{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,1]],"date-time":"2026-10-01T05:09:21Z","timestamp":1790831361814,"version":"4.1.0"},"reference-count":34,"publisher":"MDPI AG","issue":"1","license":[{"start":{"date-parts":[[2023,12,27]],"date-time":"2023-12-27T00:00:00Z","timestamp":1703635200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["32170761"],"award-info":[{"award-number":["32170761"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>CBP60b (CALMODULIN-BINDING PROTEIN 60b) is a member of the CBP60 transcription factor family. In Arabidopsis, AtCBP60b not only regulates growth and development but also activates the transcriptions in immune responses. So far, CBP60b has only been studied extensively in the model plant Arabidopsis and rarely in crops. In this study, Bean pod mottle virus (BPMV)-mediated gene silencing (BPMV-VIGS) was used to silence GmCBP60b.1\/2 in soybean plants. The silencing of GmCBP60b.1\/2 resulted in typical autoimmunity, such as dwarfism and enhanced resistance to both Soybean mosaic virus (SMV) and Pseudomonas syringae pv. glycinea (Psg). To further understand the roles of GmCBP60b in immunity and circumvent the recalcitrance of soybean transformation, we generated transgenic tobacco lines that overexpress GmCBP60b.1. The overexpression of GmCBP60b.1 also resulted in autoimmunity, including spontaneous cell death on the leaves, highly induced expression of PATHOGENESIS-RELATED (PR) genes, significantly elevated accumulation of defense hormone salicylic acid (SA), and significantly enhanced resistance to Pst DC3000 (Pseudomonas syrangae pv. tomato DC3000). The transient coexpression of a luciferase reporter gene driven by the promoter of soybean SYSTEMIC ACQUIRED RESISTANCE DEFICIENT 1 (GmSARD1) (ProGmSARD1::LUC), together with GmCBP60b.1 driven by the 35S promoter, led to the activation of the LUC reporter gene, suggesting that GmCBP60b.1 could bind to the core (A\/T)AATT motifs within the promoter region of GmSARD1 and, thus, activate the expression of the LUC reporter. Taken together, our results indicate that GmCBP60b.1\/2 play both positive and negative regulatory roles in immune responses. These results also suggest that the function of CBP60b is conserved across plant species.<\/jats:p>","DOI":"10.3390\/ijms25010378","type":"journal-article","created":{"date-parts":[[2023,12,27]],"date-time":"2023-12-27T07:45:32Z","timestamp":1703663132000},"page":"378","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":7,"title":["GmCBP60b Plays Both Positive and Negative Roles in Plant Immunity"],"prefix":"10.3390","volume":"25","author":[{"given":"Mei-Yan","family":"Ye","sequence":"first","affiliation":[{"name":"College of Life Sciences, Zhejiang Normal University, Jinhua 321004, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hu-Jiao","family":"Lan","sequence":"additional","affiliation":[{"name":"College of Life Sciences, Zhejiang Normal University, Jinhua 321004, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7826-7045","authenticated-orcid":false,"given":"Jian-Zhong","family":"Liu","sequence":"additional","affiliation":[{"name":"College of Life Sciences, Zhejiang Normal University, Jinhua 321004, China"},{"name":"Zhejiang Provincial Key Laboratory of Biotechnology on Specialty Economic Plants, Zhejiang Normal University, Jinhua 321004, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2023,12,27]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"950","DOI":"10.1016\/j.tplants.2018.08.010","article-title":"Pathogens suppress host transcription factors for rampant proliferation","volume":"23","author":"Ding","year":"2018","journal-title":"Trends Plant Sci."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"1029","DOI":"10.1111\/j.1365-313X.2011.04655.x","article-title":"CBP60g and SARD1 play partially redundant critical roles in salicylic acid signaling","volume":"67","author":"Wang","year":"2011","journal-title":"Plant J."},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"Wang, L., Tsuda, K., Sato, M., Cohen, J.D., Katagiri, F., and Glazebrook, J. (2009). Arabidopsis CaM binding protein CBP60g contributes to MAMP-induced SA accumulation and is involved in disease resistance against Pseudomonas syringae. PLoS Pathog., 5.","DOI":"10.1371\/journal.ppat.1000301"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"18220","DOI":"10.1073\/pnas.1005225107","article-title":"Control of salicylic acid synthesis and systemic acquired resistance by two members of a plant-specific family of transcription factors","volume":"107","author":"Zhang","year":"2010","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"216","DOI":"10.1186\/1471-2229-12-216","article-title":"Co-expression analysis identifies putative targets for CBP60g and SARD1 regulation","volume":"12","author":"Truman","year":"2012","journal-title":"BMC Plant Biol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"10159","DOI":"10.1038\/ncomms10159","article-title":"ChIP-seq reveals broad roles of SARD1 and CBP60g in regulating plant immunity","volume":"6","author":"Sun","year":"2015","journal-title":"Nat. Commun."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"e34902","DOI":"10.7554\/eLife.34902","article-title":"The plant-specific transcription factors CBP60g and SARD1 are targeted by a Verticillium secretory protein VdSCP41 to modulate immunity","volume":"7","author":"Qin","year":"2018","journal-title":"eLife"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"344","DOI":"10.1111\/nph.14780","article-title":"TGACG-BINDING FACTOR 1 (TGA1) and TGA4 regulate salicylic acid and pipecolic acid biosynthesis by modulating the expression of SYSTEMIC ACQUIRED RESISTANCE DEFICIENT 1 (SARD1) and CALMODULIN-BINDING PROTEIN 60g (CBP60g)","volume":"217","author":"Sun","year":"2018","journal-title":"New Phytol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"144","DOI":"10.1016\/j.molp.2019.10.016","article-title":"Redundant CAMTA transcription factors negatively regulate the biosynthesis of salicylic acid and N-hydroxypipecolic acid by modulating the expression of SARD1 and CBP60g","volume":"13","author":"Sun","year":"2020","journal-title":"Mol. Plant"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"1741","DOI":"10.1104\/pp.113.227108","article-title":"The CALMODULIN-BINDING PROTEIN60 family includes both negative and positive regulators of plant immunity","volume":"163","author":"Truman","year":"2013","journal-title":"Plant Physiol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"1645","DOI":"10.1093\/plphys\/kiab164","article-title":"Calmodulin-Binding Protein 60b is a central transcriptional activator of immunity","volume":"186","author":"Li","year":"2021","journal-title":"Plant Physiol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"100213","DOI":"10.1016\/j.xplc.2021.100213","article-title":"Arabidopsis CALMODULIN-BINDING PROTEIN 60b plays dual roles in plant immunity","volume":"2","author":"Huang","year":"2021","journal-title":"Plant Commun."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"9840","DOI":"10.1074\/jbc.M111626200","article-title":"Genes encoding calmodulin-binding proteins in the Arabidopsis genome","volume":"277","author":"Reddy","year":"2002","journal-title":"J. Biol. Chem."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"178","DOI":"10.1038\/nature08670","article-title":"Genome sequence of the palaeopolyploid soybean","volume":"463","author":"Schmutz","year":"2010","journal-title":"Nature"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"52","DOI":"10.1104\/pp.109.151639","article-title":"The development of an efficient multipurpose bean pod mottle virus viral vector set for foreign gene expression and RNA silencing","volume":"153","author":"Zhang","year":"2010","journal-title":"Plant Physiol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"123","DOI":"10.1094\/MPMI-22-2-0123","article-title":"Development and use of an efficient DNA-based viral gene silencing vector for soybean","volume":"22","author":"Zhang","year":"2009","journal-title":"Mol. Plant Microbe Interact."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"304","DOI":"10.1094\/MPMI-19-0304","article-title":"Pseudomonas syringae effector avrB confers soybean cultivar-specific avirulence on Soybean mosaic virus adapted for transgene expression but effector avrPto does not","volume":"19","author":"Wang","year":"2006","journal-title":"Mol. Plant Microbe Interact."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"323","DOI":"10.1038\/nature05286","article-title":"The plant immune system","volume":"444","author":"Jones","year":"2006","journal-title":"Nature"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"539","DOI":"10.1038\/nrg2812","article-title":"Plant immunity: Towards an integrated view of plant\u2013pathogen interactions","volume":"11","author":"Dodds","year":"2010","journal-title":"Nat. Rev. Genet."},{"key":"ref_20","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_21","doi-asserted-by":"crossref","first-page":"1190","DOI":"10.1038\/cr.2008.300","article-title":"MEKK1\/MKK1\/MKK2 and MPK4 function together in a mitogen-activated protein kinase cascade to regulate innate immunity in plants","volume":"18","author":"Gao","year":"2008","journal-title":"Cell Res."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"907","DOI":"10.1104\/pp.18.00903","article-title":"The MAPK kinase GmMEKK1 regulates cell death and defense responses","volume":"178","author":"Xu","year":"2018","journal-title":"Plant Physiol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"824","DOI":"10.1094\/MPMI-11-13-0350-R","article-title":"Positive and negative roles for soybean MPK6 in regulating defense responses","volume":"7","author":"Liu","year":"2014","journal-title":"Mol. Plant Microbe Interact."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"2054","DOI":"10.1111\/nph.15534","article-title":"TIR-NB-LRR immune receptor SOC3 pairs with truncated TIR-NB protein CHS1 or TN2 to monitor the homeostasis of E3 ligase SAUL1","volume":"221","author":"Liang","year":"2019","journal-title":"New Phytol."},{"key":"ref_25","doi-asserted-by":"crossref","unstructured":"Li, J.-M., Ye, M.-Y., Wang, C., Ma, X.-H., Wu, N.-N., Zhong, C.-L., Zhang, Y., Cheng, N., Nakata, P.A., and Zeng, L. (2023). Soybean GmSAUL1, a Bona Fide U-Box E3 Ligase, Negatively Regulates Immunity Likely through Repressing the Activation of GmMPK3. Int. J. Mol. Sci., 24.","DOI":"10.3390\/ijms24076240"},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"Li, J.-M., Ye, M.-Y., Ma, X.-H., Wu, N.-N., and Liu, J.-Z. (2023). Over-expression of soybean GmSAUL1 enhances disease resistance in Nicotiana tabacum. Agronomy, 13.","DOI":"10.3390\/agronomy13061533"},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"Zhao, T., Rui, L., Li, J., Nishimura, M.T., Vogel, J.P., Liu, N., Liu, S., Zhao, Y., Dangl, J.L., and Tang, D. (2015). A truncated NLR protein, TIR-NBS2, is required for activated defense responses in the exo70B1 mutant. PLoS Genet., 11.","DOI":"10.1371\/journal.pgen.1004945"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"110386","DOI":"10.1016\/j.plantsci.2019.110386","article-title":"Silencing GmFLS2 enhances the susceptibility of soybean to bacterial pathogen through attenuating the activation of GmMAPK signaling pathway","volume":"292","author":"Tian","year":"2020","journal-title":"Plant Sci."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"3901","DOI":"10.1002\/j.1460-2075.1987.tb02730.x","article-title":"GUS fusions: Beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants","volume":"6","author":"Jefferson","year":"1987","journal-title":"EMBO J."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"559","DOI":"10.1074\/jbc.M109495200","article-title":"Cell death mediated by MAPK is associated with hydrogen peroxide production in Arabidopsis","volume":"277","author":"Ren","year":"2002","journal-title":"J. Biol. Chem."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"1082","DOI":"10.1104\/pp.17.00695","article-title":"S5H\/DMR6 Encodes a Salicylic Acid 5-Hydroxylase That Fine-Tunes Salicylic Acid Homeostasis","volume":"175","author":"Zhang","year":"2017","journal-title":"Plant Physiol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"1268","DOI":"10.1105\/tpc.104.029637","article-title":"Molecular genetic evidence for the role of SGT1 in the intramolecular complementation of Bs2 protein activity in Nicotiana benthamiana","volume":"17","author":"Leister","year":"2005","journal-title":"Plant Cell"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"1229","DOI":"10.1126\/science.227.4691.1229","article-title":"A simple and general method for transferring genes into plants","volume":"227","author":"Horsch","year":"1985","journal-title":"Science"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1186\/1746-4811-1-13","article-title":"Transient expression vectors for functional genomics, quantification of promoter activity and RNA silencing in plants","volume":"1","author":"Hellens","year":"2005","journal-title":"Plant Methods"}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/25\/1\/378\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T21:42:44Z","timestamp":1760132564000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/25\/1\/378"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,12,27]]},"references-count":34,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2024,1]]}},"alternative-id":["ijms25010378"],"URL":"https:\/\/doi.org\/10.3390\/ijms25010378","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,12,27]]}}}