Monitoring wheat leaf rust severity using machine learning techniques
Wheat leaf rust, caused by Puccinia triticina Eriks., is recognized as one of the most destructive diseases affecting wheat worldwide, including Iran, resulting in substantial losses in grain yield and quality. This research focused on evaluating the pathogenic factors of nine leaf rust isolates col...
Saved in:
| Published in: | Scientific reports Vol. 15; no. 1; p. 42951 |
|---|---|
| Main Authors: | , , , , , , , , , |
| Format: | Journal Article |
| Language: | English |
| Published: |
London
Nature Publishing Group UK
29.11.2025
|
| Subjects: | |
| ISSN: | 2045-2322, 2045-2322 |
| Online Access: | Get full text |
| Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
| Abstract | Wheat leaf rust, caused by
Puccinia triticina
Eriks., is recognized as one of the most destructive diseases affecting wheat worldwide, including Iran, resulting in substantial losses in grain yield and quality. This research focused on evaluating the pathogenic factors of nine leaf rust isolates collected from four different climates in Iran, using various differential genotypes. The assessment of leaf rust infection types was conducted on 49 durum and bread wheat genotypes, including susceptible control genotypes and 55 differential genotypes at the seedling stages. The results revealed a significant difference among wheat genotypes in their response to all isolates (
p
≤ 0.01). Notably, certain genotypes, such as the Italian landrace (P.S. No4), Shabrang, Chamran2, Mehregan, Shosh, and Gonbad, exhibited resistance to all isolates at the seedling stage, indicating the presence of seedling resistance genes. Additionally, we determined the virulence/avirulence patterns for various resistance genes in the differential genotypes by assessing their responses to different isolates and recording the infection types. The findings indicated that all isolates were virulent on the lines carrying the
Lr34
and
Lr37
genes, whereas none of the isolates displayed a virulence on the lines carrying the
Lr19
gene. This research provides valuable insights into the resistance patterns of wheat genotypes against leaf rust isolates in different climates in Iran, contributing to our understanding of the genetic basis of resistance and aiding in the development of effective strategies for disease management in wheat cultivation. The XGBoost (extreme gradient boosting) algorithm generated the most accurate predictions for the variables thousand grain weight and grain yield, while the MARS (multivariate adaptive regression spline) algorithm generated the most accurate predictions for the variables spike weight, number of grains per spike, and grain weight per spike. For each of these variables, GP (Gaussian process), MARS, and XGBoost achieved the lowest RMSE (root mean square error) values, indicating minimal prediction errors, and the highest R² values, signifying a strong correlation between the predicted and observed data. These prediction performances highlighted the robustness and accuracy of the GP, MARS and XGBoost algorithms in modeling wheat disease severity and its effects on yield outcomes. |
|---|---|
| AbstractList | Wheat leaf rust, caused by Puccinia triticina Eriks., is recognized as one of the most destructive diseases affecting wheat worldwide, including Iran, resulting in substantial losses in grain yield and quality. This research focused on evaluating the pathogenic factors of nine leaf rust isolates collected from four different climates in Iran, using various differential genotypes. The assessment of leaf rust infection types was conducted on 49 durum and bread wheat genotypes, including susceptible control genotypes and 55 differential genotypes at the seedling stages. The results revealed a significant difference among wheat genotypes in their response to all isolates (p ≤ 0.01). Notably, certain genotypes, such as the Italian landrace (P.S. No4), Shabrang, Chamran2, Mehregan, Shosh, and Gonbad, exhibited resistance to all isolates at the seedling stage, indicating the presence of seedling resistance genes. Additionally, we determined the virulence/avirulence patterns for various resistance genes in the differential genotypes by assessing their responses to different isolates and recording the infection types. The findings indicated that all isolates were virulent on the lines carrying the Lr34 and Lr37 genes, whereas none of the isolates displayed a virulence on the lines carrying the Lr19 gene. This research provides valuable insights into the resistance patterns of wheat genotypes against leaf rust isolates in different climates in Iran, contributing to our understanding of the genetic basis of resistance and aiding in the development of effective strategies for disease management in wheat cultivation. The XGBoost (extreme gradient boosting) algorithm generated the most accurate predictions for the variables thousand grain weight and grain yield, while the MARS (multivariate adaptive regression spline) algorithm generated the most accurate predictions for the variables spike weight, number of grains per spike, and grain weight per spike. For each of these variables, GP (Gaussian process), MARS, and XGBoost achieved the lowest RMSE (root mean square error) values, indicating minimal prediction errors, and the highest R² values, signifying a strong correlation between the predicted and observed data. These prediction performances highlighted the robustness and accuracy of the GP, MARS and XGBoost algorithms in modeling wheat disease severity and its effects on yield outcomes.Wheat leaf rust, caused by Puccinia triticina Eriks., is recognized as one of the most destructive diseases affecting wheat worldwide, including Iran, resulting in substantial losses in grain yield and quality. This research focused on evaluating the pathogenic factors of nine leaf rust isolates collected from four different climates in Iran, using various differential genotypes. The assessment of leaf rust infection types was conducted on 49 durum and bread wheat genotypes, including susceptible control genotypes and 55 differential genotypes at the seedling stages. The results revealed a significant difference among wheat genotypes in their response to all isolates (p ≤ 0.01). Notably, certain genotypes, such as the Italian landrace (P.S. No4), Shabrang, Chamran2, Mehregan, Shosh, and Gonbad, exhibited resistance to all isolates at the seedling stage, indicating the presence of seedling resistance genes. Additionally, we determined the virulence/avirulence patterns for various resistance genes in the differential genotypes by assessing their responses to different isolates and recording the infection types. The findings indicated that all isolates were virulent on the lines carrying the Lr34 and Lr37 genes, whereas none of the isolates displayed a virulence on the lines carrying the Lr19 gene. This research provides valuable insights into the resistance patterns of wheat genotypes against leaf rust isolates in different climates in Iran, contributing to our understanding of the genetic basis of resistance and aiding in the development of effective strategies for disease management in wheat cultivation. The XGBoost (extreme gradient boosting) algorithm generated the most accurate predictions for the variables thousand grain weight and grain yield, while the MARS (multivariate adaptive regression spline) algorithm generated the most accurate predictions for the variables spike weight, number of grains per spike, and grain weight per spike. For each of these variables, GP (Gaussian process), MARS, and XGBoost achieved the lowest RMSE (root mean square error) values, indicating minimal prediction errors, and the highest R² values, signifying a strong correlation between the predicted and observed data. These prediction performances highlighted the robustness and accuracy of the GP, MARS and XGBoost algorithms in modeling wheat disease severity and its effects on yield outcomes. Wheat leaf rust, caused by Puccinia triticina Eriks., is recognized as one of the most destructive diseases affecting wheat worldwide, including Iran, resulting in substantial losses in grain yield and quality. This research focused on evaluating the pathogenic factors of nine leaf rust isolates collected from four different climates in Iran, using various differential genotypes. The assessment of leaf rust infection types was conducted on 49 durum and bread wheat genotypes, including susceptible control genotypes and 55 differential genotypes at the seedling stages. The results revealed a significant difference among wheat genotypes in their response to all isolates ( p ≤ 0.01). Notably, certain genotypes, such as the Italian landrace (P.S. No4), Shabrang, Chamran2, Mehregan, Shosh, and Gonbad, exhibited resistance to all isolates at the seedling stage, indicating the presence of seedling resistance genes. Additionally, we determined the virulence/avirulence patterns for various resistance genes in the differential genotypes by assessing their responses to different isolates and recording the infection types. The findings indicated that all isolates were virulent on the lines carrying the Lr34 and Lr37 genes, whereas none of the isolates displayed a virulence on the lines carrying the Lr19 gene. This research provides valuable insights into the resistance patterns of wheat genotypes against leaf rust isolates in different climates in Iran, contributing to our understanding of the genetic basis of resistance and aiding in the development of effective strategies for disease management in wheat cultivation. The XGBoost (extreme gradient boosting) algorithm generated the most accurate predictions for the variables thousand grain weight and grain yield, while the MARS (multivariate adaptive regression spline) algorithm generated the most accurate predictions for the variables spike weight, number of grains per spike, and grain weight per spike. For each of these variables, GP (Gaussian process), MARS, and XGBoost achieved the lowest RMSE (root mean square error) values, indicating minimal prediction errors, and the highest R² values, signifying a strong correlation between the predicted and observed data. These prediction performances highlighted the robustness and accuracy of the GP, MARS and XGBoost algorithms in modeling wheat disease severity and its effects on yield outcomes. Wheat leaf rust, caused by Puccinia triticina Eriks., is recognized as one of the most destructive diseases affecting wheat worldwide, including Iran, resulting in substantial losses in grain yield and quality. This research focused on evaluating the pathogenic factors of nine leaf rust isolates collected from four different climates in Iran, using various differential genotypes. The assessment of leaf rust infection types was conducted on 49 durum and bread wheat genotypes, including susceptible control genotypes and 55 differential genotypes at the seedling stages. The results revealed a significant difference among wheat genotypes in their response to all isolates (p ≤ 0.01). Notably, certain genotypes, such as the Italian landrace (P.S. No4), Shabrang, Chamran2, Mehregan, Shosh, and Gonbad, exhibited resistance to all isolates at the seedling stage, indicating the presence of seedling resistance genes. Additionally, we determined the virulence/avirulence patterns for various resistance genes in the differential genotypes by assessing their responses to different isolates and recording the infection types. The findings indicated that all isolates were virulent on the lines carrying the Lr34 and Lr37 genes, whereas none of the isolates displayed a virulence on the lines carrying the Lr19 gene. This research provides valuable insights into the resistance patterns of wheat genotypes against leaf rust isolates in different climates in Iran, contributing to our understanding of the genetic basis of resistance and aiding in the development of effective strategies for disease management in wheat cultivation. The XGBoost (extreme gradient boosting) algorithm generated the most accurate predictions for the variables thousand grain weight and grain yield, while the MARS (multivariate adaptive regression spline) algorithm generated the most accurate predictions for the variables spike weight, number of grains per spike, and grain weight per spike. For each of these variables, GP (Gaussian process), MARS, and XGBoost achieved the lowest RMSE (root mean square error) values, indicating minimal prediction errors, and the highest R² values, signifying a strong correlation between the predicted and observed data. These prediction performances highlighted the robustness and accuracy of the GP, MARS and XGBoost algorithms in modeling wheat disease severity and its effects on yield outcomes. |
| Author | Sarhangi, Mohsen Türkoğlu, Aras Bakhshi, Tayebeh Sarbarzeh, Mostafa Aghaee Mehrabi, Rahim Ahmadi, Farajollah Shahriari Haliloğlu, Kamil Demirel, Fatih Bocianowski, Jan Benlioğlu, Berk |
| Author_xml | – sequence: 1 givenname: Tayebeh surname: Bakhshi fullname: Bakhshi, Tayebeh organization: Department of Crop Biotechnology and Breeding, Faculty of Agriculture, Ferdowsi University of Mashhad – sequence: 2 givenname: Rahim surname: Mehrabi fullname: Mehrabi, Rahim organization: Department of Biotechnology, Isfahan University of Technology – sequence: 3 givenname: Mostafa Aghaee surname: Sarbarzeh fullname: Sarbarzeh, Mostafa Aghaee email: maghaee@yahoo.com organization: Seed and Plant Improvement Institute, Agricultural Research, Education and Extension Organization (AREEO) – sequence: 4 givenname: Aras surname: Türkoğlu fullname: Türkoğlu, Aras email: aras.turkoglu@erbakan.edu.tr organization: Department of Field Crops, Faculty of Agriculture, Necmettin Erbakan University – sequence: 5 givenname: Fatih surname: Demirel fullname: Demirel, Fatih organization: Department of Agricultural Biotechnology, Faculty of Agriculture, Igdır University – sequence: 6 givenname: Kamil surname: Haliloğlu fullname: Haliloğlu, Kamil organization: Department of Biology, Faculty of Science, Gazi University – sequence: 7 givenname: Berk surname: Benlioğlu fullname: Benlioğlu, Berk organization: Department of Field Crops, Faculty of Agriculture, Ankara University – sequence: 8 givenname: Mohsen surname: Sarhangi fullname: Sarhangi, Mohsen organization: Seed and Plant Improvement Institute, Agricultural Research, Education and Extension Organization (AREEO) – sequence: 9 givenname: Farajollah Shahriari surname: Ahmadi fullname: Ahmadi, Farajollah Shahriari organization: Department of Crop Biotechnology and Breeding, Faculty of Agriculture, Ferdowsi University of Mashhad – sequence: 10 givenname: Jan surname: Bocianowski fullname: Bocianowski, Jan organization: Department of Mathematical and Statistical Methods, Poznan University of Life Sciences |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/41318653$$D View this record in MEDLINE/PubMed |
| BookMark | eNpNkMlOwzAQhi0EoqX0BTigHLkEbI8dO0dUlUUq4gJnK8uEpkqcYCegvj0OLRJzme3TLP8FObWdRUKuGL1lFPSdF0ymOqZcxlwIqmJ9QuacipAC56f_4hlZer-jwSRPBUvPyUwwYDqRMCfrl87WQ-dq-xF9bzEbogazKnKjHyKPX-jqYR-Nfmq3WbGtLU6As1NhwGJr688R_SU5q7LG4_LoF-T9Yf22eoo3r4_Pq_tN3DMhdFwkokpTAKQFUlQllRUvFOO5KmgJQKEKBc3TSnKQuawgVUoFJMmlLrMkhwW5OcztXTftHUxb-wKbJrPYjd4AV0miVaJkQK-P6Ji3WJre1W3m9ubv9QDAAfD99D06s-tGZ8P5hlEzaWwOGpugsfnV2Gj4AeXrbb8 |
| ContentType | Journal Article |
| Copyright | The Author(s) 2025 2025. The Author(s). |
| Copyright_xml | – notice: The Author(s) 2025 – notice: 2025. The Author(s). |
| DBID | C6C CGR CUY CVF ECM EIF NPM 7X8 |
| DOI | 10.1038/s41598-025-24407-8 |
| DatabaseName | Springer Nature OA Free Journals Medline MEDLINE MEDLINE (Ovid) MEDLINE MEDLINE PubMed MEDLINE - Academic |
| DatabaseTitle | MEDLINE Medline Complete MEDLINE with Full Text PubMed MEDLINE (Ovid) MEDLINE - Academic |
| DatabaseTitleList | MEDLINE - Academic MEDLINE |
| Database_xml | – sequence: 1 dbid: NPM name: PubMed url: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed sourceTypes: Index Database – sequence: 2 dbid: 7X8 name: MEDLINE - Academic url: https://search.proquest.com/medline sourceTypes: Aggregation Database |
| DeliveryMethod | fulltext_linktorsrc |
| Discipline | Biology |
| EISSN | 2045-2322 |
| ExternalDocumentID | 41318653 10_1038_s41598_025_24407_8 |
| Genre | Journal Article |
| GeographicLocations | Iran |
| GeographicLocations_xml | – name: Iran |
| GroupedDBID | 0R~ 4.4 53G 5VS 7X7 88E 88I 8FE 8FH 8FI 8FJ AAFWJ AAJSJ AAKDD AASML ABDBF ABUWG ACGFS ACUHS ADBBV ADRAZ AENEX AEUYN AFFHD AFKRA AFPKN AGGLG ALMA_UNASSIGNED_HOLDINGS AOIJS AZQEC BAWUL BBNVY BCNDV BENPR BHPHI BPHCQ BVXVI C6C CCPQU DIK DWQXO EBD EBLON EBS ESX FYUFA GNUQQ GROUPED_DOAJ GX1 HCIFZ HH5 HMCUK HYE KQ8 LK8 M1P M2P M7P M~E NAO OK1 PHGZM PHGZT PIMPY PJZUB PPXIY PQGLB PQQKQ PROAC PSQYO RNT RNTTT RPM SNYQT UKHRP CGR CUY CVF ECM EIF NPM 7X8 |
| ID | FETCH-LOGICAL-p1448-c64f9933e0ce0e7d05f2c712b7c0d3303f5f2829f5235b5f39777f2c6b58da6b3 |
| ISSN | 2045-2322 |
| IngestDate | Mon Dec 01 00:09:59 EST 2025 Wed Dec 10 14:04:49 EST 2025 Wed Dec 10 10:37:25 EST 2025 |
| IsDoiOpenAccess | true |
| IsOpenAccess | true |
| IsPeerReviewed | true |
| IsScholarly | true |
| Issue | 1 |
| Keywords | Leaf rust Resistance gene Wheat Virulence factor |
| Language | English |
| License | 2025. The Author(s). |
| LinkModel | OpenURL |
| MergedId | FETCHMERGED-LOGICAL-p1448-c64f9933e0ce0e7d05f2c712b7c0d3303f5f2829f5235b5f39777f2c6b58da6b3 |
| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 |
| OpenAccessLink | http://dx.doi.org/10.1038/s41598-025-24407-8 |
| PMID | 41318653 |
| PQID | 3276687675 |
| PQPubID | 23479 |
| ParticipantIDs | proquest_miscellaneous_3276687675 pubmed_primary_41318653 springer_journals_10_1038_s41598_025_24407_8 |
| PublicationCentury | 2000 |
| PublicationDate | 20251129 2025-Nov-29 |
| PublicationDateYYYYMMDD | 2025-11-29 |
| PublicationDate_xml | – month: 11 year: 2025 text: 20251129 day: 29 |
| PublicationDecade | 2020 |
| PublicationPlace | London |
| PublicationPlace_xml | – name: London – name: England |
| PublicationTitle | Scientific reports |
| PublicationTitleAbbrev | Sci Rep |
| PublicationTitleAlternate | Sci Rep |
| PublicationYear | 2025 |
| Publisher | Nature Publishing Group UK |
| Publisher_xml | – name: Nature Publishing Group UK |
| SSID | ssj0000529419 |
| Score | 2.464883 |
| Snippet | Wheat leaf rust, caused by
Puccinia triticina
Eriks., is recognized as one of the most destructive diseases affecting wheat worldwide, including Iran,... Wheat leaf rust, caused by Puccinia triticina Eriks., is recognized as one of the most destructive diseases affecting wheat worldwide, including Iran,... |
| SourceID | proquest pubmed springer |
| SourceType | Aggregation Database Index Database Publisher |
| StartPage | 42951 |
| SubjectTerms | 631/114 631/208 631/326 631/449 Basidiomycota - pathogenicity Disease Resistance - genetics Genotype Humanities and Social Sciences Iran Machine Learning multidisciplinary Plant Diseases - genetics Plant Diseases - microbiology Plant Leaves - genetics Plant Leaves - microbiology Puccinia - pathogenicity Science Science (multidisciplinary) Seedlings - genetics Seedlings - microbiology Triticum - genetics Triticum - microbiology |
| Title | Monitoring wheat leaf rust severity using machine learning techniques |
| URI | https://link.springer.com/article/10.1038/s41598-025-24407-8 https://www.ncbi.nlm.nih.gov/pubmed/41318653 https://www.proquest.com/docview/3276687675 |
| Volume | 15 |
| hasFullText | 1 |
| inHoldings | 1 |
| isFullTextHit | |
| isPrint | |
| journalDatabaseRights | – providerCode: PRVAON databaseName: DOAJ Directory of Open Access Journals customDbUrl: eissn: 2045-2322 dateEnd: 99991231 omitProxy: false ssIdentifier: ssj0000529419 issn: 2045-2322 databaseCode: DOA dateStart: 20110101 isFulltext: true titleUrlDefault: https://www.doaj.org/ providerName: Directory of Open Access Journals – providerCode: PRVHPJ databaseName: ROAD: Directory of Open Access Scholarly Resources customDbUrl: eissn: 2045-2322 dateEnd: 99991231 omitProxy: false ssIdentifier: ssj0000529419 issn: 2045-2322 databaseCode: M~E dateStart: 20110101 isFulltext: true titleUrlDefault: https://road.issn.org providerName: ISSN International Centre – providerCode: PRVPQU databaseName: Biological Science Database (ProQuest) customDbUrl: eissn: 2045-2322 dateEnd: 99991231 omitProxy: false ssIdentifier: ssj0000529419 issn: 2045-2322 databaseCode: M7P dateStart: 20110101 isFulltext: true titleUrlDefault: http://search.proquest.com/biologicalscijournals providerName: ProQuest – providerCode: PRVPQU databaseName: Health & Medical Collection (ProQuest) customDbUrl: eissn: 2045-2322 dateEnd: 99991231 omitProxy: false ssIdentifier: ssj0000529419 issn: 2045-2322 databaseCode: 7X7 dateStart: 20110101 isFulltext: true titleUrlDefault: https://search.proquest.com/healthcomplete providerName: ProQuest – providerCode: PRVPQU databaseName: ProQuest Central (subscription) customDbUrl: eissn: 2045-2322 dateEnd: 99991231 omitProxy: false ssIdentifier: ssj0000529419 issn: 2045-2322 databaseCode: BENPR dateStart: 20110101 isFulltext: true titleUrlDefault: https://www.proquest.com/central providerName: ProQuest – providerCode: PRVPQU databaseName: Publicly Available Content Database customDbUrl: eissn: 2045-2322 dateEnd: 99991231 omitProxy: false ssIdentifier: ssj0000529419 issn: 2045-2322 databaseCode: PIMPY dateStart: 20110101 isFulltext: true titleUrlDefault: http://search.proquest.com/publiccontent providerName: ProQuest – providerCode: PRVPQU databaseName: Science Database customDbUrl: eissn: 2045-2322 dateEnd: 99991231 omitProxy: false ssIdentifier: ssj0000529419 issn: 2045-2322 databaseCode: M2P dateStart: 20110101 isFulltext: true titleUrlDefault: https://search.proquest.com/sciencejournals providerName: ProQuest |
| link | http://cvtisr.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwtV3db9owELcobFNfpn2PfaBM2lsWLSRx7Dy2FdX2AEIVk9hTZCd2qVoCIkDb_fU7n5PQjk3aHvZyQkmwJf9-Pp_PvjtCPjIRCKoSmEg0ibxIR9oTkaRezClVYaJhzfWx2AQbjfh0moxbrW0dC7O9YkXBb26S5X-FGp4B2CZ09h_gbhqFB_AbQAcJsIP8K-DtLMVrdddG05rCENo1oRUurILKFKtzN-ghmONFSlVXjjh3m4Su5V2bFac_XimqTxh27s_LWYlVgV3Y-QNQjW95qGYrIfHNmZhdzBtHDh5v_FDozBkuwDTVwj06nwnVEGxizu6PT1aXC2PoJqdXG9RfK3HPQxFQE6pXuTEUajKT8t4D0-2-2qV79LI6FFZIm4N2T7vbXO4l2BwmLhA6AtvEZ4js-g6yyzlCC8tzn8c2FfEvObXrVwekEzBorE0646_D8ffGO2fOP6N-UkVZQb-f93s9JI_qdn63Pdk7WkeLZfKEPK62Gs6RpchT0lLFM_LQFh-9fU4GO6I4SBTHEMUxRHFqojhIFKciilMTxdkR5QX5djqYnHzxqqIa3hL2ztzL4kiDTRoqP1O-YrlPdZCxfiBZ5uchGDQaHvAg0TQIqaTabBAYfBJLynMRy_AlaReLQr0mjpBhnkkV-lr1I5n5AuxFqZI8y-Hvvoy65EM9KikoLXMSJQq12JRpGLA45iaPUJe8ssOVLm12lbQe0y75VI9fWk2vMsUrEyFPLRopoJEiGil_88eG3pLDHSvfkfZ6tVHvyYNsu74oVz1ywKYMJe-RzvFgND7roWMG5DAYG8lAWn78BOeRes0 |
| linkProvider | ProQuest |
| openUrl | ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=Monitoring+wheat+leaf+rust+severity+using+machine+learning+techniques&rft.jtitle=Scientific+reports&rft.au=Bakhshi%2C+Tayebeh&rft.au=Mehrabi%2C+Rahim&rft.au=Sarbarzeh%2C+Mostafa+Aghaee&rft.au=T%C3%BCrko%C4%9Flu%2C+Aras&rft.date=2025-11-29&rft.eissn=2045-2322&rft.volume=15&rft.issue=1&rft.spage=42951&rft_id=info:doi/10.1038%2Fs41598-025-24407-8&rft_id=info%3Apmid%2F41318653&rft.externalDocID=41318653 |
| thumbnail_l | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=2045-2322&client=summon |
| thumbnail_m | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=2045-2322&client=summon |
| thumbnail_s | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=2045-2322&client=summon |