Abstract
Main Conclusion
The pUceS8.3 is a constitutive gene promoter with potential for ectopic and strong genes overexpression or active biomolecules in plant tissues attacked by pests, including nematode-induced giant cells or galls.
Abstract
Soybean (Glycine max) is one of the most important agricultural commodities worldwide and a major protein and oil source. Herein, we identified the soybean ubiquitin-conjugating (E2) enzyme gene (GmUBC4; Glyma.18G216000), which is significantly upregulated in response to Anticarsia gemmatalis attack and Meloidogyne incognita-induced galls during plant parasitism by plant nematode. The GmUBC4 promoter sequence and its different modules were functionally characterized in silico and in planta using transgenic Arabidopsis thaliana and G. max lines. Its full-length transcriptional regulatory region (promoter and 5´-UTR sequences, named pUceS8.3 promoter) was able to drive higher levels of uidA (β-glucuronidase) gene expression in different tissues of transgenic A. thaliana lines compared to its three shortened modules and the p35SdAMV promoter. Notably, higher β-glucuronidase (GUS) enzymatic activity was shown in M. incognita-induced giant cells when the full pUceS8.3 promoter drove the expression of this reporter gene. Furthermore, nematode-specific dsRNA molecules were successfully overexpressed under the control of the pUceS8.3 promoter in transgenic soybean lines. The RNAi gene construct used here was designed to post-transcriptionally downregulate the previously characterized pre-mRNA splicing factor genes from Heterodera glycines and M. incognita. A total of six transgenic soybean lines containing RNAi gene construct were selected for molecular characterization after infection with M. incognita pre-parasitic second-stage (ppJ2) nematodes. A strong reduction in the egg number produced by M. incognita after parasitism was observed in those transgenic soybean lines, ranging from 71 to 92% compared to wild-type control plants. The present data demonstrated that pUceS8.3 is a gene promoter capable of effectively driving dsRNA overexpression in nematode-induced giant cells of transgenic soybean lines and can be successfully applied as an important biotechnological asset to generate transgenic crops with improved resistance to root-knot nematodes as well as other pests.
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Data availability
The datasets associated with transcript abundance analyzed during the current study are available in the last release of soybean genome assembly (Glycine max Wm82.a4.v1) deposited in Phytozome 13 repository (https://phytozome-next.jgi.doe.gov/) and JGI Data Portal (https://data.jgi.doe.gov/).
Abbreviations
- DAI:
-
Days after inoculation
- GUS:
-
β-Glucuronidase enzyme
- NBTs:
-
New biotechnological tools
- ppJ2:
-
Pre-parasitic second-stage juvenile
- RKN:
-
Root-knot nematode
- UBC:
-
Ubiquitin conjugating
- uidA :
-
GUS-encoding gene
References
Ali MA, Azeem F, Abbas A, Joyia FA, Li H, Dababat AA (2017) Transgenic strategies for enhancement of nematode resistance in plants. Front Plant Sci 8:750. https://doi.org/10.3389/fpls.2017.00750
Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25(17):3389–3402. https://doi.org/10.1093/nar/25.17.3389
Artico S, Lambret-Frotté J, Nardeli SM, Oliveira-Neto OB, Grossi-de-Sa MF, Alves-Ferreira M (2014) Isolation and characterization of three new promoters from Gossypium hirsutum that show high activity in reproductive tissues. Plant Mol Biol Rep 32(3):630–643. https://doi.org/10.1007/s11105-013-0674-0
Bae S-H, Han HW, Moon J (2015) Functional analysis of the molecular interactions of TATA box-containing genes and essential genes. PLoS ONE 10(3):e0120848. https://doi.org/10.1371/journal.pone.0120848
Basso MF, Ferreira PCG, Kobayashi AK, Harmon FG, Nepomuceno AL, Molinari HBC, Grossi-de-Sa MF (2019) MicroRNAs and new biotechnological tools for its modulation and improving stress tolerance in plants. Plant Biotechnol J 17(8):1482–1500. https://doi.org/10.1111/pbi.13116
Basso MF, Arraes FBM, Grossi-de-Sa M, Moreira VJV, Alves-Ferreira M, Grossi-de-Sa MF (2020a) Insights into genetic and molecular elements for transgenic crop development. Front Plant Sci 11:509. https://doi.org/10.3389/fpls.2020.00509
Basso MF, Lourenço-Tessutti IT, Busanello C, Pinto CEM, de Oliveira FE, Ribeiro TP, de Almeida EJ, de Oliveira AC, Morgante CV, Alves-Ferreira M, Grossi-de-Sa MF (2020b) Insights obtained using different modules of the cotton uceA1.7 promoter. Planta 251(2):56. https://doi.org/10.1007/s00425-020-03348-8
Bel Y, Zack M, Narva K, Escriche B (2019) Specific binding of Bacillus thuringiensis Cry1Ea toxin, and Cry1Ac and Cry1Fa competition analyses in Anticarsia gemmatalis and Chrysodeixis includens. Sci Rep 9(1):18201. https://doi.org/10.1038/s41598-019-54850-3
Bird DM (1996) Manipulation of host gene expression by root-knot nematodes. J Parasitol 82(6):881–888
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. https://doi.org/10.1006/abio.1976.9999
Chen K, Tang W-S, Zhou Y-B, Xu Z-S, Chen J, Ma Y-Z, Chen M, Li H-Y (2020) Overexpression of GmUBC9 gene enhances plant drought resistance and affects flowering time via histone H2B monoubiquitination. Front Plant Sci 11:555794. https://doi.org/10.3389/fpls.2020.555794
Chow CN, Zheng HQ, Wu NY, Chien CH, Huang HD, Lee TY, Chiang-Hsieh YF, Hou PF, Yang TY, Chang WC (2016) PlantPAN 2.0: an update of plant promoter analysis navigator for reconstructing transcriptional regulatory networks in plants. Nucleic Acids Res 44(D1):D1154-1160. https://doi.org/10.1093/nar/gkv1035
Christensen AH, Sharrock RA, Quail PH (1992) Maize polyubiquitin genes: structure, thermal perturbation of expression and transcript splicing, and promoter activity following transfer to protoplasts by electroporation. Plant Mol Biol 18(4):675–689. https://doi.org/10.1007/BF00020010
Ciechanover A, Orian A, Schwartz AL (2000) Ubiquitin-mediated proteolysis: biological regulation via destruction. BioEssays 22(5):442–451. https://doi.org/10.1002/(SICI)1521-1878(200005)22:5%3c442::AID-BIES6%3e3.0.CO;2-Q
Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16(6):735–743. https://doi.org/10.1046/j.1365-313x.1998.00343.x
Datla RSS, Bekkaoui F, Hammerlindl JK, Pilate G, Dunstan DI, Crosby WL (1993) Improved high-level constitutive foreign gene expression in plants using an AMV RNA4 untranslated leader sequence. Plant Sci 94(1):139–149. https://doi.org/10.1016/0168-9452(93)90015-R
Dey N, Sarkar S, Acharya S, Maiti IB (2015) Synthetic promoters in planta. Planta 242:1077–1094. https://doi.org/10.1007/s00425-015-2377-2
Doyle, J (1991). DNA protocols for plants. In: Hewitt GM, Johnston AWB, Young JPW (eds) Molecular techniques in taxonomy, 1st edn. Springer Berlin, Heidelberg. doi:https://doi.org/10.1007/978-3-642-83962-7_18
Feng H, Wang S, Dong D, Zhou R, Wang H (2020) Arabidopsis ubiquitin-conjugating enzymes UBC7, UBC13, and UBC14 are required in plant responses to multiple stress conditions. Plants 9(6):723. https://doi.org/10.3390/plants9060723
Gao Y, Wang Y, Xin H, Li S, Liang Z (2017) Involvement of ubiquitin-conjugating enzyme (E2 gene family) in ripening process and response to cold and heat stress of Vitis vinifera. Sci Rep 7(1):13290. https://doi.org/10.1038/s41598-017-13513-x
Garbarino JE, Oosumi T, Belknap WR (1995) Isolation of a polyubiquitin promoter and its expression in transgenic potato plants. Plant Physiol 109(4):1371–1378. https://doi.org/10.1104/pp.109.4.1371
Goodstein DM, Shu S, Howson R, Neupane R, Hayes RD, Fazo J, Mitros T, Dirks W, Hellsten U, Putnam N, Rokhsar DS (2012) Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res 40(D1):D1178–D1186. https://doi.org/10.1093/nar/gkr944
Grefen C, Donald N, Hashimoto K, Kudla J, Schumacher K, Blatt MR (2010) A ubiquitin-10 promoter-based vector set for fluorescent protein tagging facilitates temporal stability and native protein distribution in transient and stable expression studies. Plant J 64(2):355–365. https://doi.org/10.1111/j.1365-313X.2010.04322.x
Grossi-de-Sa MF, Guimarães L, Batista JAN, Viana A, Fragoso RR, Silva MCM (2013) Compositions and methods for modifying gene expression using the promoter of ubiquitin conjugating protein coding gene of soybean plants. USPTO US20130152226A1
Hamawaki OT, Hamawaki RL, Nogueira APO, Glasenapp JS, Hamawaki CDL, Silva COD (2019) Evaluation of soybean breeding lineages to new sources of root-knot nematode resistance. Cienc Agrotec 43:e009519. https://doi.org/10.1590/1413-7054201943009519
Hamera S, Mural RM, Liu Y, Zeng L (2014) The tomato ubiquitin-conjugating enzyme variant SUV, but not SlUev1C and SlUev1D regulates Fen-mediated programmed cell death in Nicotiana benthamiana. Plant Signal Behav 9(10):e973814. https://doi.org/10.4161/15592324.2014.973814
Harrison SJ, Mott EK, Parsley K, Aspinall S, Gray JC, Cottage A (2006) A rapid and robust method of identifying transformed Arabidopsis thaliana seedlings following floral dip transformation. Plant Methods 2(1):19. https://doi.org/10.1186/1746-4811-2-19
Hartman GL, West ED, Herman TK (2011) Crops that feed the world 2. Soybean-worldwide production, use, and constraints caused by pathogens and pests. Food Secur 3(1):5–17. https://doi.org/10.1007/s12571-010-0108-x
Hellemans J, Mortier G, Paepe A, Speleman F, Vandesompele J (2007) qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biol 8(2):1–14. https://doi.org/10.1186/gb-2007-8-2-r19
Hernandez-Garcia CM, Finer JJ (2014) Identification and validation of promoters and cis-acting regulatory elements. Plant Sci 217:109–119. https://doi.org/10.1016/j.plantsci.2013.12.007
Hernandez-Garcia CM, Martinelli AP, Bouchard RA, Finer JJ (2009) A soybean (Glycine max) polyubiquitin promoter gives strong constitutive expression in transgenic soybean. Plant Cell Rep 28(5):837–849. https://doi.org/10.1007/s00299-009-0681-7
Hernandez-Garcia CM, Bouchard RA, Rushton PJ, Jones ML, Chen X, Timko MP, Finer JJ (2010) High level transgenic expression of soybean (Glycine max) GmERF and Gmubi gene promoters isolated by a novel promoter analysis pipeline. BMC Plant Biol 10:237. https://doi.org/10.1186/1471-2229-10-237
Hetzel J, Duttke SH, Benner C, Chory J (2016) Nascent RNA sequencing reveals distinct features in plant transcription. Proc Natl Acad Sci USA 113(43):12316–12321. https://doi.org/10.1073/pnas.1603217113
Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database: 1999. Nucleic Acids Res 27(1):297–300. https://doi.org/10.1093/nar/27.1.297
Holsters M, de Waele D, Depicker A, Messens E, van Montagu M, Schell J (1978) Transfection and transformation of Agrobacterium tumefaciens. Mol Gen Genet 163(2):181–187. https://doi.org/10.1007/BF00267408
Horikoshi RJ, Dourado PM, Berger GU, de S. Fernandes D, Omoto C, Willse A, Martinelli S, Head GP, Correa AS, (2021) Large-scale assessment of lepidopteran soybean pests and efficacy of Cry1Ac soybean in Brazil. Sci Rep 11(1):15956. https://doi.org/10.1038/s41598-021-95483-9
Huseth AS, Koch RL, Reisig D, Davis JA, Paula-Moraes SV, Hodgson EW (2021) Current distribution and population persistence of five lepidopteran pests in U.S. soybean. J Integr Pest Manag. https://doi.org/10.1093/jipm/pmab004
Ichimura Y, Kirisako T, Takao T, Satomi Y, Shimonishi Y, Ishihara N, Mizushima N, Tanida I, Kominami E, Ohsumi M, Noda T, Ohsumi Y (2000) A ubiquitin-like system mediates protein lipidation. Nature 408(6811):488–492. https://doi.org/10.1038/35044114
Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6(13):3901–3907. https://doi.org/10.1002/j.1460-2075.1987.tb02730.x
Jiao Y, Vuong TD, Liu Y, Li Z, Noe J, Robbins RT, Joshi T, Xu D, Shannon JG, Nguyen HT (2015) Identification of quantitative trait loci underlying resistance to southern root-knot and reniform nematodes in soybean accession PI 567516C. Mol Breed 35(6):131–131. https://doi.org/10.1007/s11032-015-0330-5
Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30(4):772–780. https://doi.org/10.1093/molbev/mst010
Kaur A, Pati PK, Pati AM, Nagpal AK (2017) In-silico analysis of cis-acting regulatory elements of pathogenesis-related proteins of Arabidopsis thaliana and Oryza sativa. PLoS ONE 12(9):e0184523. https://doi.org/10.1371/journal.pone.0184523
Kay R, Chan A, Daly M, McPherson J (1987) Duplication of CaMV35S promoter sequences creates a strong enhancer for plant genes. Science 236(4806):1299–1302. https://doi.org/10.1126/science.236.4806.1299
Kim M, Hyten DL, Niblack TL, Diers BW (2011) Stacking resistance alleles from wild and domestic soybean sources improves soybean cyst nematode resistance. Crop Sci 51(3):934–943. https://doi.org/10.2135/cropsci2010.08.0459
Kiselev KV, Aleynova OA, Ogneva ZV, Suprun AR, Dubrovina AS (2021) 35S promoter-driven transgenes are variably expressed in different organs of Arabidopsis thaliana and in response to abiotic stress. Mol Biol Rep 48(3):2235–2241. https://doi.org/10.1007/s11033-021-06235-x
Lescot M, Déhais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, Rouzé P, Rombauts S (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30(1):325–327. https://doi.org/10.1093/nar/30.1.325
Letunic I, Bork P (2021) Interactive tree of life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res 49(W1):W293–W296. https://doi.org/10.1093/nar/gkab301
Li J, Todd TC, Oakley TR, Lee J, Trick HN (2010) Host-derived suppression of nematode reproductive and fitness genes decreases fecundity of Heterodera glycines Ichinohe. Planta 232(3):775–785. https://doi.org/10.1007/s00425-010-1209-7
Limera C, Sabbadini S, Sweet JB, Mezzetti B (2017) New biotechnological tools for the genetic improvement of major woody fruit species. Front Plant Sci 8:1418. https://doi.org/10.3389/fpls.2017.01418
Liu YG, Mitsukawa N, Oosumi T, Whittier RF (1995) Efficient isolation and mapping of Arabidopsis thaliana T-DNA insert junctions by thermal asymmetric interlaced PCR. Plant J 8(3):457–463. https://doi.org/10.1046/j.1365-313x.1995.08030457.x
Lu J, Sivamani E, Li X, Qu R (2008) Activity of the 5´ regulatory regions of the rice polyubiquitin rubi3 gene in transgenic rice plants as analyzed by both GUS and GFP reporter genes. Plant Cell Rep 27(10):1587–1600. https://doi.org/10.1007/s00299-008-0577-y
Marchler-Bauer A, Derbyshire MK, Gonzales NR, Lu S, Chitsaz F, Geer LY, Geer RC, He J, Gwadz M, Hurwitz DI, Lanczycki CJ, Lu F, Marchler GH, Song JS, Thanki N, Wang Z, Yamashita RA, Zhang D, Zheng C, Bryant SH (2015) CDD: NCBI’s conserved domain database. Nucleic Acids Res 43(D1):D222–D226. https://doi.org/10.1093/nar/gku1221
Mazzetti VCG, Visintin GL, Valério IP, Camera JN, Deuner CC, Soares PLM (2019) Reaction of soybean cultivars to Meloidogyne javanica and Meloidogyne incognita. Rev Ceres 66:220–225. https://doi.org/10.1590/0034-737X
Melo BP, Moura SM, Morgante CV, Pinheiro DH, Alves NSF, Rodrigues-Silva PL, Lourenço-Tessutti IT, Andrade RV, Fragoso RR, Grossi-de-Sa MF (2021) Regulated promoters applied to plant engineering: an insight over promising soybean promoters under biotic stress and their cis-elements. BIORI 5:e2021005. https://doi.org/10.4322/biori.202105
Miranda VJ, Coelho RR, Viana AA, Oliveira-Neto OB, Carneiro RM, Rocha TL, Grossi-de-Sa MF, Fragoso RR (2013) Validation of reference genes aiming accurate normalization of qPCR data in soybean upon nematode parasitism and insect attack. BMC Res Notes 6:196. https://doi.org/10.1186/1756-0500-6-196
Moon J, Parry G, Estelle M (2004) The ubiquitin-proteasome pathway and plant development. Plant Cell 16(12):3181–3195. https://doi.org/10.1105/tpc.104.161220
Moura SM, Freitas EO, Ribeiro TP, Paes-de-Melo B, Arraes FBM, Macedo LLP, Paixão JFR, Lourenço-Tessutti IT, Artico S, Cunha-Valença D, Silva MCM, Oliveira AC, Alves-Ferreira M, Grossi-de-Sa MF (2022) Discovery and functional characterization of novel cotton promoters with potential application to pest control. Plant Cell Rep 41(7):1589–1601. https://doi.org/10.1007/s00299-022-02880-z
Park S-H, Yi N, Kim YS, Jeong M-H, Bang S-W, Choi YD, Kim J-K (2010) Analysis of five novel putative constitutive gene promoters in transgenic rice plants. J Exp Bot 61(9):2459–2467. https://doi.org/10.1093/jxb/erq076
Potter SC, Luciani A, Eddy SR, Park Y, Lopez R, Finn RD (2018) HMMER web server: 2018 update. Nucleic Acids Res 46(W1):W200–W204. https://doi.org/10.1093/nar/gky448
Rech EL, Vianna GR, Aragão FJ (2008) High-efficiency transformation by biolistics of soybean, common bean and cotton transgenic plants. Nat Protoc 3(3):410–418. https://doi.org/10.1038/nprot.2008.9
Roth MG, Webster RW, Mueller DS, Chilvers MI, Faske TR, Mathew FM, Bradley CA, Damicone JP, Kabbage M, Smith DL (2020) Integrated management of important soybean pathogens of the United States in changing climate. J Integr Pest Manag. https://doi.org/10.1093/jipm/pmaa013
Savary S, Willocquet L, Pethybridge SJ, Esker P, McRoberts N, Nelson A (2019) The global burden of pathogens and pests on major food crops. Nat Ecol Evol 3(3):430–439. https://doi.org/10.1038/s41559-018-0793-y
Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T, Nelson W, Hyten DL, Song Q, Thelen JJ, Cheng J, Xu D, Hellsten U, May GD, Yu Y, Sakurai T, Umezawa T, Bhattacharyya MK, Sandhu D, Valliyodan B, Lindquist E, Peto M, Grant D, Shu S, Goodstein D, Barry K, Futrell-Griggs M, Abernathy B, Du J, Tian Z, Zhu L, Gill N, Joshi T, Libault M, Sethuraman A, Zhang X-C, Shinozaki K, Nguyen HT, Wing RA, Cregan P, Specht J, Grimwood J, Rokhsar D, Stacey G, Shoemaker RC, Jackson SA (2010) Genome sequence of the palaeopolyploid soybean. Nature 463(7278):178–183. https://doi.org/10.1038/nature08670
Sharma B, Bhatt TK (2017) Genome-wide identification and expression analysis of E2 ubiquitin-conjugating enzymes in tomato. Sci Rep 7(1):8613. https://doi.org/10.1038/s41598-017-09121-4
Sönnichsen B, Koski LB, Walsh A, Marschall P, Neumann B, Brehm M, Alleaume AM, Artelt J, Bettencourt P, Cassin E, Hewitson M, Holz C, Khan M, Lazik S, Martin C, Nitzsche B, Ruer M, Stamford J, Winzi M, Heinkel R, Röder M, Finell J, Häntsch H, Jones SJM, Jones M, Piano F, Gunsalus KC, Oegema K, Gönczy P, Coulson A, Hyman AA, Echeverri CJ (2005) Full-genome RNAi profiling of early embryogenesis in Caenorhabditis elegans. Nature 434(7032):462–469. https://doi.org/10.1038/nature03353
Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30(9):1312–1313. https://doi.org/10.1093/bioinformatics/btu033
Untergasser A, Ruijter JM, Benes V, van den Hoff MJ (2021) Web-based LinRegPCR: application for the visualization and analysis of (RT)-qPCR amplification and melting data. BMC Bioinformatics 22:398. https://doi.org/10.1186/s12859-021-04306-1
Valliyodan B, Cannon SB, Bayer PE, Shu S, Brown AV, Ren L, Jenkins J, Chung CY-L, Chan T-F, Daum CG, Plott C, Hastie A, Baruch K, Barry KW, Huang W, Patil G, Varshney RK, Hu H, Batley J, Yuan Y, Song Q, Stupar RM, Goodstein DM, Stacey G, Lam H-M, Jackson SA, Schmutz J, Grimwood J, Edwards D, Nguyen HT (2019) Construction and comparison of three reference-quality genome assemblies for soybean. Plant J 100(5):1066–1082. https://doi.org/10.1111/tpj.14500
van der Kuyl AC, Neeleman L, Bol JF (1991) Deletion analysis of cis- and trans-acting elements involved in replication of Alfalfa mosaic virus RNA 3 in vivo. Virol 183(2):687–694. https://doi.org/10.1016/0042-6822(91)90997-p
Vernimmen D, Bickmore WA (2015) The hierarchy of transcriptional activation: from enhancer to promoter. Trends Genet 31(12):696–708. https://doi.org/10.1016/j.tig.2015.10.004
Viana AA, Fragoso RR, Guimarães LM, Pontes N, Oliveira-Neto OB, Artico S, Nardeli SM, Alves-Ferreira M, Batista JA, Silva MC, Grossi-de-Sa MF (2011) Isolation and functional characterization of a cotton ubiquitination-related promoter and 5´-UTR that drives high levels of expression in root and flower tissues. BMC Biotechnol 11:115. https://doi.org/10.1186/1472-6750-11-115
Wang J, Oard JH (2003) Rice ubiquitin promoters: deletion analysis and potential usefulness in plant transformation systems. Plant Cell Rep 22(2):129–134. https://doi.org/10.1007/s00299-003-0657-y
Wang R, Zhu M, Ye R, Liu Z, Zhou F, Chen H, Lin Y (2015) Novel green tissue-specific synthetic promoters and cis-regulatory elements in rice. Sci Rep 5(1):18256. https://doi.org/10.1038/srep18256
Waterhouse A, Bertoni M, Bienert S, Studer G, Tauriello G, Gumienny R, Heer FT, Beer TAP, Rempfer C, Bordoli L, Lepore R, Schwede T (2018) SWISS-MODEL: homology modelling of protein structures and complexes. Nucleic Acids Res 46(W1):W296–W303. https://doi.org/10.1093/nar/gky427
Wei H, Wang ML, Moore PH, Albert HH (2003) Comparative expression analysis of two sugarcane polyubiquitin promoters and flanking sequences in transgenic plants. J Plant Physiol 160(10):1241–1251. https://doi.org/10.1078/0176-1617-01086
Yadav BC, Veluthambi K, Subramaniam K (2006) Host-generated double stranded RNA induces RNAi in plant-parasitic nematodes and protects the host from infection. Mol Biochem Parasitol 148(2):219–222. https://doi.org/10.1016/j.molbiopara.2006.03.013
Zhang C, Song L, Choudhary MK, Zhou B, Sun G, Broderick K, Giesler L, Zeng L (2018) Genome-wide analysis of genes encoding core components of the ubiquitin system in soybean (Glycine max) reveals a potential role for ubiquitination in host immunity against soybean cyst nematode. BMC Plant Biol 18(1):149. https://doi.org/10.1186/s12870-018-1365-7
Zhao S, Fernald RD (2005) Comprehensive algorithm for quantitative real-time polymerase chain reaction. Cell Rep 35(4):1047–1064. https://doi.org/10.1089/cmb.2005.12.1047
Zhou B, Mural RV, Chen X, Oates ME, Connor RA, Martin GB, Gough J, Zeng L (2017) A subset of ubiquitin-conjugating enzymes is essential for plant immunity. Plant Physiol 173(2):1371–1390. https://doi.org/10.1104/pp.16.01190
Acknowledgements
We thank Waldir Pereira Dias from Embrapa Soybean for supplying M. incognita isolates, Regina Carneiro from Embrapa Genetic Resources and Biotechnology for her advice on the nematology bioassay, and the team at the Biological Control Lab at Embrapa Genetic Resources and Biotechnology for supplying the A. gemmatalis insects. We are also thankful to all our collaborators from INRA Sophia-Antipolis, France, especially those on the Nematology and Microscopy team.
Funding
This work was supported by the Brazilian Agricultural Research Corporation (Embrapa, call MP2, grant# 02.12.01.002.000), National Council for Scientific and Technological Development (CNPq, call PVE/Linha2, grant 401733/2013–0), Federal District Research Foundation (FAP-DF, call 03/2015 DE, grant 0193.000850/2015), INCT-PlantStress Biotech, Coordination for the Improvement of Higher Education Personnel (CAPES), ABRAPA, and UCB.
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Fragoso, R.R., Arraes, F.B.M., Lourenço-Tessutti, I.T. et al. Functional characterization of the pUceS8.3 promoter and its potential use for ectopic gene overexpression. Planta 256, 69 (2022). https://doi.org/10.1007/s00425-022-03980-6
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DOI: https://doi.org/10.1007/s00425-022-03980-6