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Efficient Silencing Gene Construct for Resistance to Multiple Common Bean (Phaseolus Vulgaris L.) Viruses

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Efficient Silencing Gene Construct for Resistance to Multiple Common Bean (Phaseolus Vulgaris L.) Viruses 3 Biotech (2020) 10:278 https://doi.org/10.1007/s13205-020-02276-4 ORIGINAL ARTICLE Efcient silencing gene construct for resistance to multiple common bean (Phaseolus vulgaris L.) viruses Abdolbaset Azizi1 · Jeanmarie Verchot2 · Ahmad Moieni1 · Masoud Shams‑bakhsh1 Received: 14 January 2019 / Accepted: 25 May 2020 © King Abdulaziz City for Science and Technology 2020 Abstract One promising strategy to engineer plants that are resistant to plant pathogens involves transforming plants with RNA silencing constructs for resistance to multiple pathogens. Garden bean is signifcantly damaged by bean common mosaic virus (BCMV), bean common mosaic necrosis virus (BCMNV) and cucumber mosaic virus (CMV). In this study, we prepared constructs producing sense, antisense and hairpin RNA (hpRNA) structures to target single as well as multiple viruses. Silencing efciency of these constructions was analyzed using Agrobacterium (GV3101) transient expression in Nicothinia bethamiana and Phaseolus vulgaris plants. The results showed signifcantly reduced disease symptoms and virus accumulation in N. bethamiana plants. Generally, the efciency of the prepared constructs was hairpin, antisense and sense, respectively, and also, there was a signifcant diference between mono-gene and multiple-gene constructs for reducng virus accumulation and the multiple-gene constructs showed higher efectiveness. Experiments in this study showed that using Agrobacterium harboring binary constructs containing a Caenorhabditis elegans gene, Ced-9, or a plant gene, AtBag-4, anti-apoptosis gene as a mix suspension with an Agrobacterium containing pFGC-BNC.h, a plasmid containing multiple gene fragments consisting of BCMV-CP, BCMNV-HC-Pro and CMV-2b, improved the efciency of pFGC-BNC.h trans- formation. We showed reduced virus accumulation in these transgenic bean plans. Keywords Viruses · RNA silencing · Breeding · Transgenic plant Introduction manner, and by seeds (ICTV Description). CMV is the member of the genus Cucumovirus in the family Bromov- Bean common mosaic virus (BCMV), bean common mosaic iridae, has a broad host range of more than 1300 plant spe- necrosis virus (BCMNV) and cucumber mosaic virus cies, and is transmitted by aphids and mechanically. CMV is (CMV) are major concerns for common bean (Phaseolus transmitted through seeds in certain hosts such as common vulgaris L.) producers worldwide and cause considerable bean (García-Arenal and Palukatis 2008; Yang et al. 1997; damage in common bean plantings (El-Bramaw and El- Davis and Hampton 1986). Beshehy 2011; Faria et al. 1994). BCMV and BCMNV are This study uses RNAi to knock down the expression the related members of the genus Potyvirus in the family of viral suppressors of RNA silencing and to compromise Potyviridae, usually transmitted by aphids in nonpersistent viral response to host defenses (Diaz-Pendon et al. 2007; Goto et al. 2007; Kim et al. 2016). We target the CMV 2b, BCMNV-HC-Pro and BCMV-CP; CMV-2b protein has been Electronic supplementary material The online version of this reported to suppress plant RNA silencing machinery and can article (https ://doi.org/10.1007/s1320 5-020-02276 -4) contains interfere with the salicylic acid pathway which is involved supplementary material, which is available to authorized users. in systemic acquired resistance (Zhang et al. 2006; Ziebell * Masoud Shams-bakhsh et al. 2011). The potyvirus HC-Pro is another silencing [email protected] suppressor protein that interacts with several viral and host proteins and plays an important role in virus transmission 1 Faculty of Agriculture, Tarbiat Modares University, Tehran, by aphids, viral polyprotein maturation and suppression of Iran RNA silencing (Valli et al. 2018). HCPro interferes with 2 Dallas Research, Texas A&M AgriLife Research, Dallas, the methylation of the viral-derived short interfering RNA Texas, USA Vol.:(0123456789)1 3 278 Page 2 of 10 3 Biotech (2020) 10:278 (vsiRNA) (Ivanov et al. 2016), or by inhibition of HEN1 BCMNV was obtained by collecting common bean plants (Jamous et al. 2011). HC-Pro may also disturb the calcium- with typical mosaic symptoms from Tehran bean felds binding capacity of virus (Shen et al. 2010). With this expla- which were diagnosed by polymerase chain reaction (PCR) nation, HC-Pro has been suggested for plant resistance to and enzyme-linked immunosorbent assay (ELISA). potyviruses using RNAi. The potyviral coat protein (CP) has a diferent role including protection of viral genome, viral Bioinformatic analyses and designing of constructs movement, vector transmission (Atreya et al. 1995; Rojas et al. 1997), viral amplifcation (Mahajanet al. 1996) and Genome sequences of the viruses (BCMV, BCMNV and potyviral accumulation (Andrejeva et al. 1999). Potyviral CMV) were obtained from GenBank and multiple sequence CP termini afect long-distance movement (Lopez-Moya and alignments were performed using the GeneDoc software to Pirone 1998), and inhibit viral RNA translation in a dose- fnd the most conservative nucleic acid segment as an RNAi dependent system (Besong-Ndika et al. 2015). This gene has target sequence: (a) a 144-nt fragment of the CMV 2b gene been used efectively for the control of potyviruses (Kim (2442-2586-nt isolate of S72187); (b) a 163-bp fragment of et al. 2016, 2013). the BCMNV-HC-pro (2330-2493-nt isolate of AY138897); Incorporating genetic resistance from wild species into and (c) a 136-bp fragment of the BCMV CP gene (9570- breeding programs is the widely used approach for the con- 9706 nt of AY112735) RNAi scan was used (https ://bioin trol of plant viruses, but this process can take several years fo2.noble.org/RNAiS can/RNAiS can.htm ) to identify poten- to produce a commercial variety (Strausbaugh et al. 2003). tial of-target sequences within the host genome. Fragments Another approach is the use of genetic engineering and were analyzed for secondary structure using RNA structure pathogen-derived resistance (PDR) targets the plant post- software (Reuter and Mathews 2010), sequences were ana- transcriptional gene silencing (PTGS) machinery (Lenne- lyzed for secondary structure, because of the fact that the fors et al. 2006). Many reports show transgene-derived small sequences with low secondary structure are readily available RNAs efectively confer virus resistance (Frizzi and Huang for siRNA production (Duan et al. 2012). The simulations of 2010; Wang et al. 2000) and can be adapted for control- fragments cloning in a sense and antisense orientations were ling several plant viruses (Hu et al. 2011; Sun et al. 2010; run using Vector NTI (v11). Guo et al. 2015; Tan et al. 2012). Robost resistance against seven bean potyviruses was reported in soybean expressing Construction of the binary vectors for gene silencing an intron hairpin NIb RNA (Yang et al. 2017). It was shown that fve intron-spliced hairpin RNA (ihpRNA) constructs The consensus of selected sequences was synthesized by from seven genes of CMV induce resistance to CMV (Miao Jenray Co. (China) and fused as tandem sequences with et al. 2016). The purpose of the present investigation was to adding BamHI and XhoI endonuclease restriction sites at improved the efciency of transformation to common bean the 5′ and EcoRI and HindIII restriction sites at the 3′ end. and to generate efcient gene construct for resistance against The sequence of the fragment from 5′ to 3′ was BCMV-CP, single and multiple bean viruses including CMV, BCMV BCMNV-HC-Pro, and CMV 2b, respectively. Two extra and BCMNV using sense, antisense and hairpin RNA. nucleotides (GG) were placed at each end as an anchor (Fig. 1). Synthesized DNAs and pKannibal plasmids were digested with XhoI and EcoRI enzymes and ligated together Materials and methods for cloning of sense orientation. Synthesized antisense DANS and pKannibal plasmids were digested with BamHI Plant sources and virus isolates and HindIII restriction enzymes and ligated for cloning of antisense orientation. Table 1 contains a list of constructs. Nicotiana benthamiana and common bean (Phaseolus vul- These pKannibal constructs were then partially digested garis L.) plants were used for the assessment of the con- using XhoI and BamHI restriction enzymes for cloning struct efciency. Bean plants [Pinto (Lot: MPS127), Garden into the pFGC5941 binary vector (Fig. 1). The recombinant bean roma II (Lot: PU14010001), Mehali khomain, Goli, pFGC5941 plasmids were confrmed using endonuclease Shahzand)] were mechanically inoculated with virus prepa- restriction digestion and gene sequencing by Macrogene rations diluted in phosphate bufer [0.1 M K 2HPO4, 0.15% Company (South Korea). The gene constructs were prepared 2-β-mercaptoethanol, pH 8.5] (Yarwood 1952). Three bio- in E. coli DH5α and plasmid transformation was carried out logical replicates were carried out per construct and experi- using heat-shock method (Green and Sambrook 2012). Plas- ments were repeated twice. Plants were kept in the growth mid extractions were made using an alkaline lysis method chamber (20 ± 2 °C, 16 h day, 8 h night). In this research, (Green and Sambrook 2012). Using T4 ligase (Fermentas, CMV Fars (EF620777.1) and BCMV RU1 (AY863025) Lithuania), the ligation reactions were carried out in 10 µl isolates were used as the source of viruses. The isolated (0.3 ng plasmid, 0.5 ng DNA fragment, 1 µl ligase bufer, 1 3 3 Biotech (2020) 10:278 Page 3 of 10 278 Fig. 1 Schematic of cloning steps and vector maps. Frag- ments were cloned into pKan- nibal as sense and antisense, between pdk intron and then the
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