{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,11,2]],"date-time":"2025-11-02T08:56:17Z","timestamp":1762073777322,"version":"build-2065373602"},"reference-count":51,"publisher":"MDPI AG","issue":"21","license":[{"start":{"date-parts":[[2022,10,27]],"date-time":"2022-10-27T00:00:00Z","timestamp":1666828800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"National Natural Science Foundation of China","award":["31640063","31872038"],"award-info":[{"award-number":["31640063","31872038"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>The \u03b12\u03b4 subunit is a high-voltage activated (HVA) calcium channel (Cav1 and Cav2) auxiliary subunit that increases the density and function of HVA calcium channels in the plasma membrane of mammals. However, its function in plant parasitic nematodes remains unknown. In this study, we cloned the full-length cDNA sequence of the voltage-gated calcium channel (VGCC) \u03b12\u03b4 subunit (named DdCav\u03b12\u03b4) in Ditylenchus destructor. We found that DdCav\u03b12\u03b4 tends to be expressed in the egg stage, followed by the J3 stage. RNA-DIG in situ hybridization experiments showed that the DdCav\u03b12\u03b4 subunit was expressed in the body wall, esophageal gland, uterus, post uterine, and spicules of D. destructor. The in vitro application of RNA interference (RNAi) affected the motility, reproduction, chemotaxis, stylet thrusting, and protein secretion of D. destructor to different degrees by targeting DdC\u03b11D, DdC\u03b11A, and DdCav\u03b12\u03b4 in J3 stages, respectively. Based on the results of RNAi experiments, it was hypothesized that L-type VGCC may affect the motility, chemotaxis, and stylet thrusting of D. destructor. Non-L-type VGCC may affect the protein secretion and reproduction of D. destructor. The DdCav\u03b12\u03b4 subunit gene also affected the motility, chemotaxis, and reproduction of D. destructor. These findings reveal the independent function of the VGCC \u03b12\u03b4 subunit in D. destructor as well as give a theoretical foundation for future research on plant parasitic nematode VGCC.<\/jats:p>","DOI":"10.3390\/ijms232112999","type":"journal-article","created":{"date-parts":[[2022,10,27]],"date-time":"2022-10-27T20:37:58Z","timestamp":1666903078000},"page":"12999","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":8,"title":["The \u03b12\u03b4 Calcium Channel Subunit Accessorily and Independently Affects the Biological Function of Ditylenchus destructor"],"prefix":"10.3390","volume":"23","author":[{"given":"Xueling","family":"Chen","sequence":"first","affiliation":[{"name":"College of Plant Protection, Hunan Agricultural University, Changsha 410128, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Mingwei","family":"An","sequence":"additional","affiliation":[{"name":"College of Plant Protection, Hunan Agricultural University, Changsha 410128, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Shan","family":"Ye","sequence":"additional","affiliation":[{"name":"College of Plant Protection, Hunan Agricultural University, Changsha 410128, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Zhuhong","family":"Yang","sequence":"additional","affiliation":[{"name":"College of Plant Protection, Hunan Agricultural University, Changsha 410128, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"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":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2022,10,27]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"S56","DOI":"10.1038\/sj.bjp.0706442","article-title":"A short history of voltage-gated calcium channels","volume":"147","author":"Dolphin","year":"2006","journal-title":"Br. J. Pharmacol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1177\/2398212818794805","article-title":"Voltage-gated calcium channels: Their discovery, function and importance as drug targets","volume":"2","author":"Dolphin","year":"2018","journal-title":"Brain Neurosci. Adv."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"5543","DOI":"10.1073\/pnas.0935295100","article-title":"Functional role of L-type Cav1.3 Ca2+ channels in cardiac pacemaker activity","volume":"100","author":"Mangoni","year":"2003","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"11011","DOI":"10.1523\/JNEUROSCI.2519-09.2009","article-title":"Robust pacemaking in substantia nigra dopaminergic neurons","volume":"29","author":"Guzman","year":"2009","journal-title":"J. Neurosci."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1002\/wmts.102","article-title":"L-type Ca2+ channels in heart and brain","volume":"3","author":"Striessnig","year":"2014","journal-title":"Wiley Interdiscip. Rev. Membr. Transp. Signal."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"675","DOI":"10.1038\/nature02641","article-title":"Structural basis of the \u03b11-\u03b2 subunit interaction of voltage-gated Ca2+ channels","volume":"429","author":"Chen","year":"2004","journal-title":"Nature"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"387","DOI":"10.1016\/S0896-6273(04)00250-8","article-title":"Structural analysis of the voltage-dependent Calcium Channel \u03b2 subunit functional core and its complex with the \u03b11 interaction domain","volume":"42","author":"Opatowsky","year":"2004","journal-title":"Neuron"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"1530","DOI":"10.1016\/j.bbamem.2012.08.028","article-title":"Structure and function of the \u03b2 subunit of voltage-gated Ca2+ channels","volume":"1828","author":"Buraei","year":"2013","journal-title":"Biochim. Biophys. Acta"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"6095","DOI":"10.1523\/JNEUROSCI.21-16-06095.2001","article-title":"Ducky mouse phenotype of epilepsy and ataxia is associated with mutations in the Cacna2d2 gene and decreased calcium channel current in cerebellar Purkinje cells","volume":"21","author":"Barclay","year":"2001","journal-title":"J. Neurosci."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"7684","DOI":"10.1074\/jbc.M109404200","article-title":"The ducky mutation in Cacna2d2 results in altered Purkinje cell morphology and is associated with the expression of a truncated alpha 2 delta-2 protein with abnormal function","volume":"277","author":"Brodbeck","year":"2002","journal-title":"J. Biol. Chem."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"684","DOI":"10.1523\/JNEUROSCI.19-02-00684.1999","article-title":"Molecular diversity of the calcium channel alpha2delta subunit","volume":"19","author":"Klugbauer","year":"1999","journal-title":"J. Neurosci."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"485","DOI":"10.1124\/mol.62.3.485","article-title":"Molecular cloning and characterization of the human voltage-gated calcium channel alpha(2)delta-4 subunit","volume":"62","author":"Qin","year":"2002","journal-title":"Mol. Pharmacol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"973","DOI":"10.1086\/508944","article-title":"Mutation in the auxiliary calcium-channel subunit CACNA2D4 causes autosomal recessive cone dystrophy","volume":"79","author":"Wycisk","year":"2006","journal-title":"Am. J. Hum. Genet."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"22","DOI":"10.1016\/j.ceca.2011.10.002","article-title":"Identification of a disulfide bridge essential for structure and function of the voltage-gated Ca2+ channel \u03b12\u03b4-1 auxiliary subunit","volume":"51","author":"Andrade","year":"2012","journal-title":"Cell Calcium"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"1654","DOI":"10.1073\/pnas.0908735107","article-title":"The alpha2delta subunits of voltage-gated calcium channels form GPI-anchored proteins, a posttranslational modification essential for function","volume":"107","author":"Davies","year":"2010","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/1471-2105-9-392","article-title":"PredGPI: A GPI-anchor predictor","volume":"9","author":"Pierleoni","year":"2008","journal-title":"BMC Bioinform."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"1846","DOI":"10.1093\/bioinformatics\/bti299","article-title":"Identification of GPI anchor attachment signals by a Kohonen self-organizing map","volume":"21","author":"Niklaus","year":"2005","journal-title":"Bioinformatics"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"3369","DOI":"10.1091\/mbc.e02-05-0259","article-title":"Distribution and evolution of von Willebrand\/integrin A domains: Widely dispersed domains with roles in cell adhesion and elsewhere","volume":"13","author":"Whittaker","year":"2002","journal-title":"Mol. Biol. Cell"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"11230","DOI":"10.1073\/pnas.0504183102","article-title":"The metal-ion-dependent adhesion site in the Von Willebrand factor-A domain of alpha2delta subunits is key to trafficking voltage-gated Ca2+ channels","volume":"102","author":"Foucault","year":"2005","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"1541","DOI":"10.1016\/j.bbamem.2012.11.019","article-title":"The \u03b12\u03b4 subunits of voltage-gated calcium channels","volume":"1828","author":"Dolphin","year":"2013","journal-title":"Biochim. Biophys. Acta"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"535","DOI":"10.1016\/S0968-0004(00)01672-8","article-title":"Cache\u2014A signaling domain common to animal Ca2+-channel subunits and a class of prokaryotic chemotaxis receptors","volume":"25","author":"Anantharaman","year":"2000","journal-title":"Trends Biochem. Sci."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"82","DOI":"10.1111\/j.1528-1167.2010.02868.x","article-title":"Calcium channel \u03b12\u03b4 subunits in epilepsy and as targets for antiepileptic drugs","volume":"51","author":"Dolphin","year":"2011","journal-title":"Epilepsia"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"236","DOI":"10.1006\/abio.1997.2447","article-title":"Isolation of the [3H] gabapentin-binding protein\/\u03b12\u03b4 Ca2+ channel subunit from porcine brain: Development of a radioligand binding assay for \u03b12\u03b4 subunits using [3H] leucine","volume":"255","author":"Brown","year":"1998","journal-title":"Anal. Biochem."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"833","DOI":"10.1038\/sj.bjp.0700988","article-title":"Spermine modulation of specific [3H]-gabapentin binding to the detergent-solubilized porcine cerebral cortex \u03b12\u03b4 calcium channel subunit","volume":"120","author":"Dissanayake","year":"1997","journal-title":"Br. J. Pharmacol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"2028","DOI":"10.1126\/science.282.5396.2028","article-title":"Neurobiology of the Caenorhabditis elegans Genome","volume":"282","author":"Bargmann","year":"1998","journal-title":"Science"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"36180","DOI":"10.1074\/jbc.M111.256149","article-title":"The \u03b11 Subunit EGL-19, the \u03b12\/\u03b4 Subunit UNC-36, and the \u03b2 subunit CCB-1 underlie voltage-dependent calcium currents in Caenorhabditis elegans striated muscle","volume":"286","author":"Couchoux","year":"2011","journal-title":"J. Biol. Chem."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"1125","DOI":"10.1002\/neu.20261","article-title":"Effects of voltage-gated calcium channel subunit genes on calcium influx in cultured C. elegans mechanosensory neurons","volume":"66","author":"Kindt","year":"2006","journal-title":"J. Neurobiol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"927","DOI":"10.1163\/156854109X456862","article-title":"A phylogenetic tree of nematodes based on about 1200 full-length small subunit ribosomal DNA sequences","volume":"11","author":"Holovachov","year":"2009","journal-title":"Nematology"},{"key":"ref_29","first-page":"10","article-title":"Ditylenchus destructor in hulls and seeds of peanut","volume":"21","author":"Jones","year":"1989","journal-title":"J. Nematol."},{"key":"ref_30","first-page":"59","article-title":"Reproductive and Damage Potential of Ditylenchus destructor on Six Peanut Cultivars","volume":"25","author":"Venter","year":"1993","journal-title":"J. Nematol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"e2020","DOI":"10.21307\/jofnem-2020-087","article-title":"First report of potato rot nematode, Ditylenchus destructor Thorne, 1945 infecting Codonopsis pilosula in Gansu province, China","volume":"52","author":"Ni","year":"2020","journal-title":"J. Nematol."},{"key":"ref_32","first-page":"778","article-title":"Pathological histology, hosts, and culture of the potato rot nematode","volume":"51","author":"Faulkner","year":"1961","journal-title":"Phytopathology"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"91","DOI":"10.1016\/j.biochi.2020.02.010","article-title":"Molecular characterization of Ditylenchus destructor voltage-gated calcium channel \u03b11 subunits and analysis of the effect of their knockdown on nematode activity","volume":"171","author":"Ye","year":"2020","journal-title":"Biochimie"},{"key":"ref_34","first-page":"1025","article-title":"Nematode spliced leaders\u2014Ubiquity, evolution and utility","volume":"26","author":"Blaxter","year":"1996","journal-title":"Int. J. Parasitol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"138","DOI":"10.1007\/s00438-004-1054-0","article-title":"A survey of SL1-spliced transcripts from the root-lesion nematode Pratylenchus penetrans","volume":"272","author":"Mitreva","year":"2004","journal-title":"Mol. Genet. Genom."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1016\/S0896-6273(00)81133-2","article-title":"From ionic currents to molecular mechanisms: The structure and function of voltage-gated sodium channels","volume":"26","author":"Catterall","year":"2000","journal-title":"Neuron"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"84","DOI":"10.1016\/j.pestbp.2017.03.005","article-title":"Deltamethrin affects the expression of voltage-gated calcium channel \u03b11 subunits and the locomotion, egg-laying, foraging behavior of Caenorhabditis elegans","volume":"138","author":"Zeng","year":"2017","journal-title":"Pestic. Biochem. Physiol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"298","DOI":"10.1016\/S0959-4388(03)00066-7","article-title":"Auxiliary subunits: Essential components of the voltage-gated calcium channel complex","volume":"13","author":"Arikkath","year":"2003","journal-title":"Curr. Opin. Neurobiol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"105","DOI":"10.4149\/gpb_2014037","article-title":"Emerging evidence for specific neuronal functions of auxiliary calcium channel \u03b1\u2082\u03b4 subunits","volume":"34","author":"Geisler","year":"2014","journal-title":"Gen. Physiol. Biophys."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"784","DOI":"10.3390\/ijms23020784","article-title":"Co-Silencing of the Voltage-Gated Calcium Channel \u03b2 Subunit and High-Voltage Activated \u03b11 Subunit by dsRNA Soaking Resulted in Enhanced Defects in Locomotion, Stylet Thrusting, Chemotaxis, Protein Secretion, and Reproduction in Ditylenchus destructor","volume":"23","author":"An","year":"2022","journal-title":"Int. J. Mol. Sci."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"67","DOI":"10.1038\/368067a0","article-title":"Calcium channel beta-subunit binds to a conserved motif in the I-II cytoplasmic linker of the alpha 1-subunit","volume":"368","author":"Pragnell","year":"1994","journal-title":"Nature"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"41809","DOI":"10.1117\/1.NPh.3.4.041809","article-title":"Dynamic association of calcium channel subunits at the cellular membrane","volume":"3","author":"Voigt","year":"2016","journal-title":"Neurophotonics"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"25","DOI":"10.1111\/j.1744-7348.1965.tb07864.x","article-title":"A comparison of some quantitative methods of extracting small vermiform nematodes from soil","volume":"55","author":"Whitehead","year":"1965","journal-title":"Ann. Appl. Biol."},{"key":"ref_44","first-page":"203","article-title":"The Use of Density-Gradient Centrifugation for the Purification of Eggs of Meloidogyne spp.","volume":"7","author":"Schaad","year":"1975","journal-title":"J. Nematol."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"754","DOI":"10.1093\/bioinformatics\/17.8.754","article-title":"MRBAYES: Bayesian inference of phylogenetic trees","volume":"17","author":"Huelsenbeck","year":"2001","journal-title":"Bioinformatics"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"402","DOI":"10.1006\/meth.2001.1262","article-title":"Analysis of relative gene expression data using real- time quantitative PCR and the 2\u2212\u0394\u0394CT Method","volume":"25","author":"Livak","year":"2001","journal-title":"Methods"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"e3372","DOI":"10.21769\/BioProtoc.3372","article-title":"In situ Hybridization of Plant-parasitic Nematode Globodera pallida Juveniles to Detect Gene Expression","volume":"9","author":"Kud","year":"2019","journal-title":"Bio Protoc."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"747","DOI":"10.1094\/MPMI.2002.15.8.747","article-title":"Ingestion of double-stranded RNA by preparasitic juvenile cyst nematodes leads to RNA interference","volume":"15","author":"Urwin","year":"2002","journal-title":"Mol. Plant. Microbe Interact."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"1233","DOI":"10.1096\/fj.06-7343com","article-title":"flp gene disruption in a parasitic nematode reveals motor dysfunction and unusual neuronal sensitivity to RNA interference","volume":"21","author":"Kimber","year":"2007","journal-title":"FASEB J."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"1463","DOI":"10.1094\/Phyto-77-1463","article-title":"Induced Salivation in Plant-Parasitic Nematodes","volume":"77","author":"McClure","year":"1987","journal-title":"Phytopathology"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"1","DOI":"10.2307\/3001478","article-title":"Multiple range and multiple F tests","volume":"11","author":"Duncan","year":"1955","journal-title":"Biometrics"}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/23\/21\/12999\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T01:03:50Z","timestamp":1760144630000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/23\/21\/12999"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,10,27]]},"references-count":51,"journal-issue":{"issue":"21","published-online":{"date-parts":[[2022,11]]}},"alternative-id":["ijms232112999"],"URL":"https:\/\/doi.org\/10.3390\/ijms232112999","relation":{},"ISSN":["1422-0067"],"issn-type":[{"type":"electronic","value":"1422-0067"}],"subject":[],"published":{"date-parts":[[2022,10,27]]}}}