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Journal of Integrative Agriculture  2016, Vol. 15 Issue (10): 2215-2227    DOI: 10.1016/S2095-3119(16)61362-X
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Functional analysis of a wheat pleiotropic drug resistance gene involved in Fusarium head blight resistance
WANG Gui-ping1*, HOU Wen-qian1, 2*, ZHANG Lei3, WU Hong-yan1, ZHAO Lan-fei1, DU Xu-ye1, MA Xin1, LI An-fei1, WANG Hong-wei1, KONG Ling-rang1
1 State Key Laboratory of Crop Biology/College of Agronomy, Shandong Agricultural University, Tai’an 271018, P.R.China
2 College of Life Science, Guizhou Normal University, Guiyang 550001, P.R.China
3 College of Horticulture and Forestry Sciences, Huazhong Agricultural University, Wuhan 430070, P.R.China
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Abstract      The pleiotropic drug resistance (PDR) sub-family of adenosine triphosphate (ATP)-binding cassette (ABC) transporter had been reported to participate in diverse biological processes of plant. In this study, we cloned three novel PDR genes in Fusarium head blight (FHB) resistant wheat cultivar Ning 7840, which were located on wheat chromosomes 6A, 6B and 6D. In phylogeny, these genes were members of cluster I together with AePDR7 and BdPDR7. Subcellular localization analysis showed that TaPDR7 was expressed on the plasmalemma. The quantitative real time PCR (RT-PCR) analysis showed that this gene and its probable orthologues in chromosomes 6B and 6D were both up-regulated sharply at 48 h after infected by Fusarium graminearum and trichothecene deoxynivalenol (DON) in spike. When knocking down the transcripts of all TaPDR7 members by barely stripe mosaic virus-induced gene silencing (BSMV-VIGS) system, it could promote the F. graminearum hyphae growth and made larger pathogen inoculation points in Ning 7840, which suggested that TaPDR7 might play an important role in response to F. graminearum. Although salicylic acid (SA), methyl jasmonate (MeJA) and abscisic acid (ABA) had been reported to possibly regulate wheat FHB resistance, here, we found that the three members of TaPDR7 were negatively regulated by these three hormones but positively regulated by indoleacetic acid (IAA).
Keywords:  PDR        FHB        VIGS  
Received: 20 November 2015   Accepted:
Fund: 

This work was supported by the National Natural Science Foundation of China (3315203911, 31471488 and 31171553), the National High-Tech R&D Program of China (2011AA100102 and 2014CB138100), the Transgenic Special Item, China (2016ZX08009-003 and 2016ZX08002003-002), the Natural Science Foundation of Guizhou Province, China (Qianke 2015-2116), the Scientific Research Starting Fund of Doctor of Guizhou Normal University, China, and the Open Subject of National Key Laboratory of Crop Biology, China (2015KF05).

Corresponding Authors:  KONG Ling-rang, Tel: +86-538-8249278, Fax: +86-538-8242226, E-mail: lkong@sdau.edu.cn; WANG Hong-wei, E-mail: wanghongwei@sdau.edu.cn   
About author:  WANG Gui-ping, E-mail: wgp03165@163.com; HOU Wen-qian, E-mail: houwenqian123@163.com;

Cite this article: 

WANG Gui-ping, HOU Wen-qian, ZHANG Lei, WU Hong-yan, ZHAO Lan-fei, DU Xu-ye, MA Xin, LI An-fei, WANG Hong-wei, KONG Ling-rang. 2016. Functional analysis of a wheat pleiotropic drug resistance gene involved in Fusarium head blight resistance. Journal of Integrative Agriculture, 15(10): 2215-2227.

Anderson J P, Badruzsaufari E, Schenk P M, Manners J M, Desmond O J, Ehlert C, Maclean D J, Ebert P R, Kazan K. 2004. Antagonistic interaction between abscisic acid and jasmonate-ethylene signaling pathways modulates defense gene expression and disease resistance in Arabidopsis. The Plant Cell, 16, 3460–3479.

Audenaert K, Meyer G B, Hofte M M. 2002. Abscisic acid determines basal susceptibility of tomato to Botrytis cinerea ans suppresses salicylic acid-dependent signaling mechanisms. Plant Physiology, 128, 491–501.

Bai G H, Shaner G. 2004. Management and resistance in wheat and barley to Fusarium head blight. Annual Review of Phytopathology, 42, 135–161.

Bari R, Jones J D G. 2009. Role of plant hormones in plant defense responses. Plant Molecular Biology, 69, 473–488.

Van Den Brûle S, Müller A, Fleming A J, Smart C C. 2002. The ABC transporter SpTUR2 confers resistance to the antifungal diterpene sclareol. The Plant Journal, 30, 649–662.

Van Den Brûle S, Smart C C. 2002. The plant PDR family of ABC transporters. Planta, 216, 95–106.

Campbell E J, Schenk P M, Kazan K, Penninckx I A M A, Manners J M. 2003. Pathogen-responsive expression of a putative ATP-binding cassette transporter gene conferring resistance to the diterpenoid sclareol is regulated by multiple defense signaling pathways in Arabidopsis. Plant Physiology, 133, 1272–1284.

Chen X, Steed A, Travella S, Keller B, Nicholson P. 2009. Fusarium graminearum exploits ethylene signalling to colonize dicotyledonous and monocotyledonous plants. New Phytologist, 182, 975–983.

Cheng Y, Cui L, Li J Y, Andrew O J, Zhi Y L, Cheng G H, Jia L Y, Da W L. 2011. A high throughput barely stripe mosaic virus vector for virus induced gene silencing in monocots and dicots. PLoS ONE, 10, e26468-e26468.

Cuthbert P A, Somers D J, Brule-Babel A. 2007. Mapping of Fhb2 on chromosome 6BS: A gene controlling Fusarium head blight field resistance in bread wheat (Triticum aestivum L.). Theoretical and Applied Genetics, 114, 429–437.

Das P, Ito T, Wellmer F, Vernoux T, Dedieu A, Traas J, Meyerowitz E M. 2009. Floral stem cell termination involves the direct regulation of AGAMOUS by PERIANTHIA. Development, 136, 1605–1611.

Ding L N, Xu H B, Yi H Y, Yang L M, Kong Z X, Zhang L X, Xue S L, Jia H Y, Ma Z Q. 2011. Resistance to hemi-biotrophi

F. graminearum infection is associated with coordinated and ordered expression of diverse defense signaling pathways. PLoS ONE, 4, e19008.

Ducos E, Fraysse S, Boutry M. 2005. NtPDR3, an iron-deficiency inducible ABC transporter in Nicotiana tabacum. FEBS Letters, 579, 6791–6795.

Eichhorn H, Klinghammer M, Becht P, Tenhaken R. 2006. Isolation of a novel ABC-transporter gene from soybean induced by salicylic acid. Journal of Experimental Botany, 10, 2193–2201.

Ferrari S, Sella L, Janni M, De Lorenzo G, Favaron F, D’Ovidio R. 2011. Transgenic expression of polygalacturonase-inhibiting proteins in Arabidopsis and wheat increases resistance to the flower pathogene Fusarium graminearum. Plant Biology, 14, 31–38.

Garcia O, Bouige P, Forestier C, Dassa E. 2004. Inventory and comparative analysis of rice and Arabidopsis ATP-binding cassette (ABC) system. Journal of Molecular Biology, 343, 249–265.

Goswami R S, Kistler H C. 2005. Pathogenicity and in planta mycotoxin accumulation among members of the Fusarium graminearum species complex on wheat and rice. Phytopathology, 95, 1397–1404.

Higgins C F. 2001. ABC transporters: Physiology, structure and mechanism - An overview. Research in Microbiology, 152, 205–210.

Höfgen R, Willmitzer L. 1988. Storage of competent cells for Agrobacterium transformation. Nucleic Acids Research, 16, 9877.

Holland I B, Blight M A. 1999. ABC-ATPases, adaptable energy generators fuelling transmembrane movement of a variety of molecules in organisms from bacteria to humans. Journal of Molecular Biology, 293, 381–399.

Hollenstein K, Dawson R J, Locher K P. 2007. Structure and mechanism of ABC transporter proteins. Current Opinion in Structural Biology, 17, 412–418.

Hou W Q, Mou J J, Li A F, Wang H W, Kong L R. 2015. Identification of a wheat polygalacturonase-inhibiting protein involved in Fusarium head blight resistance. European Journal of Plant Pathology, 141, 731–745.

Jansen C, von Wettstein D, Schafer W, Kogel K H, Felk A, Maier F J. 2005. Infection patterns in barley and wheat spikes inoculated with wild-type and trichodiene synthase gene disrupted Fusarium graminearum. Proceedings of the National Academy of Sciences of the United States of America, 102, 16892–16897.

Jantasuriyarant C, Gowda M, Haller K, Hatfield J, Lu G, Stahlberg E, Zhou B, Li H, Kim H, Yu Y, Dean R A, Wing R A, Soderlund C, Wang G L. 2005. Large-scale identification of expressed sequence tags involved in rice and rice blast fungus interaction. Plant Physiology, 138, 105–115.

Jasinski M, Ducos E, Martinoia E, Boutry M. 2003. The ATP-binding cassette transporters: Structure, function, and gene family comparison between rice and Arabidopsis. Plant Physiology, 131, 1169–1177.

Kong L R, Anderson J M, Ohm H W. 2005. Induction of wheat defense and stress-related genes in response to Fusarium graminearum. Genome, 48, 29–40.

Kong L R, Ohm H W, Anderson J M. 2007. Expression analysis of defense-related genes in wheat in response to infection by Fusarium graminearum. Genome, 50, 1038–1048.

Lee M, Lee K, Lee J, Noh E W, Lee Y. 2005. AtPDR12 contributes to lead resistance in Arabidopsis. Plant Physiology, 138, 827–836.

Li G, Yen Y. 2008. Jasmonate and ethylene signaling pathway may mediate Fusarium head blight resistance in wheat. Crop Science, 48, 1888–1896.

Llorente F, Muskett P, Sánchez-Vallet A, Lòpez G, Ramos B, Sánchez-Rodríguez C, Jordá L, Parker J, Molina A. 2008. Repression of the auxin response pathway increases Arabidopsis susceptibility to necrotrophic fungi. Molecular Plant, 1, 486–509.

Ma L L, Shang Y, Cao A Z, Qi Z J, Xing L P, Chen P D, Liu D J, Wang X E. 2010. Molecular cloning and characterization of an up-regulated UDP-glucosyltransferase gene induced by DON from Triticum aestivum L. cv. Wangshuibai. Molecular Biology Reports, 37, 785–795.

Makandar R, Essig J S, Schapaugh M A, Trick H N, Shah J. 2006. Genetically engineered resistance to Fusarium head blight in wheat by expression of Arabidopsis NPR1. Molecular Plant-Microbe Interactions, 19, 123–129.

Martinoia E, Klein M, Geisler M, Bovet L, Forestier C, Kolukisaoglu Ü, Müller-Pöber B, Schulz B. 2002. Multifunctionality of plant ABC transporters-more than just detoxifiers. Planta, 214, 345–355.

Mauch-Mani B, Mauch F. 2005. The role of abscisic acid in plant-pathogen interactions. Current Opinion in Plant Biology, 8, 409–414.

Ma X, Du X Y, Liu G J, Yang Z D, Hou W Q, Wang H W, Feng D S. 2015. Cloning and characterization of a novel UDP-glycosyltransferase gene induced by DON from wheat. Journal of Integrative Agriculture, 14, 830–838.

Migocka M, Papierniak A, Warzybok A, Klobus G. 2012. CsPDR8 and CsPDR12, two of the 16 pleiotropic drug resistance genes in cucumber, are transcriptionally regulated by phytohormones and auxin herbicide in roots. Plant Growth Regulation, 67, 171–184.

Moons A. 2003. Ospdr9, which encodes a PDR-type ABC transporter, is induced by heavy metals, hypoxic stress and redox perturbations in rice roots. FEBS Letters, 553, 370–376.

Pritsch C, Muehlbauer G J, Bushnell W R, Somers D A, Vance C P. 2000. Fungal development and induction of defense response genes during early infection of wheat spikes by Fusarium graminearum. Molecular Plant-Microbe Interactions, 13, 159–169.

Ribichich K F, Lopez S E, Vegetti A C. 2000. Histopathological spikelet changes produced by Fusarium graminearum in susceptible and resistant wheat cultivars. Plant Disease, 84, 794–802.

Sánchez F R, Davies T G, Coleman J O, Rea P A. 2001. The Arabidopsis thaliana ABC protein superfamily, a complete inventory. Journal of Biological Chemistry, 276, 30231–30244.

Shang Y, Xiao J, Ma L L, Wang H Y, Qi Z Y, Chen P D, Liu D J, Wang X E. 2009. Characterization of a PDR type ABC transporter gene from wheat (Triticum aestivum L.). Chinese Science Bulletin, 54, 3249–3257.

Shin S, Torres-Acosta J A, Heinen S J, McCormick S, Lemmens M, Paris M P, Berthiller F, Adam G, Muehlbauer G J. 2012. Transgenic Arabidopsis thaliana expressing a barley UDP-glucosyltransferase exhibit resistance to the mycotoxin deoxynivalenol. Journal of Experimental Botany, 63, 4731–4740.

Smart C C, Fleming A J. 1996. Hormonal and environment regulation of a plant PDR5-like ABC transporter. Journal of Biological Chemistry, 271, 19351–19357.

Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. 2011. MEGA 5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution, 28, 2731–2739.

Thaler J S, Bostock R M. 2004. Interactions between abscisic-acid-mediated responses and plant resistance to pathogens and insects. Ecology, 85, 48–58.

Trombik T, Jasunski M, Crouzet J, Boutry M. 2008. Identification of a cluster IV pleiotropic drug resistance transporter gene expressed in the style of Nicotiana plumbaginifolia. Plant Molecular Biology, 66, 165–175.

Walter S, Nicholson P, Doohan FM. 2010. Action and reaction of host and pathogen during Fusarium head blight disease. New Phytologist, 185, 54–66.

Wilde F, Miedaner T. 2006. Selection for Fusarium head blight resistance in early generations reduces the deoxynivalenol (DON) content in grain of winter and spring wheat. Plant Breeding, 125, 96–98.

Xiang Y, Song M, Wei Z Y, Tong J H, Zhang L X, Xiao LT, Ma Z Q, Wang Y. 2011. A jacalin-related lection-like gene in wheat is a component of the plant defence system. Journal of Experimental Botany, 62, 5471–5483.

Xiao J, Jin X H, Jia X P, Wang H Y, Cao A Z, Zhao W P, Pei H Y, Xue Z K, He L Q, Chen Q G, Wang X E. 2013. Transcriptome-based discovery of pathways and genes related to resistance against Fusarium head blight in wheat landrace Wangshuibai. BMC Genomics, 14, 197–216.

Xu X, Nicholson P. 2009. Community ecology of fungal pathogens causing wheat head blight. Annual Review of Phytopathology, 47, 83–103.

Zhang R, Huang J J, Zhu J, Xie X L, Tang Q, Chen X H, Luo J, Lou Z Y. 2013. Isolation and characterization of a novel PDR-type ABC transporter gene PgPDR3 from Panax ginseng C.A. Meyer induced by methyl jasmonate. Molecular Biology Reports, 40, 6195–6204.

Zhang R, Zhu J, Cao H Z, An Y R, Huang J J, Chen X H, Mohammed N, Afrin S, Luo Z Y. 2013. Molecular cloning and expression analysis of PDR-1 like gene in ginseng subjected to salt and cold stress or hormonal treatment. Plant Physiology and Biochemistry, 71, 203–211.

Zhang X L, Shen X R, Hao Y F, Cai J J, Ohm H W, Kong L R. 2011. A genetic map of Lophopyrum ponticum chromosome 7E, harboring resistance genes to Fusarium head blight and leaf rust. Theoretical and Applied Genetics, 122, 263–270.

Zhu X L, Li Z, Xu H J, Zhou M P, Du L P, Zhang Z Y. 2012. Overexpression of wheat lipid transfer protein gene TaLTP5 increases resistance to Cochilobolus sativus and Fusarium graminearum in transgenic wheat. Functional and Integrative Genomics, 12, 481–488.
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