{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,3]],"date-time":"2026-09-03T17:27:26Z","timestamp":1788456446295,"version":"build-2803163510"},"reference-count":109,"publisher":"MDPI AG","issue":"22","license":[{"start":{"date-parts":[[2025,11,7]],"date-time":"2025-11-07T00:00:00Z","timestamp":1762473600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Funda\u00e7\u00e3o de Amparo \u00e0 Pesquisa do Estado de Distrito Federal","award":["00.193.00002413\/2023-77"],"award-info":[{"award-number":["00.193.00002413\/2023-77"]}]},{"name":"Instituto Nacional de Ci\u00eancia e Tecnologia (INCT)","award":["465480\/2014-4"],"award-info":[{"award-number":["465480\/2014-4"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>MicroRNAs (miRNAs) are key post-transcriptional regulators of plant development and stress responses, with many being conserved across diverse plant lineages. In this study, we investigated the expression profiles of miRNAs and their corresponding target genes in Arachis stenosperma, a wild peanut relative that exhibits robust resistance to root-knot nematodes (RKN). Small RNA sequencing of nematode-infected roots identified 107 miRNA loci, of which 93 corresponded to conserved miRNA families and 14 represented novel candidates, designated as miRNOVO. Among these, 18 miRNAs belonging to 11 conserved families were identified as differentially expressed (DEMs). Notably, miR399 and miR319 showed the highest upregulation (logFC = 4.25 and 4.20), while miR393 and miR477 were the most downregulated (logFC = \u22120.83 and \u22120.79). Integrated analysis of miRNA and transcriptome data revealed several regulatory interactions involving key defense-related genes. These included NLR genes targeted by miR393 and miR477, hormone signaling components such as the auxin response factor ARF8 targeted by miR167, and the growth regulator GRF2 targeted by miR396. Additionally, miR408 was predicted to target laccase3, a gene involved in the oxidation of phenolic compounds, lignin biosynthesis, copper homeostasis and defense responses. Remarkably, four immune receptor genes belonging to the nucleotide-binding site leucine-rich repeat (NLR) family displayed inverse expression patterns relative to their regulatory miRNAs, suggesting miRNA-mediated post-transcriptional control during the early stages of nematode infection. These findings reveal both conserved and species-specific miRNA\u2013mRNA modules associated with nematode resistance in A. stenosperma, highlighting promising targets for developing RKN-tolerant peanut cultivars through miRNA-based strategies.<\/jats:p>","DOI":"10.3390\/ijms262210824","type":"journal-article","created":{"date-parts":[[2025,11,7]],"date-time":"2025-11-07T11:41:47Z","timestamp":1762515707000},"page":"10824","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":2,"title":["miRNA-Mediated Regulation of Meloidogyne arenaria Responses in Wild Arachis"],"prefix":"10.3390","volume":"26","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-9799-3042","authenticated-orcid":false,"given":"Patricia Messenberg","family":"Guimaraes","sequence":"first","affiliation":[{"name":"EMBRAPA Recursos Gen\u00e9ticos e Biotecnologia, Bras\u00edlia 70770-917, Brazil"},{"name":"Instituto Nacional de Ci\u00eancia e Tecnologia\u2014INCT PlantStress Biotech-Embrapa, Bras\u00edlia 70770-917, Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Andressa da Cunha Quintana","family":"Martins","sequence":"additional","affiliation":[{"name":"EMBRAPA Recursos Gen\u00e9ticos e Biotecnologia, Bras\u00edlia 70770-917, Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Roberto Coiti","family":"Togawa","sequence":"additional","affiliation":[{"name":"EMBRAPA Recursos Gen\u00e9ticos e Biotecnologia, Bras\u00edlia 70770-917, Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mario Alfredo de Passos","family":"Saraiva","sequence":"additional","affiliation":[{"name":"EMBRAPA Recursos Gen\u00e9ticos e Biotecnologia, Bras\u00edlia 70770-917, Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ana Luiza Machado","family":"Lacerda","sequence":"additional","affiliation":[{"name":"EMBRAPA Recursos Gen\u00e9ticos e Biotecnologia, Bras\u00edlia 70770-917, Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0530-062X","authenticated-orcid":false,"given":"Ana Cristina Miranda","family":"Brasileiro","sequence":"additional","affiliation":[{"name":"EMBRAPA Recursos Gen\u00e9ticos e Biotecnologia, Bras\u00edlia 70770-917, Brazil"},{"name":"Instituto Nacional de Ci\u00eancia e Tecnologia\u2014INCT PlantStress Biotech-Embrapa, Bras\u00edlia 70770-917, Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4009-9538","authenticated-orcid":false,"given":"Priscila","family":"Grynberg","sequence":"additional","affiliation":[{"name":"EMBRAPA Recursos Gen\u00e9ticos e Biotecnologia, Bras\u00edlia 70770-917, Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2025,11,7]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"891","DOI":"10.1080\/15476286.2017.1318009","article-title":"Host-Pathogen Interactions Modulated by Small RNAs","volume":"14","author":"Islam","year":"2017","journal-title":"RNA Biol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"73","DOI":"10.2174\/2211536611302010008","article-title":"Small Yet Mighty\u2014MicroRNAs in Plant-Microbe Interactions","volume":"2","author":"Balmer","year":"2013","journal-title":"MicroRNA"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"562","DOI":"10.1016\/j.cell.2013.04.005","article-title":"MicroRNAs Inhibit the Translation of Target MRNAs on the Endoplasmic Reticulum in Arabidopsis","volume":"153","author":"Li","year":"2013","journal-title":"Cell"},{"key":"ref_4","doi-asserted-by":"crossref","unstructured":"Subramanian, S., Fu, Y., Sunkar, R., Barbazuk, W.B., Zhu, J.K., and Yu, O. (2008). Novel and Nodulation-Regulated MicroRNAs in Soybean Roots. BMC Genom., 9.","DOI":"10.1186\/1471-2164-9-160"},{"key":"ref_5","doi-asserted-by":"crossref","unstructured":"Chand Jha, U., Nayyar, H., Mantri, N., and Siddique, K.H.M. (2021). Non-Coding RNAs in Legumes: Their Emerging Roles in Regulating Biotic\/Abiotic Stress Responses and Plant Growth and Development. Cells, 10.","DOI":"10.3390\/cells10071674"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"100180","DOI":"10.1016\/j.xplc.2021.100180","article-title":"Role of Non-Coding RNAs in Plant Immunity","volume":"2","author":"Song","year":"2021","journal-title":"Plant Commun."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"1749","DOI":"10.1093\/jxb\/erv013","article-title":"MicroRNA: A New Target for Improving Plant Tolerance to Abiotic Stress","volume":"66","author":"Zhang","year":"2015","journal-title":"J. Exp. Bot."},{"key":"ref_8","doi-asserted-by":"crossref","unstructured":"Barrera-Figueroa, B.E., Gao, L., Diop, N.N., Wu, Z., Ehlers, J.D., Roberts, P.A., Close, T.J., Zhu, J.K., and Liu, R. (2011). Identification and Comparative Analysis of Drought-Associated MicroRNAs in Two Cowpea Genotypes. BMC Plant Biol., 11.","DOI":"10.1186\/1471-2229-11-127"},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Tong, B., Shi, Y., Ntambiyukuri, A., Li, X., Zhan, J., Wang, A., Xiao, D., and He, L. (2022). Integration of Small RNA and Degradome Sequencing Reveals the Regulatory Network of Al-Induced Programmed Cell Death in Peanut. Int. J. Mol. Sci., 23.","DOI":"10.3390\/ijms23010246"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"1390","DOI":"10.1094\/PDIS-11-19-2286-RE","article-title":"Peanut Yield Loss in the Presence of Defoliation Caused by Late or Early Leaf Spot","volume":"104","author":"Anco","year":"2020","journal-title":"Plant Dis."},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Biswal, A.K., Ozias-Akins, P., and Holbrook, C.C. (2024). Recent Technological Advancements for Identifying and Exploiting Novel Sources of Pest and Disease Resistance for Peanut Improvement. Agronomy, 14.","DOI":"10.3390\/agronomy14123071"},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Guimaraes, P.M., Guimaraes, L.A., Morgante, C.V., Silva, O.B., Araujo, A.C.G., Martins, A.C.Q., Saraiva, M.A.P., Oliveira, T.N., Togawa, R.C., and Leal-Bertioli, S.C.M. (2015). Root Transcriptome Analysis of Wild Peanut Reveals Candidate Genes for Nematode Resistance. PLoS ONE, 10.","DOI":"10.1371\/journal.pone.0140937"},{"key":"ref_13","doi-asserted-by":"crossref","unstructured":"Mota, A.P.Z., Vidigal, B., Danchin, E.G.J., Togawa, R.C., Leal-Bertioli, S.C.M., Bertioli, D.J., Araujo, A.C.G., Brasileiro, A.C.M., and Guimaraes, P.M. (2018). Comparative Root Transcriptome of Wild Arachis Reveals NBS-LRR Genes Related to Nematode Resistance. BMC Plant Biol., 18.","DOI":"10.1186\/s12870-018-1373-7"},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Kumar, D., and Kirti, P.B. (2023). The Genus Arachis: An Excellent Resource for Studies on Differential Gene Expression for Stress Tolerance. Front. Plant Sci., 14.","DOI":"10.3389\/fpls.2023.1275854"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"1681","DOI":"10.1111\/tpj.15409","article-title":"Ectopic Expression of an Expansin-like B Gene from Wild Arachis Enhances Tolerance to Both Abiotic and Biotic Stresses","volume":"107","author":"Brasileiro","year":"2021","journal-title":"Plant J."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"377","DOI":"10.1534\/g3.115.023044","article-title":"Genetic Mapping of Resistance to Meloidogyne arenaria in Arachis stenosperma: A New Source of Nematode Resistance for Peanut","volume":"6","author":"Moretzsohn","year":"2016","journal-title":"G3 Genes Genomes Genet."},{"key":"ref_17","doi-asserted-by":"crossref","unstructured":"Guimar\u00e3es, P.M., Brasileiro, A.C.M., Mehta, A., and Araujo, A.C.G. (2017). Functional Genomics in Peanut Wild Relatives. The Peanut Genome, Springer International Publishing.","DOI":"10.1007\/978-3-319-63935-2_10"},{"key":"ref_18","doi-asserted-by":"crossref","unstructured":"Shen, Y., Liu, Y.H., Zhang, X.J., Sha, Q., and Chen, Z.D. (2016). Gynophore MiRNA Analysis at Different Developmental Stages in Arachis duranensis. Genet. Mol. Res., 15.","DOI":"10.4238\/gmr15048691"},{"key":"ref_19","doi-asserted-by":"crossref","unstructured":"Chen, H., Yang, Q., Chen, K., Zhao, S., Zhang, C., Pan, R., Cai, T., Deng, Y., Wang, X., and Chen, Y. (2019). Integrated MicroRNA and Transcriptome Profiling Reveals a MiRNA-Mediated Regulatory Network of Embryo Abortion under Calcium Deficiency in Peanut (Arachis hypogaea L.). BMC Genom., 20.","DOI":"10.1186\/s12864-019-5770-6"},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"Gao, C., Wang, P., Zhao, S., Zhao, C., Xia, H., Hou, L., Ju, Z., Zhang, Y., Li, C., and Wang, X. (2017). Small RNA Profiling and Degradome Analysis Reveal Regulation of MicroRNA in Peanut Embryogenesis and Early Pod Development. BMC Genom., 18.","DOI":"10.1186\/s12864-017-3587-8"},{"key":"ref_21","doi-asserted-by":"crossref","unstructured":"Li, J., Ma, Y., Hu, M., Zhao, Y., Liu, B., Wang, C., Zhang, M., Zhang, L., Yang, X., and Mu, G. (2022). Multi-Omics and MiRNA Interaction Joint Analysis Highlight New Insights into Anthocyanin Biosynthesis in Peanuts (Arachis hypogaea L.). Front. Plant Sci., 13, Erratum in Front. Plant Sci. 2022, 13, 929085.","DOI":"10.3389\/fpls.2022.818345"},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Ma, X., Zhang, X., Zhao, K., Li, F., Li, K., Ning, L., He, J., Xin, Z., and Yin, D. (2018). Small RNA and Degradome Deep Sequencing Reveals the Roles of MicroRNAs in Seed Expansion in Peanut (Arachis hypogaea L.). Front. Plant Sci., 9.","DOI":"10.3389\/fpls.2018.00349"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"1013","DOI":"10.1007\/s11105-014-0806-1","article-title":"Small RNA and Degradome Deep Sequencing Reveals Peanut MicroRNA Roles in Response to Pathogen Infection","volume":"33","author":"Zhao","year":"2015","journal-title":"Plant Mol. Biol. Rep."},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"Zhao, C., Li, T., Zhao, Y., Zhang, B., Li, A., Zhao, S., Hou, L., Xia, H., Fan, S., and Qiu, J. (2020). Integrated Small RNA and MRNA Expression Profiles Reveal MiRNAs and Their Target Genes in Response to Aspergillus flavus Growth in Peanut Seeds. BMC Plant Biol., 20.","DOI":"10.1186\/s12870-020-02426-z"},{"key":"ref_25","doi-asserted-by":"crossref","unstructured":"Joshi, P., Sharma, V., Pandey, A.K., Nayak, S.N., Bajaj, P., Sudini, H.K., Sharma, S., Varshney, R.K., and Pandey, M.K. (2025). Identification of MiRNAs Associated with Aspergillus flavus Infection and Their Targets in Groundnut (Arachis hypogaea L.). BMC Plant Biol., 25.","DOI":"10.1186\/s12870-025-06322-2"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"276","DOI":"10.1007\/s12042-022-09321-x","article-title":"Multiple MicroRNAs Are Involved in Regulating Peanut (Arachis hypogaea L.) Resistance to Sclerotium rolfsii at the Early Stage","volume":"15","author":"Xu","year":"2022","journal-title":"Trop. Plant Biol."},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"Xu, P., Li, H., Wang, X., Zhao, G., Lu, X., Dai, S., Cui, X., Yuan, M., and Liu, Z. (2022). Integrated Analysis of the LncRNA\/CircRNA-MiRNA-MRNA Expression Profiles Reveals Novel Insights into Potential Mechanisms in Response to Root-Knot Nematodes in Peanut. BMC Genom., 23.","DOI":"10.1186\/s12864-022-08470-3"},{"key":"ref_28","doi-asserted-by":"crossref","unstructured":"Li, F., Han, Y., Zhang, Z., Zhang, B., Zhou, Y., Li, L., Li, Q., Davis, K.E., Patterson, C., and Oo, S. (2021). Response of Root Growth and Development to Nitrogen and Potassium Deficiency as Well as MicroRNA-Mediated Mechanism in Peanut (Arachis hypogaea L.). Front. Plant Sci., 12.","DOI":"10.3389\/fpls.2021.695234"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"e20350","DOI":"10.1002\/tpg2.20350","article-title":"The Role of MicroRNAs in Responses to Drought and Heat Stress in Peanut (Arachis hypogaea)","volume":"16","author":"Mittal","year":"2023","journal-title":"Plant Genome"},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"Zhang, X., Ren, C., Xue, Y., Tian, Y., Zhang, H., Li, N., Sheng, C., Jiang, H., and Bai, D. (2022). Small RNA and Degradome Deep Sequencing Reveals the Roles of MicroRNAs in Peanut (Arachis hypogaea L.) Cold Response. Front. Plant Sci., 13.","DOI":"10.3389\/fpls.2022.920195"},{"key":"ref_31","doi-asserted-by":"crossref","unstructured":"Garg, V., Agarwal, G., Pazhamala, L.T., Nayak, S.N., Kudapa, H., Khan, A.W., Doddamani, D., Sharma, M., Kavi Kishor, P.B., and Varshney, R.K. (2017). Genome-Wide Identification, Characterization, and Expression Analysis of Small RNA Biogenesis Purveyors Reveal Their Role in Regulation of Biotic Stress Responses in Three Legume Crops. Front. Plant Sci., 8.","DOI":"10.3389\/fpls.2017.00488"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"438","DOI":"10.1038\/ng.3517","article-title":"The Genome Sequences of Arachis duranensis and Arachis ipaensis, the Diploid Ancestors of Cultivated Peanut","volume":"48","author":"Bertioli","year":"2016","journal-title":"Nat. Genet."},{"key":"ref_33","doi-asserted-by":"crossref","unstructured":"Chi, X., Yang, Q., Chen, X., Wang, J., Pan, L., Chen, M., Yang, Z., He, Y., Liang, X., and Yu, S. (2011). Identification and Characterization of MicroRNAs from Peanut (Arachis hypogaea L.) by High-Throughput Sequencing. PLoS ONE, 6.","DOI":"10.1371\/journal.pone.0027530"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"D155","DOI":"10.1093\/nar\/gky1141","article-title":"MiRBase: From MicroRNA Sequences to Function","volume":"47","author":"Kozomara","year":"2019","journal-title":"Nucleic Acids Res."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"272","DOI":"10.1105\/tpc.17.00851","article-title":"Revisiting Criteria for Plant MicroRNA Annotation in the Era of Big Data","volume":"30","author":"Axtell","year":"2018","journal-title":"Plant Cell"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"12","DOI":"10.1186\/1746-4811-3-12","article-title":"Protocol: A Highly Sensitive RT-PCR Method for Detection and Quantification of MicroRNAs","volume":"3","author":"Wu","year":"2007","journal-title":"Plant Methods"},{"key":"ref_37","doi-asserted-by":"crossref","unstructured":"Zhou, C., Yang, N., Tian, C., Wen, S., Zhang, C., Zheng, A., Hu, X., Fang, J., Zhang, Z., and Lai, Z. (2024). The MiR166 Targets CsHDZ3 Genes to Negatively Regulate Drought Tolerance in Tea Plant (Camellia sinensis). Int. J. Biol. Macromol., 264.","DOI":"10.1016\/j.ijbiomac.2024.130735"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"988","DOI":"10.1104\/pp.106.079707","article-title":"PHO2, MicroRNA399, and PHR1 Define a Phosphate-Signaling Pathway in Plants","volume":"141","author":"Bari","year":"2006","journal-title":"Plant Physiol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"323","DOI":"10.1111\/jipb.12634","article-title":"Overexpression of MicroRNA408 Enhances Photosynthesis, Growth, and Seed Yield in Diverse Plants","volume":"60","author":"Pan","year":"2018","journal-title":"J. Integr. Plant Biol."},{"key":"ref_40","doi-asserted-by":"crossref","unstructured":"Mota, A.P.Z., Brasileiro, A.C.M., Vidigal, B., Oliveira, T.N., da Cunha Quintana Martins, A., Saraiva, M.A.D.P., de Ara\u00fajo, A.C.G., Togawa, R.C., Grossi-de-S\u00e1, M.F., and Guimaraes, P.M. (2021). Defining the Combined Stress Response in Wild Arachis. Sci. Rep., 11.","DOI":"10.1038\/s41598-021-90607-7"},{"key":"ref_41","doi-asserted-by":"crossref","unstructured":"Samynathan, R., Venkidasamy, B., Shanmugam, A., Ramalingam, S., and Thiruvengadam, M. (2023). Functional Role of MicroRNA in the Regulation of Biotic and Abiotic Stress in Agronomic Plants. Front. Genet., 14.","DOI":"10.3389\/fgene.2023.1272446"},{"key":"ref_42","doi-asserted-by":"crossref","unstructured":"Xu, M., Hu, T., Zhao, J., Park, M.Y., Earley, K.W., Wu, G., Yang, L., and Poethig, R.S. (2016). Developmental Functions of MiR156-Regulated SQUAMOSA PROMOTER BINDING PROTEIN-LIKE (SPL) Genes in Arabidopsis thaliana. PLoS Genet., 12.","DOI":"10.1371\/journal.pgen.1006263"},{"key":"ref_43","doi-asserted-by":"crossref","unstructured":"Zhang, Q., Li, Y., Zhang, Y., Wu, C., Wang, S., Hao, L., Wang, S., and Li, T. (2017). Md-MiR156ab and Md-Mir395 Target WRKY Transcription Factors to Influence Apple Resistance to Leaf Spot Disease. Front. Plant Sci., 8.","DOI":"10.3389\/fpls.2017.00526"},{"key":"ref_44","doi-asserted-by":"crossref","unstructured":"Chen, G., Zou, Y., Hu, J., and Ding, Y. (2018). Genome-Wide Analysis of the Rice PPR Gene Family and Their Expression Profiles under Different Stress Treatments. BMC Genom., 19.","DOI":"10.1186\/s12864-018-5088-9"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"1694","DOI":"10.1104\/pp.17.00823","article-title":"Spatial Control of Gene Expression by MiR319-Regulated TCP Transcription Factors in Leaf Development","volume":"176","author":"Bresso","year":"2018","journal-title":"Plant Physiol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"1365","DOI":"10.1080\/15476286.2020.1774987","article-title":"Utilization of MicroRNAs and Their Regulatory Functions for Improving Biotic Stress Tolerance in Tea Plant [Camellia sinensis (L.) O. Kuntze]","volume":"17","author":"Jeyaraj","year":"2020","journal-title":"RNA Biol."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"129","DOI":"10.1016\/j.molcel.2006.03.011","article-title":"AGO1 Homeostasis Entails Coexpression of MIR168 and AGO1 and Preferential Stabilization of MiR168 by AGO1","volume":"22","author":"Vaucheret","year":"2006","journal-title":"Mol. Cell"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"1000","DOI":"10.1104\/pp.106.078063","article-title":"Pho2, a Phosphate Overaccumulator, Is Caused by a Nonsense Mutation in a MicroRNA399 Target Gene","volume":"141","author":"Aung","year":"2006","journal-title":"Plant Physiol."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"693","DOI":"10.1007\/s00425-018-3027-2","article-title":"Characterization of Genome-Wide MicroRNAs and Their Roles in Development and Biotic Stress in Pear","volume":"249","author":"Zhang","year":"2019","journal-title":"Planta"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"15932","DOI":"10.1074\/jbc.M801406200","article-title":"MicroRNA-Mediated Systemic down-Regulation of Copper Protein Expression in Response to Low Copper Availability in Arabidopsis","volume":"283","author":"Pilon","year":"2008","journal-title":"J. Biol. Chem."},{"key":"ref_51","doi-asserted-by":"crossref","unstructured":"Martins, A.C.Q., Mota, A.P.Z., Carvalho, P.A.S.V., Passos, M.A.S., Gimenes, M.A., Guimaraes, P.M., and Brasileiro, A.C.M. (2022). Transcriptome Responses of Wild Arachis to UV-C Exposure Reveal Genes Involved in General Plant Defense and Priming. Plants, 11.","DOI":"10.3390\/plants11030408"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"882","DOI":"10.1111\/nph.14717","article-title":"Characterization of MicroRNAs from Arabidopsis Galls Highlights a Role for MiR159 in the Plant Response to the Root-Knot Nematode Meloidogyne incognita","volume":"216","author":"Medina","year":"2017","journal-title":"New Phytol."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"321","DOI":"10.1104\/pp.112.193649","article-title":"The Arabidopsis MicroRNA396-GRF1\/GRF3 Regulatory Module Acts as a Developmental Regulator in the Reprogramming of Root Cells during Cyst Nematode Infection","volume":"159","author":"Hewezi","year":"2012","journal-title":"Plant Physiol."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"2431","DOI":"10.1111\/mpp.12720","article-title":"Silenced Retrotransposons Are Major RasiRNAs Targets in Arabidopsis Galls Induced by Meloidogyne javanica","volume":"19","author":"Cabrera","year":"2018","journal-title":"Mol. Plant Pathol."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"1625","DOI":"10.1111\/nph.13735","article-title":"Differentially Expressed Small RNAs in Arabidopsis Galls Formed by Meloidogyne javanica: A Functional Role for MiR390 and Its TAS3-Derived TasiRNAs","volume":"209","author":"Cabrera","year":"2016","journal-title":"New Phytol."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"1622","DOI":"10.1094\/MPMI-21-12-1622","article-title":"Arabidopsis Small RNAs and Their Targets during Cyst Nematode Parasitism","volume":"21","author":"Hewezi","year":"2008","journal-title":"Mol. Plant-Microbe Interact."},{"key":"ref_57","doi-asserted-by":"crossref","unstructured":"Guleria, P., Mahajan, M., Bhardwaj, J., and Yadav, S.K. (2012). Plant Small RNAs: Biogenesis, Mode of Action and Their Roles in Abiotic Stresses. Genom. Proteom. Bioinform., 9.","DOI":"10.1016\/S1672-0229(11)60022-3"},{"key":"ref_58","doi-asserted-by":"crossref","unstructured":"Kaur, P., Shukla, N., Joshi, G., VijayaKumar, C., Jagannath, A., Agarwal, M., Goel, S., and Kumar, A. (2017). Genome-Wide Identification and Characterization of MiRNAome from Tomato (Solanum lycopersicum) Roots and Root-Knot Nematode (Meloidogyne incognita) during Susceptible Interaction. PLoS ONE, 12.","DOI":"10.1371\/journal.pone.0175178"},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"13925","DOI":"10.1038\/ncomms13925","article-title":"Jasmonate Response Decay and Defense Metabolite Accumulation Contributes to Age-Regulated Dynamics of Plant Insect Resistance","volume":"8","author":"Mao","year":"2017","journal-title":"Nat. Commun."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"4559","DOI":"10.1093\/jxb\/erw230","article-title":"Redirection of Auxin Flow in Arabidopsis thaliana Roots after Infection by Root-Knot Nematodes","volume":"67","author":"Kyndt","year":"2016","journal-title":"J. Exp. Bot."},{"key":"ref_61","doi-asserted-by":"crossref","unstructured":"Suzuki, R., Kanno, Y., Abril-Urias, P., Seo, M., Escobar, C., Tsai, A.Y.L., and Sawa, S. (2022). Local Auxin Synthesis Mediated by YUCCA4 Induced during Root-Knot Nematode Infection Positively Regulates Gall Growth and Nematode Development. Front. Plant Sci., 13.","DOI":"10.3389\/fpls.2022.1019427"},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"5752","DOI":"10.1093\/jxb\/erad208","article-title":"AUXIN RESPONSIVE FACTOR8 Regulates Development of the Feeding Site Induced by Root-Knot Nematodes in Tomato","volume":"74","author":"Noureddine","year":"2023","journal-title":"J. Exp. Bot."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"446","DOI":"10.1038\/nature03542","article-title":"The Arabidopsis F-Box Protein TIR1 Is an Auxin Receptor","volume":"435","author":"Kepinski","year":"2005","journal-title":"Nature"},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"1653","DOI":"10.1093\/jxb\/erz022","article-title":"Homeostasis in the Soybean MiRNA396\u2013GRF Network Is Essential for Productive Soybean Cyst Nematode Infections","volume":"70","author":"Noon","year":"2019","journal-title":"J. Exp. Bot."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"101491","DOI":"10.1016\/j.pmpp.2020.101491","article-title":"Expression Analysis of MicroRNAs and Their Target Genes in Cucumis metuliferus Infected by the Root-Knot Nematode Meloidogyne incognita","volume":"111","author":"Ye","year":"2020","journal-title":"Physiol. Mol. Plant Pathol."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"417","DOI":"10.1016\/j.sajb.2023.12.042","article-title":"Identification and Characterization of MicroRNA396 and Its Targets in Cucumis metuliferus Infected with Meloidogyne incognita","volume":"165","author":"Ye","year":"2024","journal-title":"South Afr. J. Bot."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1007\/s10059-011-1043-1","article-title":"The Role of the MiR399-PHO2 Module in the Regulation of Flowering Time in Response to Different Ambient Temperatures in Arabidopsis thaliana","volume":"32","author":"Kim","year":"2011","journal-title":"Mol. Cells"},{"key":"ref_68","doi-asserted-by":"crossref","unstructured":"Tian, B., Wang, S., Todd, T.C., Johnson, C.D., Tang, G., and Trick, H.N. (2017). Genome-Wide Identification of Soybean MicroRNA Responsive to Soybean Cyst Nematodes Infection by Deep Sequencing. BMC Genom., 18.","DOI":"10.1186\/s12864-017-3963-4"},{"key":"ref_69","doi-asserted-by":"crossref","unstructured":"Val-Torregrosa, B., Bund\u00f3, M., and San Segundo, B. (2021). Crosstalk between Nutrient Signalling Pathways and Immune Responses in Rice. Agriculture, 11.","DOI":"10.3390\/agriculture11080747"},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"452","DOI":"10.1111\/tpj.15680","article-title":"Phosphate-Induced Resistance to Pathogen Infection in Arabidopsis","volume":"110","author":"Chiou","year":"2022","journal-title":"Plant J."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"283","DOI":"10.1111\/nph.18362","article-title":"Copper MicroRNAs Modulate the Formation of Giant Feeding Cells Induced by the Root Knot Nematode Meloidogyne incognita in Arabidopsis thaliana","volume":"236","author":"Noureddine","year":"2022","journal-title":"New Phytol."},{"key":"ref_72","doi-asserted-by":"crossref","unstructured":"Xu, M., Li, Y., Zhang, Q., Xu, T., Qiu, L., Fan, Y., and Wang, L. (2014). Novel MiRNA and PhasiRNA Biogenesis Networks in Soybean Roots from Two Sister Lines That Are Resistant and Susceptible to SCN Race 4. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0110051"},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"469","DOI":"10.1093\/jxb\/ery381","article-title":"MicroR408 Regulates Defense Response upon Wounding in Sweet Potato","volume":"70","author":"Kuo","year":"2019","journal-title":"J. Exp. Bot."},{"key":"ref_74","doi-asserted-by":"crossref","unstructured":"Shahbaz, M., and Pilon, M. (2019). Conserved Cu-MicroRNAs in Arabidopsis thaliana Function in Copper Economy under Deficiency. Plants, 8.","DOI":"10.3390\/plants8060141"},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"1423","DOI":"10.1007\/s00425-007-0581-4","article-title":"A Time-Course Comparative Microarray Analysis of an Incompatible and Compatible Response by Glycine max (Soybean) to Heterodera glycines (Soybean Cyst Nematode) Infection","volume":"226","author":"Klink","year":"2007","journal-title":"Planta"},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"743","DOI":"10.1016\/j.bbagrm.2008.04.004","article-title":"The Role of MicroRNAs and Other Endogenous Small RNAs in Plant Stress Responses","volume":"1779","author":"Shukla","year":"2008","journal-title":"Biochim. Biophys. Acta"},{"key":"ref_77","doi-asserted-by":"crossref","unstructured":"Pandian, B.A., Sathishraj, R., Djanaguiraman, M., Prasad, P.V.V., and Jugulam, M. (2020). Role of Cytochrome P450 Enzymes in Plant Stress Response. Antioxidants, 9.","DOI":"10.3390\/antiox9050454"},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"1721","DOI":"10.1104\/pp.107.111260","article-title":"Arabidopsis PPR40 Connects Abiotic Stress Responses to Mitochondrial Electron Transport","volume":"146","author":"Zsigmond","year":"2008","journal-title":"Plant Physiol."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"2053","DOI":"10.1104\/pp.111.177501","article-title":"The Arabidopsis Mitochondria-Localized Pentatricopeptide Repeat Protein PGN Functions in Defense against Necrotrophic Fungi and Abiotic Stress Tolerance","volume":"156","author":"Laluk","year":"2011","journal-title":"Plant Physiol."},{"key":"ref_80","doi-asserted-by":"crossref","unstructured":"Noman, A., Aqeel, M., and Lou, Y. (2019). PRRs and NB-LRRs: From Signal Perception to Activation of Plant Innate Immunity. Int. J. Mol. Sci., 20.","DOI":"10.3390\/ijms20081882"},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"859","DOI":"10.1105\/tpc.111.095380","article-title":"A MicroRNA Superfamily Regulates Nucleotide Binding Site-Leucine-Rich Repeats and Other MRNAs","volume":"24","author":"Shivaprasad","year":"2012","journal-title":"Plant Cell"},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"2222","DOI":"10.1104\/pp.109.151803","article-title":"Identification of MicroRNAs Involved in Pathogen-Associated Molecular Pattern-Triggered Plant Innate Immunity","volume":"152","author":"Li","year":"2010","journal-title":"Plant Physiol."},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"2540","DOI":"10.1101\/gad.177527.111","article-title":"MicroRNAs as Master Regulators of the Plant NB-LRR Defense Gene Family via the Production of Phased, Trans-Acting SiRNAs","volume":"25","author":"Zhai","year":"2011","journal-title":"Genes Dev."},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"3307","DOI":"10.1093\/gbe\/evv225","article-title":"Evolutionarily Dynamic, but Robust, Targeting of Resistance Genes by the MiR482\/2118 Gene Family in the Solanaceae","volume":"7","author":"Kloesges","year":"2015","journal-title":"Genome Biol. Evol."},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"2047","DOI":"10.1111\/nph.17853","article-title":"MicroRNA482\/2118, a MiRNA Superfamily Essential for Both Disease Resistance and Plant Development","volume":"233","author":"Zhang","year":"2022","journal-title":"New Phytol."},{"key":"ref_86","doi-asserted-by":"crossref","unstructured":"Liao, L., Xie, B., Guan, P., Jiang, N., and Cui, J. (2022). New Insight into the Molecular Mechanism of MiR482\/2118 during Plant Resistance to Pathogens. Front. Plant Sci., 13.","DOI":"10.3389\/fpls.2022.1026762"},{"key":"ref_87","doi-asserted-by":"crossref","unstructured":"Tang, J., Gu, X., Liu, J., and He, Z. (2021). Roles of small RNAs in crop disease resistance. Stress Biol., 1.","DOI":"10.1007\/s44154-021-00005-2"},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"6052","DOI":"10.1093\/jxb\/erad268","article-title":"Regulation of plant immunity via small RNA-mediated control of NLR expression","volume":"74","author":"Bejarano","year":"2023","journal-title":"J. Exp. Bot."},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"1298","DOI":"10.1071\/FP13096","article-title":"A Survey of Genes Involved in Arachis stenosperma Resistance to Meloidogyne arenaria Race 1","volume":"40","author":"Morgante","year":"2013","journal-title":"Funct. Plant Biol."},{"key":"ref_90","doi-asserted-by":"crossref","unstructured":"Pereira, B.M., Arraes, F., Quintana Martins, A.C., Freitas Alves, N.S., Melo, B.P., Morgante, C.V., Passos Saraiva, M.A., Grossi-De-S\u00e1, M.F., Guimaraes, P.M., and Miranda Brasileiro, A.C. (2023). A Novel Soybean Hairy Root System for Gene Functional Validation. PLoS ONE, 18.","DOI":"10.1371\/journal.pone.0285504"},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"525","DOI":"10.1038\/nbt.3519","article-title":"Near-Optimal Probabilistic RNA-Seq Quantification","volume":"34","author":"Bray","year":"2016","journal-title":"Nat. Biotechnol."},{"key":"ref_92","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_93","doi-asserted-by":"crossref","unstructured":"Langmead, B., Trapnell, C., Pop, M., and Salzberg, S.L. (2009). Ultrafast and Memory-Efficient Alignment of Short DNA Sequences to the Human Genome. Genome Biol., 10.","DOI":"10.1186\/gb-2009-10-3-r25"},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"2103","DOI":"10.1534\/g3.116.030452","article-title":"Improved Placement of Multi-Mapping Small RNAs","volume":"6","author":"Johnson","year":"2016","journal-title":"G3 Genes Genomes Genet."},{"key":"ref_95","doi-asserted-by":"crossref","first-page":"307","DOI":"10.1007\/978-1-4939-2291-8_19","article-title":"The ViennaRNA Web Services","volume":"1269","author":"Gruber","year":"2015","journal-title":"Methods Mol. Biol."},{"key":"ref_96","doi-asserted-by":"crossref","first-page":"W49","DOI":"10.1093\/nar\/gky316","article-title":"psRNATarget: A plant small RNA target analysis server (2017 release)","volume":"46","author":"Dai","year":"2018","journal-title":"Nucleic Acids Res."},{"key":"ref_97","doi-asserted-by":"crossref","first-page":"139","DOI":"10.1093\/bioinformatics\/btp616","article-title":"EdgeR: A Bioconductor Package for Differential Expression Analysis of Digital Gene Expression Data","volume":"26","author":"Robinson","year":"2009","journal-title":"Bioinformatics"},{"key":"ref_98","doi-asserted-by":"crossref","first-page":"W566","DOI":"10.1093\/nar\/gkv468","article-title":"ClustVis: A Web Tool for Visualizing Clustering of Multivariate Data Using Principal Component Analysis and Heatmap","volume":"43","author":"Metsalu","year":"2015","journal-title":"Nucleic Acids Res."},{"key":"ref_99","doi-asserted-by":"crossref","unstructured":"Wickham, H. (2016). Ggplot2, Springer International Publishing.","DOI":"10.1007\/978-3-319-24277-4"},{"key":"ref_100","doi-asserted-by":"crossref","first-page":"e179","DOI":"10.1093\/nar\/gni178","article-title":"Real-Time Quantification of MicroRNAs by Stem-Loop RT-PCR","volume":"33","author":"Chen","year":"2005","journal-title":"Nucleic Acids Res."},{"key":"ref_101","doi-asserted-by":"crossref","first-page":"1047","DOI":"10.1089\/cmb.2005.12.1047","article-title":"Comprehensive Algorithm for Quantitative Real-Time Polymerase Chain Reaction","volume":"12","author":"Zhao","year":"2005","journal-title":"J. Comput. Biol."},{"key":"ref_102","doi-asserted-by":"crossref","first-page":"e36","DOI":"10.1093\/nar\/30.9.e36","article-title":"Relative Expression Software Tool (REST) for Group-Wise Comparison and Statistical Analysis of Relative Expression Results in Real-Time PCR","volume":"30","author":"Pfaffl","year":"2002","journal-title":"Nucleic Acids Res."},{"key":"ref_103","doi-asserted-by":"crossref","first-page":"3523","DOI":"10.1007\/s11033-019-04779-7","article-title":"Quantitative Expression of MicroRNAs in Brassica oleracea Infected with Xanthomonas campestris pv. campestris","volume":"46","author":"Santos","year":"2019","journal-title":"Mol. Biol. Rep."},{"key":"ref_104","doi-asserted-by":"crossref","unstructured":"Morgante, C.V., Guimar\u00e3es, P.M., Martins, A.C.Q., Ara\u00fajo, A.C.G., Leal-Bertioli, S.C.M., Bertioli, D.J., and Brasileiro, A.C.M. (2011). Reference Genes for Quantitative Reverse Transcription-Polymerase Chain Reaction Expression Studies in Wild and Cultivated Peanut. BMC Res. Notes, 4.","DOI":"10.1186\/1756-0500-4-339"},{"key":"ref_105","doi-asserted-by":"crossref","first-page":"1799","DOI":"10.1111\/pbi.14091","article-title":"A High-Efficiency Gene Silencing in Plants Using Two-Hit Asymmetrical Artificial MicroRNAs","volume":"21","author":"Teotia","year":"2023","journal-title":"Plant Biotechnol. J."},{"key":"ref_106","doi-asserted-by":"crossref","first-page":"241","DOI":"10.1016\/j.gpb.2019.11.006","article-title":"MicroRNAs Are Involved in Maize Immunity Against Fusarium Verticillioides Ear Rot","volume":"18","author":"Zhou","year":"2020","journal-title":"Genom. Proteom. Bioinform."},{"key":"ref_107","doi-asserted-by":"crossref","first-page":"674","DOI":"10.1111\/j.1365-313X.2007.03328.x","article-title":"Gene Silencing in Plants Using Artificial MicroRNAs and Other Small RNAs","volume":"53","author":"Ossowski","year":"2008","journal-title":"Plant J."},{"key":"ref_108","doi-asserted-by":"crossref","unstructured":"Bravo-V\u00e1zquez, L.A., Castro-Pacheco, A.M., P\u00e9rez-Vargas, R., Vel\u00e1zquez-Jim\u00e9nez, J.F., and Paul, S. (2025). The Emerging Applications of Artificial MicroRNA-Mediated Gene Silencing in Plant Biotechnology. Non-Coding RNA, 11.","DOI":"10.3390\/ncrna11020019"},{"key":"ref_109","doi-asserted-by":"crossref","unstructured":"Zhang, F., Yang, J., Zhang, N., Wu, J., and Si, H. (2022). Roles of MicroRNAs in Abiotic Stress Response and Characteristics Regulation of Plant. Front. Plant Sci., 13.","DOI":"10.3389\/fpls.2022.919243"}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/26\/22\/10824\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,11,7]],"date-time":"2025-11-07T11:42:15Z","timestamp":1762515735000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/26\/22\/10824"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,11,7]]},"references-count":109,"journal-issue":{"issue":"22","published-online":{"date-parts":[[2025,11]]}},"alternative-id":["ijms262210824"],"URL":"https:\/\/doi.org\/10.3390\/ijms262210824","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,11,7]]}}}