affiliation":[{"name":"Biotechnology Department, Al-Farabi Kazakh National University, Al-Farabi Av. 71, Almaty 050041, Kazakhstan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Aigul","family":"Amirova","sequence":"additional","affiliation":[{"name":"Biotechnology Department, Al-Farabi Kazakh National University, Al-Farabi Av. 71, Almaty 050041, Kazakhstan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Albrecht","family":"Serfling","sequence":"additional","affiliation":[{"name":"Federal Research Centre for Cultivated Plants (JKI), Institute for Resistance Research and Stress Tolerance, Erwin-Baur-Str. 27, 06484 Quedlinburg, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2026,7,10]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","unstructured":"Ellis, J.G., Lagudah, E.S., Spielmeyer, W., and Dodds, P.N. (2014). The past, present and future of breeding rust resistant wheat. Front. Plant Sci., 5.","DOI":"10.3389\/fpls.2014.00641"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"2113","DOI":"10.1094\/PDIS-09-18-1638-SR","article-title":"Virulence of Puccinia triticina, the wheat leaf rust fungus, in the United States in 2017","volume":"103","author":"Kolmer","year":"2019","journal-title":"Plant Dis."},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"Bhardwaj, S.C., Singh, G.P., Gangwar, O.P., Prasad, P., and Kumar, S. (2019). Status of wheat rust research and progress in rust management-Indian context. Agronomy, 9.","DOI":"10.3390\/agronomy9120892"},{"key":"ref_4","doi-asserted-by":"crossref","unstructured":"Huerta-Espino, J., Singh, R., Crespo-Herrera, L.A., Villase\u00f1or-Mir, H.E., Rodriguez-Garcia, M.F., Dreisigacker, S., Barcenas-Santana, D., and Lagudah, E. (2020). Adult plant slow rusting genes confer high levels of resistance to rusts in bread wheat cultivars from Mexico. Front. Plant Sci., 11.","DOI":"10.3389\/fpls.2020.00824"},{"key":"ref_5","doi-asserted-by":"crossref","unstructured":"Mapuranga, J., Zhang, N., Zhang, L., Liu, W., Chang, J., and Yang, W. (2022). Harnessing genetic resistance to rusts in wheat and integrated rust management methods to develop more durable resistant cultivars. Front. Plant Sci., 13.","DOI":"10.3389\/fpls.2022.951095"},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"Ren, X., Wang, C., Ren, Z., Wang, J., Zhang, P., Zhao, S., Li, M., Yuan, M., Yu, X., and Li, Z. (2023). Genetics of resistance to leaf rust in wheat: An overview in a genome-wide level. Sustainability, 15.","DOI":"10.3390\/su15043247"},{"key":"ref_7","doi-asserted-by":"crossref","unstructured":"Rehman, S.U., Qiao, L., Shen, T., Hua, L., Li, H., Ahmad, Z., and Chen, S. (2024). Exploring the frontier of wheat rust resistance: Latest approaches, mechanisms, and novel insights. Plants, 13.","DOI":"10.3390\/plants13172502"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"201","DOI":"10.1146\/annurev-phyto-121923-082727","article-title":"Challenges to wheat disease resistance and current global strategies","volume":"63","author":"Singh","year":"2025","journal-title":"Annu. Rev. Phytopathol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"495","DOI":"10.1111\/1574-6976.12004","article-title":"The impact of transition metals on bacterial plant disease","volume":"37","author":"Fones","year":"2013","journal-title":"FEMS Microbiol. Rev."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"1377","DOI":"10.1126\/science.aal4273","article-title":"Starving the enemy","volume":"354","author":"Dodds","year":"2016","journal-title":"Science"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"E913","DOI":"10.1073\/pnas.1619268114","article-title":"Uncovering hidden variation in polyploid wheat","volume":"114","author":"Krasileva","year":"2017","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"435","DOI":"10.1146\/annurev-genet-120116-024533","article-title":"Combining traditional mutagenesis with new high-throughput sequencing and genome editing to reveal hidden variation in polyploid wheat","volume":"51","author":"Uauy","year":"2017","journal-title":"Annu. Rev. Genet."},{"key":"ref_13","doi-asserted-by":"crossref","unstructured":"Komura, S., Jinno, H., Sonoda, T., Oono, Y., Handa, H., Takumi, S., Yoshida, K., and Kobayashi, F. (2022). Genome sequencing-based coverage analyses facilitate high-resolution detection of deletions linked to phenotypes of gamma-irradiated wheat mutants. BMC Genom., 23.","DOI":"10.1186\/s12864-022-08344-8"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"9339","DOI":"10.1038\/s41467-025-64428-5","article-title":"Genome-assisted identification of wheat leaf rust resistance gene Lr.ace-4A\/Lr30","volume":"16","author":"Yang","year":"2025","journal-title":"Nat. Commun."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"56","DOI":"10.1007\/s11032-025-01576-y","article-title":"Durum wheat mutants with enhanced disease resistance to stripe rust show differential responses to other fungal diseases","volume":"45","author":"Lunde","year":"2025","journal-title":"Mol. Breed."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"689","DOI":"10.3390\/cimb46010045","article-title":"Phenotyping and exploitation of kompetitive allele-specific PCR assays for genes underpinning leaf rust resistance in new spring wheat mutant lines","volume":"46","author":"Kenzhebayeva","year":"2024","journal-title":"Curr. Issues Mol. Biol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"100551","DOI":"10.1016\/j.cpb.2025.100551","article-title":"Identification of unknown leaf and stripe rust resistances in adult and seedling stages of Fe and Zn biofortified spring wheat mutant lines using microscopy, KASP markers and expression dynamics of pathogenesis-related (PR) protein genes","volume":"44","author":"Kenzhebayeva","year":"2025","journal-title":"Curr. Plant Biol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"224","DOI":"10.1007\/s00122-024-04730-w","article-title":"Wheat improvement through advances in single nucleotide polymorphism (SNP) detection and genotyping with a special emphasis on rust resistance","volume":"137","author":"Geethanjali","year":"2024","journal-title":"Theor. Appl. Genet."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"811","DOI":"10.1093\/aob\/mcp128","article-title":"New insights into ferritin synthesis and function highlight a link between iron homeostasis and oxidative stress in plants","volume":"105","author":"Briat","year":"2009","journal-title":"Ann. Bot."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"813","DOI":"10.1039\/C7MT00136C","article-title":"Iron homeostasis in plants\u2014A brief overview","volume":"9","author":"Connorton","year":"2017","journal-title":"Metallomics"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"e13515","DOI":"10.7717\/peerj.13515","article-title":"Organ-specific expression of genes involved in iron homeostasis in wheat mutant lines with increased grain iron and zinc content","volume":"10","author":"Kenzhebayeva","year":"2022","journal-title":"PeerJ"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"3001","DOI":"10.1093\/jxb\/erv155","article-title":"New insights into the role of siderophores as triggers of plant immunity: What can we learn from animals?","volume":"66","author":"Aznar","year":"2015","journal-title":"J. Exp. Bot."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"355","DOI":"10.1146\/annurev-phyto-080516-035537","article-title":"Iron and immunity","volume":"55","author":"Verbon","year":"2017","journal-title":"Ann. Rev. Phytopathol."},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"Mapuranga, J., Zhang, M., and Xiao, S. (2023). The underexplored mechanisms of wheat resistance to leaf rust. Plants, 12.","DOI":"10.3390\/plants12233996"},{"key":"ref_25","doi-asserted-by":"crossref","unstructured":"M\u00e9rida-Garc\u00eda, R., G\u00e1lvez, S., Sol\u00eds, I., Mart\u00ednez-Moreno, F., Camino, C., Soriano, J.M., Sansaloni, C., Ammar, K., Bentley, A.R., and Gonzalez-Dugo, V. (2024). High-throughput phenotyping using hyperspectral indicators supports the genetic dissection of yield in durum wheat grown under heat and drought stress. Front. Plant Sci., 15.","DOI":"10.3389\/fpls.2024.1470520"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"100149","DOI":"10.1016\/j.plaphe.2025.100149","article-title":"Predictions of wheat phenotypic variability by integrating high-throughput phenotyping observations into a crop growth model","volume":"8","author":"Cai","year":"2025","journal-title":"Plant Phenomics"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"431","DOI":"10.1080\/13102818.2017.1304180","article-title":"Genetic analysis of rust resistance genes in global wheat cultivars: An overview","volume":"31","author":"Hanafi","year":"2017","journal-title":"Biotechnol. Biotechnol. Equip."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"102311","DOI":"10.1016\/j.pbi.2022.102311","article-title":"Emerging principles in the design of bioengineered made-to-order plant immune receptors","volume":"70","author":"Marchal","year":"2022","journal-title":"Curr. Opin. Plant Biol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"1523","DOI":"10.1111\/mpp.12618","article-title":"A review of wheat diseases\u2014A field perspective","volume":"19","author":"Figueroa","year":"2017","journal-title":"Mol. Plant Pathol."},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"Avasthi, S., Gautam, A.K., Niranjan, M., Verma, R.K., Karunarathna, S.C., Kumar, A., and Suwannarach, N. (2023). Insights into diversity, distribution, and systematics of rust genus Puccinia. J. Fungi, 9.","DOI":"10.3390\/jof9060639"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"430","DOI":"10.1038\/s41559-018-0793-y","article-title":"The global burden of pathogens and pests on major food crops","volume":"3","author":"Savary","year":"2019","journal-title":"Nat. Ecol. Evol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"S333","DOI":"10.1080\/07060661.2021.1888156","article-title":"Physiologic specialization of Puccinia triticina, the causal agent of wheat leaf rust, in Canada in 2015\u20132019","volume":"43","author":"McCallum","year":"2021","journal-title":"Can. J. Plant Pathol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"3282","DOI":"10.1093\/gbe\/evx241","article-title":"Pathogenomic analysis of wheat yellow rust lineages detects seasonal variation and host specificity","volume":"9","author":"Persoons","year":"2017","journal-title":"Genome Biol. Evol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"phcs20240023","DOI":"10.1079\/planthealthcases.2024.0023","article-title":"Wheat leaf rust, caused by Puccinia triticina, and mitigation through host genetic resistance","volume":"11","author":"McCallum","year":"2024","journal-title":"Plant Health Cases"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"179","DOI":"10.1007\/s00122-024-04689-8","article-title":"Genome-wide atlas of rust resistance loci in wheat","volume":"137","author":"Tong","year":"2024","journal-title":"Theor. Appl. Genet."},{"key":"ref_36","doi-asserted-by":"crossref","unstructured":"Petre, B., Joly, D.L., and Duplessis, S. (2014). Effector proteins of rust fungi. Front. Plant Sci., 5.","DOI":"10.3389\/fpls.2014.00416"},{"key":"ref_37","doi-asserted-by":"crossref","unstructured":"Pati, R., Sandhu, S., Kawadiwale, A.K., and Kaur, G. (2025). Unveiling the underlying complexities in breeding for disease resistance in crop plants: Review. Front. Plant Sci., 16.","DOI":"10.3389\/fpls.2025.1559751"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1007\/s44154-025-00230-z","article-title":"A fungal effector hijacks a plastid protein to dampen plant immunity; PR1 is here for rescue","volume":"5","author":"Khan","year":"2025","journal-title":"Stress. Biol."},{"key":"ref_39","doi-asserted-by":"crossref","unstructured":"Kainat, M., Mujtaba, M., Wang, Y., and Zhou, B. (2025). Effectors of plant pathogenic fungi and fungal-like microbes: A comprehensive review on mechanisms, roles, and host interactions. Front. Plant Sci., 16.","DOI":"10.3389\/fpls.2025.1626960"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"14718","DOI":"10.1038\/s41598-018-32825-0","article-title":"A rust fungal effector binds plant DNA and modulates transcription","volume":"8","author":"Ahmed","year":"2018","journal-title":"Sci. Rep."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.pbi.2019.02.005","article-title":"Cell surface immune receptors: The guardians of the plant\u2019s extracellular spaces","volume":"50","author":"Kanyuka","year":"2019","journal-title":"Curr. Opin. Plant Biol."},{"key":"ref_42","doi-asserted-by":"crossref","unstructured":"Qi, Y., Li, J., Mapuranga, J., Zhang, N., Chang, J., Shen, Q., Zhang, Y., Wei, J., Cui, L., and Liu, D. (2023). Wheat leaf rust fungus effector Pt13024 is avirulent to TcLr30. Front. Plant Sci., 13.","DOI":"10.3389\/fpls.2022.1098549"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"1604","DOI":"10.1126\/science.aao7294","article-title":"Variation in the AvrSr35 gene determines Sr35 resistance against wheat stem rust race Ug99","volume":"358","author":"Salcedo","year":"2017","journal-title":"Science"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"1220","DOI":"10.1038\/s41477-021-00971-5","article-title":"Genomics accelerated isolation of a new stem rust avirulence gene\u2013wheat resistance gene pair","volume":"7","author":"Upadhyaya","year":"2021","journal-title":"Nat. Plants"},{"key":"ref_45","doi-asserted-by":"crossref","unstructured":"Asghar, R., Cheng, Y., Wu, N., and Akkaya, M.S. (2025). A Puccinia striiformis f. sp. Tritici effector with DPBB domain suppresses wheat defense. Plants, 14.","DOI":"10.3390\/plants14030435"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1007\/s00425-019-03167-6","article-title":"Rust pathogen effectors: Perspectives in resistance breeding","volume":"250","author":"Prasad","year":"2019","journal-title":"Planta"},{"key":"ref_47","doi-asserted-by":"crossref","unstructured":"Song, L., Cui, L., Li, H., Zhang, N., and Yang, W. (2025). Wheat leaf rust effector Pt48115 localized in the chloroplasts and suppressed wheat immunity. J. Fungi, 11.","DOI":"10.3390\/jof11010080"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"2530","DOI":"10.1093\/plphys\/kiab434","article-title":"Two stripe rust effectors impair wheat resistance by suppressing import of host Fe-S protein into chloroplasts","volume":"187","author":"Wang","year":"2021","journal-title":"Plant Physiol."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"703","DOI":"10.4161\/viru.29652","article-title":"Effector biology during biotrophic invasion of plant cells","volume":"5","author":"Chaudhari","year":"2014","journal-title":"Virulence"},{"key":"ref_50","first-page":"100103","article-title":"NLRs in plant immunity: Structural insights and molecular mechanisms","volume":"4","author":"Gu","year":"2025","journal-title":"Crop Des."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"1360","DOI":"10.1126\/science.1166453","article-title":"A putative ABC transporter confers durable resistance to multiple fungal pathogens in wheat","volume":"323","author":"Krattinger","year":"2009","journal-title":"Science"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"1494","DOI":"10.1038\/ng.3439","article-title":"A recently evolved hexose transporter variant confers resistance to multiple pathogens in wheat","volume":"47","author":"Moore","year":"2015","journal-title":"Nat. Genet."},{"key":"ref_53","doi-asserted-by":"crossref","unstructured":"Hao, Y., Pan, Y., Chen, W., Rashid, M.A.R., Li, M., Che, N., Duan, X., and Zhao, Y. (2023). Contribution of Duplicated Nucleotide-Binding Leucine-Rich Repeat (NLR) Genes to Wheat Disease Resistance. Plants, 12.","DOI":"10.20944\/preprints202306.1693.v1"},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"3445","DOI":"10.1111\/pce.14144","article-title":"Lr21 diversity unveils footprints of wheat evolution and its new role in broad-spectrum leaf rust resistance","volume":"44","author":"Naz","year":"2021","journal-title":"Plant Cell Environ."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"btae581","DOI":"10.1093\/bioinformatics\/btae581","article-title":"Identifying nucleotide-binding leucine-rich repeat receptor and pathogen effector pairing using transfer-learning and bilinear attention network","volume":"40","author":"Qiao","year":"2024","journal-title":"Bioinformatics"},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"31308","DOI":"10.1038\/s41598-024-82772-2","article-title":"Evaluation of resistance and molecular detection of resistance genes to wheat stripe rust of 82 wheat cultivars in Xinjiang, China","volume":"14","author":"Zhang","year":"2024","journal-title":"Sci. Rep."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"486","DOI":"10.1134\/S2079059712060081","article-title":"Identification of sources of resistance to wheat stem rust using molecular markers","volume":"2","author":"Kokhmetova","year":"2012","journal-title":"Russ. J. Genet. Appl. Res."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"02021","DOI":"10.1051\/bioconf\/202410002021","article-title":"Determination of resistance to yellow rust in new breeding mutant lines of spring wheat at adult plant and seedling stages","volume":"100","author":"Kenzhebayeva","year":"2024","journal-title":"BIO Web Conf."},{"key":"ref_59","doi-asserted-by":"crossref","unstructured":"Beukert, U., Pfeiffer, N., Ebmeyer, E., Hinterberger, V., Lueck, S., Serfling, A., Ordon, F., Schulthess, A.W., and Reif, J.C. (2021). Efficiency of a seedling phenotyping strategy to support european wheat breeding focusing on leaf rust resistance. Biology, 10.","DOI":"10.3390\/biology10070628"},{"key":"ref_60","doi-asserted-by":"crossref","unstructured":"Serfling, A., Templer, S.E., Winter, P., and Ordon, F. (2016). Microscopic and molecular characterization of the prehaustorial resistance against wheat leaf rust (Puccinia triticina) in Einkorn (Triticum monococcum). Front. Plant Sci., 7.","DOI":"10.3389\/fpls.2016.01668"},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"1285","DOI":"10.1104\/pp.18.00945","article-title":"The wheat Lr67 gene from the sugar transport protein 13 family confers multipathogen resistance in barley","volume":"179","author":"Milne","year":"2019","journal-title":"Plant Physiol."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"eadv1760","DOI":"10.1126\/sciadv.adv1760","article-title":"Stripe rust fungi hijack a host transcriptional repressor to induce TaSWEET14d for enhanced sugar uptake in wheat","volume":"11","author":"Zheng","year":"2025","journal-title":"Sci. Adv."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"1254","DOI":"10.1093\/plphys\/kiad104","article-title":"Expression of the wheat multipathogen resistance hexose transporter Lr67res is associated with anion fluxes","volume":"192","author":"Milne","year":"2023","journal-title":"Plant Physiol."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"13444","DOI":"10.1074\/jbc.REV120.010856","article-title":"Iron homeostasis and plant immune responses: Recent insights and translational implications","volume":"295","author":"Herlihy","year":"2020","journal-title":"J. Biol. Chem."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"285","DOI":"10.1105\/tpc.17.00579","article-title":"Defended to the nines: 25 years of resistance gene cloning identifies nine mechanisms for R protein function","volume":"30","author":"Kourelis","year":"2018","journal-title":"Plant Cell."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"33","DOI":"10.1016\/j.tplants.2014.07.005","article-title":"Iron nutrition, biomass production, and plant product quality","volume":"20","author":"Briat","year":"2015","journal-title":"Trends Plant Sci."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"163","DOI":"10.1023\/A:1015678432355","article-title":"The population genetics of plant pathogens and breeding strategies for durable resistance","volume":"124","author":"McDonald","year":"2002","journal-title":"Euphytica"},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"e53817","DOI":"10.15252\/embr.202153817","article-title":"MAP kinase cascades in plant development and immune signaling","volume":"23","author":"Sun","year":"2022","journal-title":"EMBO Rep."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"jkac247","DOI":"10.1093\/g3journal\/jkac247","article-title":"Comprehensive analysis of pathogen-responsive wheat NAC transcription factors: New candidates for crop improvement","volume":"12","author":"Vranic","year":"2022","journal-title":"G3 Genes Genomes Genet."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"836","DOI":"10.1093\/plphys\/kiab127","article-title":"Plant SWEETs: From sugar transport to plant-pathogen interaction and more unexpected physiological roles","volume":"186","author":"Breia","year":"2021","journal-title":"Plant Physiol."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"eaav5868","DOI":"10.1126\/science.aav5868","article-title":"Ligand-triggered allosteric ADP release primes a plant NLR complex","volume":"364","author":"Wang","year":"2019","journal-title":"Science"},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"200","DOI":"10.3390\/agronomy3010200","article-title":"Induced mutations unleash the potentials of plant genetic resources for food and agriculture","volume":"3","author":"Mba","year":"2013","journal-title":"Agronomy"},{"key":"ref_73","doi-asserted-by":"crossref","unstructured":"Qi, T., Wang, J., Sun, Q., Day, B., Guo, J., and Ma, Q. (2017). TaARPC3, Contributes to wheat resistance against the stripe rust fungus. Front. Plant Sci., 8.","DOI":"10.3389\/fpls.2017.01245"},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"1929","DOI":"10.1111\/pbi.14312","article-title":"CRISPR-targeted mutagenesis of mitogen-activated protein kinase phosphatase 1 improves both immunity and yield in wheat","volume":"22","author":"Liu","year":"2024","journal-title":"Plant Biotechnol. J."},{"key":"ref_75","first-page":"233","article-title":"Utilizing high-throughput phenotyping for disease resistance in wheat","volume":"15","author":"Zhang","year":"2024","journal-title":"Mol. Plant Breed."},{"key":"ref_76","doi-asserted-by":"crossref","unstructured":"Kaushal, S., Gill, H.S., Billah, M.M., Khan, S.N., Halder, J., Bernardo, A., Amand, P.S., Bai, G., Glover, K., and Maimaitijiang, M. (2024). Enhancing the potential of phenomic and genomic prediction in winter wheat breeding using high-throughput phenotyping and deep learning. Front. Plant Sci., 15.","DOI":"10.3389\/fpls.2024.1410249"},{"key":"ref_77","doi-asserted-by":"crossref","unstructured":"Abdelhameed, A.A., Ali, M., Darwish, D.B.E., AlShaqhaa, M.A., Selim, D.A.H., Nagah, A., and Zayed, M. (2024). Induced genetic diversity through mutagenesis in wheat gene pool and significant use of SCoT markers to underpin key agronomic traits. BMC Plant Biol., 24.","DOI":"10.1186\/s12870-024-05345-5"},{"key":"ref_78","doi-asserted-by":"crossref","unstructured":"Uauy, C., Paraiso, F., Colasuonno, P., Tran, R.K., Tsai, H., Berardi, S., Comai, L., and Dubcovsky, J. (2009). A modified TILLING approach to detect induced mutations in tetraploid and hexaploid wheat. BMC Plant Biol., 9.","DOI":"10.1186\/1471-2229-9-115"},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"80","DOI":"10.1007\/s11032-025-01588-8","article-title":"Speed breeding enhances crop resilience and productivity in a changing climate","volume":"45","author":"Kayess","year":"2025","journal-title":"Mol. Breed."},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1038\/s41477-017-0083-8","article-title":"Speed breeding is a powerful tool to accelerate crop research and breeding","volume":"4","author":"Watson","year":"2018","journal-title":"Nat. Plants"},{"key":"ref_81","doi-asserted-by":"crossref","unstructured":"Alam, M., Baenziger, P.S., and Frels, K. (2024). Emerging Trends in Wheat (Triticum spp.) Breeding: Implications for the Future. Front. Biosci., 16.","DOI":"10.31083\/j.fbe1601002"},{"key":"ref_82","doi-asserted-by":"crossref","unstructured":"Wulff, B.B.H., and Moscou, M.J. (2014). Strategies for transferring resistance into wheat: From wide crosses to GM cassettes. Front. Plant Sci., 5.","DOI":"10.3389\/fpls.2014.00692"},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"667","DOI":"10.1094\/PHYTO-02-23-0041-IA","article-title":"The keys to controlling wheat rusts: Identification and deployment of genetic resistance","volume":"113","author":"Norman","year":"2023","journal-title":"Phytopathol."},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1080\/13102818.2015.1087333","article-title":"Principle and application of plant mutagenesis in crop improvement: A review","volume":"30","author":"Oladosu","year":"2016","journal-title":"Biotechnol. Biotechnol. Equip."},{"key":"ref_85","doi-asserted-by":"crossref","unstructured":"Abdulridha, J., Min, A., Rouse, M.N., Kianian, S., Isler, V., and Yang, C. (2023). Evaluation of stem rust disease in wheat fields by drone hyperspectral imaging. Sensors, 23.","DOI":"10.2139\/ssrn.4314627"},{"key":"ref_86","doi-asserted-by":"crossref","unstructured":"Chen, Y.-E., Cui, J.-M., Su, Y.-Q., Yuan, S., Yuan, M., and Zhang, H.-Y. (2015). Influence of stripe rust infection on the photosynthetic characteristics and antioxidant system of susceptible and resistant wheat cultivars at the adult plant stage. Front. Plant Sci., 6.","DOI":"10.3389\/fpls.2015.00779"},{"key":"ref_87","doi-asserted-by":"crossref","unstructured":"Guo, A., Huang, W., Ye, H., Dong, Y., Ma, H., Ren, Y., and Ruan, C. (2020). Identification of wheat yellow rust using spectral and texture features of hyperspectral images. Remote Sens., 12.","DOI":"10.3390\/rs12091419"},{"key":"ref_88","doi-asserted-by":"crossref","unstructured":"Terentev, A., Badenko, V., Shaydayuk, E., Emelyanov, D., Eremenko, D., Klabukov, D., Fedotov, A., and Dolzhenko, V. (2023). Hyperspectral remote sensing for early detection of wheat leaf rust caused by Puccinia triticina. Agriculture, 13.","DOI":"10.3390\/agriculture13061186"},{"key":"ref_89","doi-asserted-by":"crossref","unstructured":"Yao, Z., Lei, Y., and He, D. (2019). Early visual detection of wheat stripe rust using visible\/near-infrared hyperspectral imaging. Sensors, 19.","DOI":"10.3390\/s19040952"},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"320","DOI":"10.1111\/nph.14097","article-title":"Molecular genetics and evolution of disease resistance in cereals","volume":"212","author":"Krattinger","year":"2016","journal-title":"New Phytol."},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"100729","DOI":"10.1016\/j.stress.2024.100729","article-title":"Metabolic responses to multi-stress: An update","volume":"15","author":"Bulut","year":"2025","journal-title":"Plant Stress."},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"663","DOI":"10.1038\/s41580-022-00499-2","article-title":"Reactive oxygen species signalling in plant stress responses","volume":"23","author":"Mittler","year":"2022","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"209","DOI":"10.1146\/annurev-arplant-042817-040322","article-title":"Reactive oxygen species in plant signaling","volume":"69","author":"Waszczak","year":"2018","journal-title":"Annu. Rev. Plant Biol."},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"109259","DOI":"10.1016\/j.plaphy.2024.109259","article-title":"Do different wheat ploidy levels respond differently against stripe rust infection: Interplay between reactive oxygen species (ROS) and the antioxidant defense system?","volume":"219","author":"Jan","year":"2025","journal-title":"Plant Physiol. Biochem."},{"key":"ref_95","doi-asserted-by":"crossref","first-page":"101960","DOI":"10.1016\/j.pmpp.2023.101960","article-title":"Antioxidant enzymes activity and gene expression in wheat\u2013stripe rust interaction at seedling stage","volume":"124","author":"Zainy","year":"2023","journal-title":"Physiol. Mol. Plant Pathol."},{"key":"ref_96","doi-asserted-by":"crossref","first-page":"2515","DOI":"10.1074\/jbc.M113.514828","article-title":"Ascorbate efflux as a new strategy for iron reduction and transport in plants","volume":"289","author":"Grillet","year":"2014","journal-title":"J. Biol. Chem."},{"key":"ref_97","doi-asserted-by":"crossref","first-page":"131","DOI":"10.1146\/annurev-arplant-042811-105522","article-title":"Iron uptake, translocation, and regulation in higher plants","volume":"63","author":"Kobayashi","year":"2012","journal-title":"Annu. Rev. Plant Biol."},{"key":"ref_98","doi-asserted-by":"crossref","first-page":"1833","DOI":"10.1111\/nph.20366","article-title":"Combating plant diseases through transition metal allocation","volume":"245","author":"De","year":"2025","journal-title":"New Phytol."},{"key":"ref_99","doi-asserted-by":"crossref","first-page":"100328","DOI":"10.1016\/j.cpb.2024.100328","article-title":"Iron biofortification in wheat: Past, present, and future","volume":"38","author":"Tanin","year":"2024","journal-title":"Curr. Plant Biol."},{"key":"ref_100","doi-asserted-by":"crossref","first-page":"652","DOI":"10.1038\/nbt.3543","article-title":"Rapid cloning of disease-resistance genes in plants using mutagenesis and sequence capture","volume":"34","author":"Steuernagel","year":"2016","journal-title":"Nat. Biotechnol."},{"key":"ref_101","doi-asserted-by":"crossref","unstructured":"Hussain, M., Iqbal, M.A., Till, B.J., and Rahman, M.-u. (2018). Identification of induced mutations in hexaploid wheat genome using exome capture assay. PLoS ONE, 13.","DOI":"10.1371\/journal.pone.0201918"},{"key":"ref_102","doi-asserted-by":"crossref","unstructured":"Babu, P., Baranwal, D.K., Pal, D., Bharti, H., Joshi, P., Thiyagarajan, B., Gaikwad, K.B., Bhardwaj, S.C., and Singh, G.P. (2020). Application of genomics tools in wheat breeding to attain durable rust resistance. Front. Plant Sci., 11.","DOI":"10.3389\/fpls.2020.567147"},{"key":"ref_103","doi-asserted-by":"crossref","first-page":"39","DOI":"10.1007\/s42976-025-00750-4","article-title":"Durable resistance to stripe rust in wheat: Integration of breeding tools and genomic technologies","volume":"54","author":"Youssef","year":"2025","journal-title":"Cereal Res. Commun."},{"key":"ref_104","doi-asserted-by":"crossref","unstructured":"Waites, J., Achary, V.M.M., Syombua, E.D., Hearne, S.J., and Bandyopadhyay, A. (2025). CRISPR-mediated genome editing of wheat for enhancing disease resistance. Front. Genome Ed., 7.","DOI":"10.3389\/fgeed.2025.1542487"},{"key":"ref_105","doi-asserted-by":"crossref","unstructured":"Jost, M., Outram, M.A., Dibley, K., Zhang, J., Luo, M., and Ayliffe, M. (2023). Plant and pathogen genomics: Essential approaches for stem rust resistance gene stacks in wheat. Front. Plant Sci., 14.","DOI":"10.3389\/fpls.2023.1223504"},{"key":"ref_106","doi-asserted-by":"crossref","first-page":"e70093","DOI":"10.1002\/tpg2.70093","article-title":"Genomic exploration of durable wheat rust resistance by integrating data from multiple worldwide populations","volume":"18","author":"Joukhadar","year":"2025","journal-title":"Plant Genome"},{"key":"ref_107","doi-asserted-by":"crossref","unstructured":"Kokhmetova, A., Rathan, N.D., Sehgal, D., Malysheva, A., Kumarbayeva, M., Nurzhuma, M., Bolatbekova, A., Krishnappa, G., Gultyaeva, E., and Kokhmetova, A. (2023). QTL mapping of seedling and adult plant resistance for stripe and leaf rust in two winter wheat populations. Front. Genet., 14.","DOI":"10.3389\/fgene.2023.1265859"},{"key":"ref_108","doi-asserted-by":"crossref","first-page":"159","DOI":"10.1007\/s10681-022-03111-y","article-title":"Genetic and genomic approaches for breeding rust resistance in wheat","volume":"218","author":"Baranwal","year":"2022","journal-title":"Euphytica"},{"key":"ref_109","doi-asserted-by":"crossref","first-page":"101195","DOI":"10.1016\/j.xplc.2024.101195","article-title":"Genetic engineering, including genome editing, for enhancing broad-spectrum disease resistance in crops","volume":"10","author":"Han","year":"2025","journal-title":"Plant Commun."},{"key":"ref_110","doi-asserted-by":"crossref","unstructured":"Mourad, A.M.I., Ahmed, A.A.M., Baenziger, P.S., B\u00f6rner, A., and Sallam, A. (2024). Broad-spectrum resistance to fungal foliar diseases in wheat: Recent efforts and achievements. Front. Plant Sci., 15.","DOI":"10.3389\/fpls.2024.1516317"},{"key":"ref_111","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1007\/s00122-020-03657-2","article-title":"QTL mapping of adult plant and seedling resistance to leaf rust (Puccinia triticina Eriks.) in a multiparent advanced generation intercross (MAGIC) wheat population","volume":"134","author":"Rollar","year":"2021","journal-title":"Theor. Appl. Genet."},{"key":"ref_112","doi-asserted-by":"crossref","first-page":"117","DOI":"10.25174\/2582-2675\/2021\/112817","article-title":"Prospects of climate change effects on wheat diseases","volume":"13","author":"Prasad","year":"2021","journal-title":"J. Cereal Res."},{"key":"ref_113","doi-asserted-by":"crossref","first-page":"56","DOI":"10.1111\/tpj.14150","article-title":"Applying the latest advances in genomics and phenomics for trait discovery in polyploid wheat","volume":"97","author":"Borrill","year":"2019","journal-title":"Plant J."},{"key":"ref_114","doi-asserted-by":"crossref","first-page":"e14544","DOI":"10.1111\/ppl.14544","article-title":"Accelerating wheat improvement through trait characterization: Advances and perspectives","volume":"176","author":"Roychowdhury","year":"2024","journal-title":"Physiol. Plant."}],"container-title":["Plants"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2223-7747\/15\/14\/2131\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,7,10]],"date-time":"2026-07-10T10:14:22Z","timestamp":1783678462000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2223-7747\/15\/14\/2131"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,7,10]]},"references-count":114,"journal-issue":{"issue":"14","published-online":{"date-parts":[[2026,7]]}},"alternative-id":["plants15142131"],"URL":"https:\/\/doi.org\/10.3390\/plants15142131","relation":{},"ISSN":["2223-7747"],"issn-type":[{"value":"2223-7747","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,7,10]]}}}