{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,5]],"date-time":"2026-10-05T09:55:17Z","timestamp":1791194117607,"version":"4.1.0"},"reference-count":57,"publisher":"MDPI AG","issue":"19","license":[{"start":{"date-parts":[[2026,10,3]],"date-time":"2026-10-03T00:00:00Z","timestamp":1790985600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100012166","name":"National Key R&D Program of China","doi-asserted-by":"publisher","award":["2023YFD1400400"],"award-info":[{"award-number":["2023YFD1400400"]}],"id":[{"id":"10.13039\/501100012166","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Guangdong S&T Program","award":["2026B0202180004"],"award-info":[{"award-number":["2026B0202180004"]}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["32272490"],"award-info":[{"award-number":["32272490"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"award":["32272490"],"award-info":[{"award-number":["32272490"]}],"id":[{"id":"https:\/\/ror.org\/01h0zpd94","id-type":"ROR","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100009997","name":"Earmarked Fund for Modern Agro-industry Technology Research System","doi-asserted-by":"publisher","award":["nycytx-001"],"award-info":[{"award-number":["nycytx-001"]}],"id":[{"id":"10.13039\/501100009997","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Shaanxi Innovation Team Project","award":["2024RS-CXTD-73"],"award-info":[{"award-number":["2024RS-CXTD-73"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Plants"],"abstract":"<jats:p>The rice root-knot nematode (Meloidogyne graminicola) is a major pathogen of rice. The resistance gene MG1 in the cultivar Zhonghua 11 (ZH11) confers effective resistance against this pathogen. To date, only one virulent population overcoming ZH11 has been reported, from Cambodia, but whether it overcomes MG1 remains unknown. Here, we collected and identified 31 M. graminicola populations from southern China. Ten of these populations were tested on ZH11. Two of the 10 tested populations were virulent, GZSD1 from Guangdong and HUNSD28 from Hunan, with reproduction factors (Rf) of 3.11 and 1.67, respectively. GZSD1 was also reproduced on NIL-MG1, a near-isogenic line developed by introgressing MG1 into the susceptible variety Huazhan, with an Rf of 2.78. Moreover, GZSD1 showed no significant differences in developmental progression or parasitic ability, either from an avirulent population HAINSD24 on the susceptible cultivar Nipponbare or between the resistant line ZH11 and the susceptible cultivar Nipponbare, suggesting that GZSD1 can overcome MG1-mediated resistance without a significant fitness cost under the tested conditions. Population genetic analysis based on mtCOI sequences revealed high haplotype diversity and low genetic differentiation with weak geographic structuring among the sampled populations. A signal of population expansion was detected. These findings identify the first virulent M. graminicola population overcoming MG1-mediated resistance in rice and suggest that virulence may have the potential to spread. This work highlights the threat to MG1-based resistance and calls for monitoring and mechanistic studies to support sustainable rice breeding.<\/jats:p>","DOI":"10.3390\/plants15193031","type":"journal-article","created":{"date-parts":[[2026,10,5]],"date-time":"2026-10-05T08:57:18Z","timestamp":1791190638000},"page":"3031","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Discovery of a Virulent Population of Meloidogyne graminicola Overcoming the Rice Resistance Gene MG1 and Population Genetic Analysis Based on mtCOI Sequences"],"prefix":"10.3390","volume":"15","author":[{"ORCID":"https:\/\/orcid.org\/0009-0009-6546-7449","authenticated-orcid":false,"given":"Ao","family":"Xu","sequence":"first","affiliation":[{"name":"College of Plant Protection, South China Agricultural University, Guangzhou 510642, China"}],"role":[{"vocabulary":"crossref","role":"author"},{"role":"methodology","vocabulary":"credit"},{"role":"investigation","vocabulary":"credit"},{"role":"writing-original-draft","vocabulary":"credit"}]},{"given":"Borong","family":"Lin","sequence":"additional","affiliation":[{"name":"College of Plant Protection, South China Agricultural University, Guangzhou 510642, China"}],"role":[{"vocabulary":"crossref","role":"author"},{"role":"methodology","vocabulary":"credit"},{"role":"investigation","vocabulary":"credit"},{"role":"writing-original-draft","vocabulary":"credit"}]},{"given":"Qiuling","family":"Huang","sequence":"additional","affiliation":[{"name":"College of Plant Protection, South China Agricultural University, Guangzhou 510642, China"}],"role":[{"vocabulary":"crossref","role":"author"},{"role":"investigation","vocabulary":"credit"}]},{"given":"Yuqing","family":"Cao","sequence":"additional","affiliation":[{"name":"College of Plant Protection, South China Agricultural University, Guangzhou 510642, China"}],"role":[{"vocabulary":"crossref","role":"author"},{"role":"investigation","vocabulary":"credit"}]},{"given":"Yaya","family":"Fan","sequence":"additional","affiliation":[{"name":"College of Plant Protection, South China Agricultural University, Guangzhou 510642, China"}],"role":[{"vocabulary":"crossref","role":"author"},{"role":"investigation","vocabulary":"credit"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6343-7355","authenticated-orcid":false,"given":"Zhong","family":"Ding","sequence":"additional","affiliation":[{"name":"College of Plant Protection, Hunan Agricultural University, Changsha 410128, China"}],"role":[{"vocabulary":"crossref","role":"author"},{"role":"resources","vocabulary":"credit"}]},{"given":"Kan","family":"Zhuo","sequence":"additional","affiliation":[{"name":"College of Plant Protection, South China Agricultural University, Guangzhou 510642, China"}],"role":[{"vocabulary":"crossref","role":"author"},{"role":"conceptualization","vocabulary":"credit"},{"role":"writing-review-editing","vocabulary":"credit"},{"role":"funding-acquisition","vocabulary":"credit"},{"role":"resources","vocabulary":"credit"}]}],"member":"1968","published-online":{"date-parts":[[2026,10,3]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"186","DOI":"10.1016\/j.rsci.2023.03.004","article-title":"Adoption of improved rice varieties in the global south: A review","volume":"30","author":"Checco","year":"2023","journal-title":"Rice Sci."},{"key":"ref_2","first-page":"221","article-title":"Characterization of isolates of Meloidogyne from rice-wheat production fields in Nepal","volume":"39","author":"Pokharel","year":"2007","journal-title":"J. Nematol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"177","DOI":"10.1007\/BF03045567","article-title":"Nature of root-knot (Meloidogyne graminicola) resistance in rice (Oryza sativa)","volume":"83","author":"Jena","year":"1976","journal-title":"Proc. Indian Acad. Sci."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"887","DOI":"10.1111\/j.1469-8137.2012.04311.x","article-title":"Transcriptional reprogramming by root knot and migratory nematode infection in rice","volume":"196","author":"Kyndt","year":"2012","journal-title":"New Phytol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1111\/mpp.12394","article-title":"Meloidogyne graminicola: A major threat to rice agriculture","volume":"18","author":"Mantelin","year":"2017","journal-title":"Mol. Plant Pathol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"2070","DOI":"10.1094\/PDIS-08-22-1796-RE","article-title":"Meloidogyne graminicola population structure in China suggests a south-to-north expansion","volume":"107","author":"Liu","year":"2023","journal-title":"Plant Dis."},{"key":"ref_7","first-page":"33","article-title":"Effect of planting and irrigation practices on nematode reproduction, root galling, plant growth and yield of two Asian lowland rice varieties infected by the rice root-knot nematode Meloidogyne graminicola","volume":"24","author":"Win","year":"2016","journal-title":"Russ. J. Nematol."},{"key":"ref_8","first-page":"274","article-title":"Evaluation of protocol for assessing the reaction of rice and wheat Germplasm to infection by Meloidogyne graminicola","volume":"44","author":"Pokharel","year":"2012","journal-title":"J. Nematol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"745","DOI":"10.1163\/156854199508775","article-title":"Resistance to the rice nematodes Heterodera sacchari, Meloidogyne graminicola and M. incognita in Oryza glaberrima and O. glaberrima \u00d7 O. sativa interspecific hybrids","volume":"1","author":"Plowright","year":"1999","journal-title":"Nematology"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"395","DOI":"10.1163\/156854199508397","article-title":"Resistance to rice root-knot nematode Meloidogyne graminicola identified in Oryza longistaminata and O. glaberrima","volume":"1","author":"Soriano","year":"1999","journal-title":"Nematology"},{"key":"ref_11","first-page":"1191","article-title":"genome-wide association study of a global rice panel reveals resistance in Oryza sativa to root-knot nematodes","volume":"37","author":"Dimkpa","year":"2015","journal-title":"J. Exp. Bot."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"621","DOI":"10.1016\/S2095-3119(17)61802-1","article-title":"Evaluation of Chinese rice varieties resistant to the root-knot nematode Meloidogyne graminicola","volume":"17","author":"Zhan","year":"2018","journal-title":"J. Integr. Agric."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"3081","DOI":"10.1016\/j.jia.2022.11.008","article-title":"Resistance analysis of the rice variety Huaidao 5 against root-knot nematode Meloidogyne graminicola","volume":"22","author":"Feng","year":"2023","journal-title":"J. Integr. Agric."},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Galeng-Lawilao, J., Kumar, A., and De Waele, D. (2018). QTL mapping for resistance to and tolerance for the rice root-knot nematode, Meloidogyne graminicola. BMC Genet., 19.","DOI":"10.1186\/s12863-018-0656-1"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"117","DOI":"10.1007\/s10681-019-2427-0","article-title":"QTL-seq reveals a major root-knot nematode resistance locus on chromosome 11 in rice (Oryza sativa L.)","volume":"215","author":"Lahari","year":"2019","journal-title":"Euphytica"},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"Nguyen, H.T., Mantelin, S., Ha, C.V., Lorieux, M., Jones, J.T., Mai, C.D., and Bellafiore, S. (2022). Insights into the genetics of the Zhonghua 11 resistance to Meloidogyne graminicola and its molecular determinism in rice. Front. Plant Sci., 13.","DOI":"10.3389\/fpls.2022.854961"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"3354","DOI":"10.1038\/s41467-023-39080-6","article-title":"MG1 interacts with a protease inhibitor and confers resistance to rice root-knot nematode","volume":"14","author":"Wang","year":"2023","journal-title":"Nat. Commun."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"391","DOI":"10.1007\/s13313-023-00926-8","article-title":"Identification and characterization of a virulent population of Meloidogyne graminicola","volume":"52","author":"Nguyen","year":"2023","journal-title":"Austral. Plant Pathol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"627","DOI":"10.1163\/15685411-bja10065","article-title":"Integrative taxonomy of Meloidogyne graminicola populations with different esterase phenotypes parasitising rice in Brazil","volume":"23","author":"Soares","year":"2021","journal-title":"Nematology"},{"key":"ref_20","first-page":"228","article-title":"Meloidogyne graminicola (Heteroderidae) a new species of root-knot nematode from grass","volume":"32","author":"Golden","year":"1965","journal-title":"Proc. Helminthol. Soc. Wash."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"275","DOI":"10.1146\/annurev.py.09.090171.001423","article-title":"Current status of the gene-for-gene concept","volume":"9","author":"Flor","year":"1971","journal-title":"Annu. Rev. Phytopathol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"282","DOI":"10.1038\/sj.hdy.6800794","article-title":"Genetic variability and adaptive evolution in parthenogenetic root-knot nematodes","volume":"96","year":"2006","journal-title":"Heredity"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"81","DOI":"10.1046\/j.1365-2540.2000.00633.x","article-title":"Virulence and molecular diversity of parthenogenetic root-knot nematodes, Meloidogyne spp.","volume":"84","author":"Semblat","year":"2000","journal-title":"Heredity"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"137","DOI":"10.1094\/PDIS-05-21-0902-RE","article-title":"Identification of four populations of Meloidogyne incognita in Georgia, United States, capable of parasitizing tomato-bearing Mi-1.2 gene","volume":"106","author":"Hajihassani","year":"2022","journal-title":"Plant Dis."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"271","DOI":"10.1094\/PDIS.2001.85.3.271","article-title":"A population of Meloidogyne javanica in Spain virulent to the Mi resistance gene in tomato","volume":"85","author":"Ornat","year":"2001","journal-title":"Plant Dis."},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"Montarry, J., Hamelin, F.M., Glais, I., Corbi\u00e8re, R., and Andrivon, D. (2010). Fitness costs associated with unnecessary virulence factors and life history traits: Evolutionary insights from the potato late blight pathogen Phytophthora infestans. BMC Evol. Biol., 10.","DOI":"10.1186\/1471-2148-10-283"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"107","DOI":"10.1007\/s10658-005-3479-7","article-title":"Durability of resistance and cost of virulence","volume":"114","author":"Pietravalle","year":"2006","journal-title":"Eur. J. Plant Pathol."},{"key":"ref_28","doi-asserted-by":"crossref","unstructured":"Blundell, A.C., Shigekane-Kraft, E., Janakowski, S., Sobczak, M., Dai, D., Zhang, Y., Shakya, P., Lin, C.-J., Williamson, V.M., and Siddique, S. (2026). Resistance breaking root-knot nematodes carry a fitness cost associated with defective feeding site development. PLoS Pathog., 22.","DOI":"10.64898\/2026.02.17.704924"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1111\/ppa.12147","article-title":"Spontaneous loss of Yr2 avirulence in two lineages of Puccinia striiformis did not affect pathogen fitness","volume":"62","author":"Justesen","year":"2013","journal-title":"Plant Pathol."},{"key":"ref_30","first-page":"457","article-title":"Fitness of virulent Meloidogyne incognita isolates on susceptible and resistant cowpea","volume":"37","author":"Petrillo","year":"2005","journal-title":"J. Nematol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"679","DOI":"10.1186\/BF03500872","article-title":"Lack of correlation between (a)virulence and phylogenetic relationships in root-knot nematodes (Meloidogyne spp.)","volume":"33","author":"Semblat","year":"2001","journal-title":"Genet. Sel. Evol."},{"key":"ref_32","doi-asserted-by":"crossref","unstructured":"Jain, A., Li, T., Wainer, J., Edwards, J., Rodoni, B.C., and Sawbridge, T.I. (2025). High-Throughput Sequencing Enables Rapid Analyses of Nematode Mitochondrial Genomes from an Environmental Sample. Pathogens, 14.","DOI":"10.3390\/pathogens14030234"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"330","DOI":"10.1111\/epp.12666","article-title":"Pest risk analysis of rice root-knot nematode (Meloidogyne graminicola) for the Italian territory","volume":"50","author":"Torrini","year":"2020","journal-title":"EPPO Bull."},{"key":"ref_34","first-page":"225","article-title":"The rice root-knot nematode, Meloidogyne graminicola, on deep water rice (Oryza sativa subsp. indica)","volume":"5","author":"Bridge","year":"1982","journal-title":"Rev. N\u00e9matol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"1015","DOI":"10.1163\/15685411-bja10008","article-title":"Arabidopsis thaliana as a model plant to study host-Meloidogyne graminicola interactions","volume":"22","author":"Huang","year":"2020","journal-title":"Nematology"},{"key":"ref_36","doi-asserted-by":"crossref","unstructured":"Tao, Y., Xu, C., Yuan, C., Wang, H., Lin, B., Zhuo, K., and Liao, J. (2017). Meloidogyne aberrans sp. nov. (Nematoda: Meloidogynidae), a new root-knot nematode parasitizing kiwifruit in China. PLoS ONE, 12.","DOI":"10.1371\/journal.pone.0182627"},{"key":"ref_37","unstructured":"Barker, K.R., Carter, C.C., and Sasser, J.N. (1985). Identification of Meloidogyne species on the basis of differential host test and perineal-pattern morphology. An Advanced Treatise on Meloidogyne, Volume II Methodology, North Carolina State University."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"455","DOI":"10.1163\/156854106778493420","article-title":"Phylogenetic analysis of Tylenchida Thorne, 1949 as inferred from D2 and D3 expansion fragments of the 28S rRNA gene sequences","volume":"8","author":"Subbotin","year":"2006","journal-title":"Nematology"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"153","DOI":"10.1163\/156854100509042","article-title":"Identification of cyst forming nematodes of the genus Heterodera (Nematoda: Heteroderidae) based on the ribosomal DNA RFLP","volume":"2","author":"Subbotin","year":"2000","journal-title":"Nematology"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"819","DOI":"10.1007\/s00239-005-0102-7","article-title":"The mitochondrial genome of Xiphinema americanum sensu stricto (Nematoda: Enoplea): Considerable economization in the length and structural features of encoded genes","volume":"61","author":"He","year":"2005","journal-title":"J. Mol. Evol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"99","DOI":"10.1163\/156854102765216731","article-title":"Molecular identification of cyst-forming nematodes (Heteroderidae) from Iran and a phylogeny based on the ITS sequences of rDNA","volume":"5","author":"Subbotin","year":"2003","journal-title":"Nematology"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"39","DOI":"10.11646\/zootaxa.2509.1.3","article-title":"Morphological and molecular characterization of Aphelenchoides fujianensis n. sp. (Nematoda: Aphelenchoididae) from Pinus massoniana in China","volume":"2509","author":"Zhuo","year":"2010","journal-title":"Zootaxa"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"1093","DOI":"10.1094\/PHYTO.2003.93.9.1093","article-title":"A new root-knot nematode, Meloidogyne baetica n. sp. (Nematoda: Heteroderidae), parasitizing wild olive in Southern Spain","volume":"93","author":"Castillo","year":"2003","journal-title":"Phytopathology"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"606","DOI":"10.1111\/j.1365-3059.2008.01991.x","article-title":"A new root-knot nematode, Meloidogyne silvestris n. sp. (Nematoda: Meloidogynidae), parasitizing European holly in northern Spain","volume":"58","author":"Castillo","year":"2009","journal-title":"Plant Pathol."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"97","DOI":"10.1007\/s10658-014-0446-1","article-title":"Comparison of two short DNA barcoding loci (COI and COII) and two longer ribosomal DNA genes (SSU & LSU rRNA) for specimen identification among quarantine root-knot nematodes (Meloidogyne spp.) and their close relatives","volume":"140","author":"Kiewnick","year":"2014","journal-title":"Eur. J. Plant Pathol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"540","DOI":"10.1093\/oxfordjournals.molbev.a026334","article-title":"Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis","volume":"17","author":"Castresana","year":"2000","journal-title":"Mol. Biol. Evol."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"587","DOI":"10.1038\/nmeth.4285","article-title":"ModelFinder: Fast model selection for accurate phylogenetic estimates","volume":"14","author":"Kalyaanamoorthy","year":"2017","journal-title":"Nat. Methods"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"539","DOI":"10.1093\/sysbio\/sys029","article-title":"MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space","volume":"61","author":"Ronquist","year":"2012","journal-title":"Syst. Biol."},{"key":"ref_49","first-page":"357","article-title":"TreeView: An application to display phylogenetic trees on personal computers","volume":"12","author":"Page","year":"1996","journal-title":"Comput. Appl. Biosci."},{"key":"ref_50","first-page":"1","article-title":"Major characteristics of the relation between nematodes and plants","volume":"66","author":"Oostenbrink","year":"1966","journal-title":"Meded. Landbouwhogesch."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"3022","DOI":"10.1093\/molbev\/msab120","article-title":"MEGA11: Molecular evolutionary genetics analysis version 11","volume":"38","author":"Tamura","year":"2021","journal-title":"Mol. Biol. Evol."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"3299","DOI":"10.1093\/molbev\/msx248","article-title":"DnaSP 6: DNA sequence polymorphism analysis of large data sets","volume":"34","author":"Rozas","year":"2017","journal-title":"Mol. Biol. Evol."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"1110","DOI":"10.1111\/2041-210X.12410","article-title":"POPART: Full-feature software for haplotype network construction","volume":"6","author":"Leigh","year":"2015","journal-title":"Methods Ecol. Evol."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"564","DOI":"10.1111\/j.1755-0998.2010.02847.x","article-title":"Arlequin suite ver. 3.5: A new series of programs to perform population genetics analyses under Linux and Windows","volume":"10","author":"Excoffier","year":"2010","journal-title":"Mol. Ecol. Resour."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"479","DOI":"10.1093\/genetics\/131.2.479","article-title":"Analysis of molecular variance inferred from metric distances among DNA haplotypes: Application to human mitochondrial DNA restriction data","volume":"131","author":"Excoffier","year":"1992","journal-title":"Genetics"},{"key":"ref_56","unstructured":"(SPSS Statistics for Windows, 2009). SPSS Statistics for Windows, version 18.0."},{"key":"ref_57","unstructured":"(GraphPad Prism, 2019). GraphPad Prism, version 8.0.2."}],"container-title":["Plants"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2223-7747\/15\/19\/3031\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,10,5]],"date-time":"2026-10-05T09:24:19Z","timestamp":1791192259000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2223-7747\/15\/19\/3031"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,10,3]]},"references-count":57,"journal-issue":{"issue":"19","published-online":{"date-parts":[[2026,10]]}},"alternative-id":["plants15193031"],"URL":"https:\/\/doi.org\/10.3390\/plants15193031","relation":{},"ISSN":["2223-7747"],"issn-type":[{"value":"2223-7747","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,10,3]]}}}