Abstract
In plant genetic engineering, to ensure the efficiently expression of foreign genes in recipient plant cells require high-quality promoters. In this study, a novel promoter, WY172, derived from Oidium heveae B.A. Steinm, was isolated and functionally characterized. GUS staining and GUS activity tests indicated that WY172 could effectively drive GUS expression in both monocotyledonous rice and dicotyledonous tobacco. The micro-hypersensitive response revealed that transgenic tobacco harbouring WY172 and HpaXm had more blue necrotic cells than that of positive control of CaMV35S-HpaXm transgenic tobacco. As well, TMV inoculation tests showed fewer lesions on the leaves of WY172-HpaXm transgenic tobacco than those of the positive control, indicating that WY172 could drive the expression of exogenous functional genes HpaXm. Furthermore, the expression level of the HpaXm gene in WY172-HpaXm transgenic tobacco after TMV inoculation was 7.1 times that of uninoculated tobacco. And WY172 also had a relative stronger ability to drive expression of HpaXm after TMV inoculation compared with non-inoculated plants, indicating that WY172 might be a pathogen-inducible promoter. Bioinformatics analysis indicated that WY172 is rich in pathogen-induced cis-acting elements such as auxin response element and light response elements, and induction experiments demonstrated that WY172 drives GUS expression after exogenous application of IAA, which both supported that WY172 might be an inducible promoter. In conclusion, WY172 promoter is an IAA- and pathogen-inducible promoter, which might has high potential for use in a wide range of hosts.
Key message
By blasting and predicting the Oidium heveae B.A. Steinm genome, we obtained and preliminarily demonstrated that the WY172 promoter that may be induced by IAA and TMV. WY172 can play a role in rice and tobacco, and can drive efficient expression of HpaXm in transgenic tobacco and produce TMV resistance and micro-hypersensitive response.
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Abbreviations
- ATMT:
-
Agrobacterium tumefaciens-mediated transformation
- Micro-HR:
-
Micro-hypersensitive response
- TMV:
-
Tobacco mosaic virus
- EPD:
-
Eukaryotic Promoter Database
- IAA:
-
Indole-3-acetic acid
References
Alvarez ME, Pennell RL, Ishikawa MRJ, A, Dixon RA, Lamb C (1998) Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity. Cell 92:773–784
Benfey PN, Chua NH (1990) The cauliflower mosaic virus 35S promoter: combinatorial regulation of transcription in plants. Science 250:959–966
Bhullar S, Chakravarthy S, Advani S, Datta S, Burma PK (2003) Strategies for development of functionally equivalent promoters with minimum sequence homology for transgene expression in plants: cis-elements in a novel DNA context versus domain swapping. Plant Physiol 132:988–998
Bigger CB, Casanova EA, Gardner PD (1996) Transcriptional regulation of neuronal nicotinic acetylcholine receptor genes. J Biol Chem 271:32842–32848
Cai M, Wei J, Li X, Xu C, Wang S (2007) A rice promoter containing both novel positive and negative cis-elements for regulation of green tissue-specific gene expression in transgenic plants. Plant Biotechnol J 5:664–674
Cejudo FJ, Ghose TK, Stabel P, Baulcombe DC (1993) Analysis of the gibberellin-responsive promoter of a cathepsin B-like gene from wheat. Plant Mol Biol 20:849–856
Chen P, Wang C, Soong S, To K (2003) Complete sequence of the binary vector pBI121 and its application in cloning T-DNA insertion from transgenic plants. Mol Breed 11:287–293
Cullen D et al (1987) Controlled expression and secretion of Bovine chymosin in Aspergillus nidulans. Nat Biotechnol 5:369–376
Curtis IS, Hanada A, Kamiya YY (2005) Modification of plant architecture through the expression of GA 2-oxidase under the control of an estrogen inducible promoter in Arabidopsis thaliana L. Planta 222:957–967
Damasevicius R (2008) Analysis of binary feature mapping rules for promoter recognition in imbalanced DNA sequence datasets using Support Vector Machine. Intelligent Systems, 2008 IS '08 4th International IEEE Conference 3:11–20
Dong H, Beer SV (2000) Riboflavin induces disease resistance in plants by activating a novel signal transduction pathway. Phytopathology 90:801–811
Dong H, Delaney TP, Bauer DW, Beer SV (1999) Harpin induces disease resistance in Arabidopsis through the systemic acquired resistance pathway mediated by salicylic acid and the NIM1 gene. Plant J 20:207–215
Dong H et al (2004) Downstream divergence of the ethylene signaling pathway for Harpin-stimulated Arabidopsis growth and insect defense. Plant Physiol 136:3628–3638
Feng H, Xu W, Lin H, Chong K (2009) Transcriptional regulation of wheat VER2 promoter in rice in response to abscisic acid, jasmonate, and light. J Genet Genomics 36:371–377
Fuller KK, Dunlap JC, Loros JJ (2018) Light-regulated promoters for tunable, temporal, and affordable control of fungal gene expression. Appl Microbiol Biotechnol 102:3849–3863
Gallois P, Marinho P (1995) Leaf disk transformation using Agrobacterium tumefaciens-expression of heterologous genes in tobacco. Methods Mol Biol 49:39–48
Gatz C (1996) Chemically inducible promoters in transgenic plants. Curr Opin Biotechnol 7:168–172
Gouka RJ, Punt PJ, Hondel CAM (1997) Efficient production of secreted proteins by Aspergillus: progress, limitations and prospects. Appl Microbiol Biotechnol 47:1–11
Hauptmann RM, Ozias-Akins P, Vasil V, Tabaeizadeh Z, Fraley RT (1987) Transient expression of electroporated DNA in monocotyledonous and dicotyledonous species. Plant Cell Rep 6:265–270
He J, Shen J, Pan H, Huang J, Liang W, He J (2015) Pulmonary lymphoepithelioma-like carcinoma: a surveillance, epidemiology, and end results database analysis. J Thorac Dis 7:2330–2338
Heyser JW, Dykes TA, Demott KJ, Nabors MW (1983) High frequency, long term regeneration of rice from callus culture. Plant Sci Lett 23:175–182
Horsch IRB, Hoffmann JEF, Hoffmann NL, Eichholtz DE, Rogers SR (1985) A simple and general method for transferring genes into plants. Science 227:1229–1231
Hull GA, Devic M (1995) The beta-glucuronidase (gus) reporter gene system. Gene fusions; spectrophotometric, fluorometric, and histochemical detection. Methods Mol Biol 49:125–141
Jefferson RA (1987) Assaying chimeric genes in plants: the GUS gene fusion system. Plant Mol Biol Rep 5:387–405
Justin L, Thorsten NK (2001) A harpin binding site in tobacco plasma membranes mediates activation of the pathogenesis-related gene HIN1 independent of extracellular calcium but dependent on mitogen-activated protein kinase activity. Plant Cell 13:1079–1093
Klement Z, Rudolph K, Sands DC (1990) Methods in phytobacteriology. Akademiai Kiado, Budapest
Kluge J, Terfehr D, Kück U (2018) Inducible promoters and functional genomic approaches for the genetic engineering of filamentous fungi. Appl Microbiol Biotechnol 102:6357
Kong W, Cheng J, Li B, Luo Z, Wu F, Liu A (2014) An overview of researches on pathogen-inducible promoters in plants. Acta Phytophylacica Sinica 41:142–150
Kop DAM, Droog FNJ, Zaal BJ, Hooykaas PJJ (1996) Expression of an auxin-inducible promoter of tobacco in Arabidopsis thaliana. Plant Growth Regul 18:7–14
Kumpatla SP, Chandrasekharan MB, Iyer LM, Li G, Hall TC (1998) Genome intruder scanning and modulation systems and transgene silencing. Trends Plant Sci 3:97–104
Lai L, Huang T, Wang Y, Liu Y, Zhang J, Song Y (2009) The expression of analgesic-antitumor peptide (AGAP) from Chinese Buthus martensii Karsch in transgenic tobacco and tomato. Mol Biol Rep 36:1033–1039
Last DI et al (1991) pEmu: an improved promoter for gene expression in cereal cells. Theor Appl Genet 81:581–588
Lee DJ, Kim SS, Kim SS (2002) The regulation of Korean radish cationic peroxidase promoter by a low ratio of cytokinin to auxin. Plant Sci 162:345–353
Lessard PA, Kulaveerasingam H, York GM, Strong A, Sinskey AJ (2002) Manipulating gene expression for the metabolic engineering of plants. Metab Eng 4:67–79
Li LL, Cheng H, Yuan HH, Xu F, Cheng SY, Cao FL (2014) Functional characterization of the Ginkgo biloba chalcone synthase gene promoter in transgenic tobacco. Genet Mol Res 13:3446–3460
Li Y, Jiang J, Ling N (2006) A rapid method for preparation of filamentous fungi chromosome DNA. J Biol 6:52–53
Li L, Miao W, Liu W, Zhang S (2017) The signal peptide-like segment of hpaXm is required for its association to the cell wall in transgenic tobacco plants. PLoS ONE 12:e0170931
Li X et al (2016) Identification of powdery mildew responsive genes in Hevea brasiliensis through mRNA differential display. Int J Mol Sci 17:172–181
Liang P et al (2019) Corrigendum: powdery mildews are characterized by contracted carbohydrate metabolism and diverse effectors to adapt to obligate biotrophic lifestyle. Front Microbiol 10:1
Limkaisang S, Komun S, Furtado EL, Liew KW, Salleh B, Sato Y, Takamatsu S (2005) Molecular phylogenetic and morphological analyses of Oidium heveae, a powdery mildew of rubber tree. Mycoscience 46:220–226
Lin C, Chen C (2017) The pathogen-inducible promoter of defense-related LsGRP1 gene from Lilium functioning in phylogenetically distinct species of plants. Plant Sci 254:22–31
Liu JJ, Ekramoddoullah AKM, Piggott N, Zamani A (2005) Molecular cloning of a pathogen/wound-inducible PR10 promoter from Pinus monticola and characterization in transgenic Arabidopsis plants. Planta 221:159–169
Liu Y et al (2020) HpaXpm, a novel harpin of Xanthomonas phaseoli pv. manihotis, acts as an elicitor with high thermal stability, reduces disease, and promotes plant growth. BMC Microbiol 20:4
Margolles-Clark E, Harman GE, Penttila M (1996) Enhanced expression of endochitinase in Trichoderma harzianum with the cbh1 promoter of Trichoderma reesei. Appl Environ Microbiol 62:2152–2155
Mcelroy D, Zhang W, Cao J, Wu R (1990) lsolation of an efficient Actin promoter for use in rice transformation. Plant Cell 2:163–171
Mcginnis SD, Madden TL (2004) BLAST: at the core of a powerful and diverse set of sequence analysis tools. Nucleic Acids Res 32:20–25
Miao W, Song C, Wang Y, Wang J (2010a) HpaXm from Xanthomonas citri subsp. malvacearum is a novel harpin with two heptads for hypersensitive response. J Microbiol Biotechnol 20:54–62
Miao W, Wang X, Song C, Wang Y, Ren Y, Wang J (2010b) Transcriptome analysis of Hpa1Xoo transformed cotton revealed constitutive expression of genes in multiple signalling pathways related to disease resistance. J Exp Bot 61:4263–4275
Muhitch MJ, Shatters RG (1998) Regulation of the maize ubiquitin (Ubi-1) promoter in developing maize (Zea mays L.) seeds examined using transient gene expression in kernels grown in vitro. Plant Cell Rep 17:476–481
Naleway JJ (1992) Histochemical, spectrophotometric, and fluorometric GUS substrates. In: Gallapher SR (ed) Gus protocols. Academic Press, New York, pp 61–76
Ni M et al (2009) Micro-HR elicited by Verticillium dahliae kleb. in transgenic hpa1xoo cotton. Xinjiang Agric Sci 46:46–49
Peng JL, Dong HS, Dong HP, Delaney TP, Bonasera JM, Beer SV (2003) Harpin-elicited hypersensitive cell death and pathogen resistance require the NDR1 and EDS1 genes. Physiol Mol Plant Pathol 62:317–326
Peng J, Bao Z, Ren H, Wang J, Dong H (2004) Expression of harpin xoo in transgenic tobacco induces pathogen defense in the absence of hypersensitive cell death. Phytopathology 94:1048–1055
Redkar RJ, Herzog RW, Singh NK (1998) Transcriptional activation of the Aspergillus nidulans gpdA promoter by osmotic signals. Appl Environ Microbiol 64:2229–2231
Schmidt GW, Delaney SK (2010) Stable internal reference genes for normalization of real-time RT-PCR in tobacco (Nicotiana tabacum) during development and abiotic stress. Mol Genet Genomics 283:233–241
Tangphatsornruang S, Uthaipaisanwong P, Sangsrakru D, Chanprasert J, Yoocha T, Jomchai N, Tragoonrung S (2011) Characterization of the complete chloroplast genome of Hevea brasiliensis reveals genome rearrangement, RNA editing sites and phylogenetic relationships. Gene 475:104–112
Wang Y, Klein TM, Fromm M, Cao J, Wu R (1988) Transient expression of foreign genes in rice, wheat and soybean cells following particle bombardment. Plant Mol Biol 11:433–439
Wang M, Rui L, Yan H, Shi H, Wang G (2017) The major leaf ferredoxin Fd2 regulates plant innate immunity in Arabidopsis: leaf ferredoxin Fd2 regulates plant innate immunity. Mol Plant Pathol 19:1377–1390
Wiebe MG (2003) Stable production of recombinant proteins in filamentous fungi - problems and improvements. Mycologist 17:140–144
Wood EJ (1983) Molecular cloning: a laboratory manual. Anal Biochem 11:182–183
Wu C, Jiang P, Guo Y, Liu J, Zhao J, Fu H (2017) Isolation and characterization of Ulva prolifera actin1 gene and function verification of the 5′ flanking region as a strong promoter. Bioeng Bugs 9:124–133
Xu W, Yu Y, Ding J, Hua Z, Wang Y (2010) Characterization of a novel stilbene synthase promoter involved in pathogen- and stress-inducible expression from Chinese wild Vitis pseudoreticulata. Planta 231:475–487
Yoji H, Kozo T, Katsuhiko K, Katsuya G, Chieko K, Gakuzo T, Shodo H (1991) Nucleotide sequence and expression of the glucoamylase-encoding gene (glaA) from Aspergillus oryzae. Gene 108:145–150
Zhou X, Shen W, Rao Z, Wang Z, Zhuge J (2004) A rapid method for preparation of fungal chromosome DNA. Microbiology 4:89–92
Zhou X et al (2019) High temperatures affect the hypersensitive reaction, disease resistance and gene expression induced by a novel harpin HpaG-Xcm. Sci Rep 9(1):1–11
Zuo X, Zhang X, Shan L, Xiao C, Duxiu HE, Binggen RU (2001) Expression of human intestinal trefoil factor (hITF) gene in lettuce. J Integr Plant Biol 43:1047–1051
Acknowledgements
This work was financially supported by the National Key R&D Program of China (No. 2018YFD0201105), the Key Research and Development Program of Hainan Province (ZDYF2018240) and the National Natural Science Foundation of China (No. 31660033, No. 31560495, No.31760499).
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Yin, J., Wang, Y., Zhu, L. et al. The determination of a novel inducible WY172 promoter derived from Oidium heveae HO-73. Plant Cell Tiss Organ Cult 143, 377–387 (2020). https://doi.org/10.1007/s11240-020-01923-1
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DOI: https://doi.org/10.1007/s11240-020-01923-1