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LrABCF1, a GCN-type ATP-binding cassette transporter from Lilium regale, is involved in defense responses against viral and fungal pathogens

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Abstract

Main conclusion

The L. regale ATP-binding cassette transporter gene, LrABCF1 belonging to GCN subfamily, functions as a positive regulator of plant defense against Cucumber mosaic virus, Tobacco rattle virus , and Botrytis cinerea in petunia.

ATP-binding cassette (ABC) transporters are essential for membrane translocation in diverse biological processes, such as plant development and defense response. Here, a general control non-derepressible (GCN)-type ABC transporter gene, designated LrABCF1, was identified from Cucumber mosaic virus (CMV)-induced cDNA library of L. regale. LrABCF1 was up-regulated upon inoculation with CMV and Lily mottle virus (LMoV). Salicylic acid (SA) and ethylene (ET) application and treatments with abiotic stresses such as cold, high salinity, and wounding increased the transcript abundances of LrABCF1. Constitutive overexpression of LrABCF1 in petunia (Petunia × hybrida) resulted in an impairment of plant growth and development. LrABCF1 overexpression conferred reduced susceptibility to CMV, Tobacco rattle virus (TRV), and B. cinerea infection in transgenic petunia plants, accompanying by elevated transcripts of PhGCN2 and a few defense-related genes in SA-signaling pathway. Our data indicate that LrABCF1 positively modulates viral and fungal resistance.

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Abbreviations

ABC:

ATP-binding cassette

GCN:

General control non-derepressible

CMV:

Cucumber mosaic virus

LMoV:

Lily mottle virus

TRV:

Tobacco rattle virus

SA:

Salicylic acid

ET:

Ethylene

eIF2α:

α subunit of eukaryotic translation initiation factor 2

References

  • Abreu ME, Munné-Bosch S (2009) Salicylic acid deficiency in NahG transgenic lines and sid2 mutants increases seed yield in the annual plant Arabidopsis thaliana. J Exp Bot 60:1261–1271

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ascencio-Ibáñez JT, Sozzani R, Lee TJ, Chu TM, Wolfinger RD, Cella R, Hanley-Bowdoin L (2008) Global analysis of Arabidopsis gene expression uncovers a complex array of changes impacting pathogen response and cell cycle during geminivirus infection. Plant Physiol 148:436–454

    Article  PubMed  PubMed Central  Google Scholar 

  • Asjes C, Blom-Barnhoorn G (2001) Control of aphid vector spread of Lily symptomless virus and Lily mottle virus by mineral oil/insecticide sprays in Lilium. Acta Hort 570:277–281

    Google Scholar 

  • Austin CM, Ma X, Graviss EA (2008) Common nonsynonymous polymorphisms in the NOD2 gene are associated with resistance or susceptibility to tuberculosis disease in African Americans. J Infect Dis 197:1713–1716

    Article  CAS  PubMed  Google Scholar 

  • Azadi P, Otang NV, Supaporn H, Khan RS, Chin DP, Nakamura I, Mii M (2011) Increased resistance to Cucumber mosaic virus (CMV) in Lilium transformed with a defective CMV replicase gene. Biotechnol Lett 33:1249–1255

    Article  CAS  PubMed  Google Scholar 

  • Barry G, Breakwell L, Fragkoudis R, Attarzadeh-Yazdi G, Rodriguez-Andres J, Kohl A, Fazakerley JK (2009) PKR acts early in infection to suppress Semliki Forest virus production and strongly enhances the type I interferon response. J Gen Virol 90:1382–1391

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bennett MD, Leitch IJ, Price HJ, Johnston JS (2003) Comparisons with Caenorhabditis (∼100 Mb) and Drosophila (∼175 Mb) using flow cytometry show genome size in Arabidopsis to be ∼157 Mb and thus ∼25 % larger than the Arabidopsis genome initiative estimate of ∼125 Mb. Ann Bot 91:547–557

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Berlanga JJ, Ventoso I, Harding HP, Deng J, Ron D, Sonenberg N, Carrasco L, de Haro C (2006) Antiviral effect of the mammalian translation initiation factor 2α kinase GCN2 against RNA viruses. EMBO J 25:1730–1740

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bryan GT, Wu KS, Farrall L, Jia Y, Hershey HP, Mcadams SA, Faulk KN, Donaldson GK, Tarchini R, Valent B (2000) A single amino acid difference distinguishes resistant and susceptible alleles of the rice blast resistance gene Pi-ta. Plant Cell 12:2033–2046

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Byrne EH (2010) Molecular cloning and characterisation of the general control non-derepressible 2 protein kinase from Triticum aestivum. University College London, London

    Google Scholar 

  • Campe R, Langenbach C, Leissing F, Popescu GV, Popescu SC, Goellner K, Beckers GJ, Conrath U (2016) ABC transporter PEN3/PDR8/ABCG36 interacts with calmodulin that, like PEN3, is required for Arabidopsis nonhost resistance. New Phytol 209:294–306

    Article  CAS  PubMed  Google Scholar 

  • Chen JC, Jiang CZ, Gookin T, Hunter D, Clark D, Reid M (2004) Chalcone synthase as a reporter in virus-induced gene silencing studies of flower senescence. Plant Mol Biol 55:521–530

    Article  CAS  PubMed  Google Scholar 

  • Faus I, Zabalza A, Santiago J, Nebauer SG, Royuela M, Serrano R, Gadea J (2015) Protein kinase GCN2 mediates responses to glyphosate in Arabidopsis. BMC Plant Biol 15:1–12

    Article  Google Scholar 

  • Gaba A, Wang Z, Krishnamoorthy T, Hinnebusch AG, Sachs MS (2001) Physical evidence for distinct mechanisms of translational control by upstream open reading frames. EMBO J 20:6453–6463

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Garcia O, Bouige P, Forestier C, Dassa E (2004) Inventory and comparative analysis of rice and Arabidopsis ATP-binding cassette (ABC) systems. J Mol Biol 343:249–265

    Article  CAS  PubMed  Google Scholar 

  • Garcia-Barrio M, Dong J, Ufano S, Hinnebusch AG (2000) Association of GCN1–GCN20 regulatory complex with the N-terminus of eIF2α kinase GCN2 is required for GCN2 activation. EMBO J 19:1887–1899

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harding HP, Novoa I, Zhang Y, Zeng H, Wek R, Schapira M, Ron D (2000) Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol Cell 6:1099–1108

    Article  CAS  PubMed  Google Scholar 

  • Higgins CF (1992) ABC transporters: from microorganisms to man. Annu Rev Cell Biol 8:67–113

    Article  CAS  PubMed  Google Scholar 

  • Hinnebusch AG (2005) Translational regulation of GCN4 and the general amino acid control of yeast. Annu Rev Microbiol 59:407–450

    Article  CAS  PubMed  Google Scholar 

  • Holland IB, Cole SP, Kuchler K, Higgins CF (2003) ABC proteins: from bacteria to man. Academic Press, London

    Google Scholar 

  • Hou PF, Chen CY (2003) Early stages of infection of lily leaves by Botrytis elliptica and B. cinerea. Plant Pathol Bulletin 12:103–108

    Google Scholar 

  • Hull R (2009) Mechanical inoculation of plant viruses. Curr Protoc Microbiol 13:16B.6.1–16B.6.4

  • Jasiński M, Stukkens Y, Degand H, Purnelle B, Marchand-Brynaert J, Boutry M (2001) A plant plasma membrane ATP binding cassette–type transporter is involved in antifungal terpenoid secretion. Plant Cell 13:1095–1107

    Article  PubMed  PubMed Central  Google Scholar 

  • Jiang CZ, Chen JC, Reid MS (2011) Virus-induced gene silencing in ornamental plants. In: Kodama H, Komamine A (eds) RNAi and plant gene function analysis: methods and protocols. Methods Mol Biol 744:81–96

  • Kobae Y, Sekino T, Yoshioka H, Nakagawa T, Martinoia E, Maeshima M (2006) Loss of AtPDR8, a plasma membrane ABC transporter of Arabidopsis thaliana, causes hypersensitive cell death upon pathogen infection. Plant Cell Physiol 47:309–318

    Article  CAS  PubMed  Google Scholar 

  • Krattinger SG, Lagudah ES, Spielmeyer W, Singh RP, Huerta-Espino J, McFadden H, Bossolini E, Selter LL, Keller B (2009) A putative ABC transporter confers durable resistance to multiple fungal pathogens in wheat. Science 323:1360–1363

    Article  CAS  PubMed  Google Scholar 

  • Kubota H, Ota K, Sakaki Y, Ito T (2001) Budding yeast GCN1 binds the GI domain to activate the eIF2α kinase GCN2. J Biol Chem 276:17591–17596

    Article  CAS  PubMed  Google Scholar 

  • Lageix S, Lanet E, Pouch-Pélissier MN, Espagnol MC, Robaglia C, Deragon JM, Pélissier T (2008) Arabidopsis eIF2α kinase GCN2 is essential for growth in stress conditions and is activated by wounding. BMC Plant Biol 8:134

    Article  PubMed  PubMed Central  Google Scholar 

  • Li M, AuYeung W, Lam H (2013a) The GCN2 homologue in Arabidopsis thaliana interacts with uncharged tRNA and uses Arabidopsis eIF2α molecules as direct substrates. Plant Biol 15:13–18

    Article  PubMed  Google Scholar 

  • Li XY, Wang CX, Sun HM, Li TL (2013b) Establishment of the total RNA extraction system for lily bulbs with abundant polysaccharides. Afr J Biotechnol 10:17907–17915

    Google Scholar 

  • Lim PO, Lee U, Ryu JS, Choi JK, Hovanessian A, Kim CS, Cho BH, Nam HG (2002) Multiple virus resistance in transgenic plants conferred by the human dsRNA-dependent protein kinase. Mol Breeding 10:11–18

    Article  CAS  Google Scholar 

  • Lim J, Rhee H, Kim Y, Lim K, Van Tuyl J (2003) Resistance to Fusarium oxysporum f. sp. lilii in Lilium. Acta Hort 620:311–318

    Article  Google Scholar 

  • Liu X, Merchant A, Rockett KS, McCormack M, Pajerowska-Mukhtar KM (2015) Characterization of Arabidopsis thaliana GCN2 kinase roles in seed germination and plant development. Plant Signal Behav 10:e992264

    Article  PubMed  PubMed Central  Google Scholar 

  • Malamy J, Carr JP, Klessig DF, Raskin I (1990) Salicylic acid: a likely endogenous signal in the resistance response of tobacco to viral infection. Science 250:1002–1004

    Article  CAS  PubMed  Google Scholar 

  • Marton MJ, De Aldana CV, Qiu H, Chakraburtty K, Hinnebusch AG (1997) Evidence that GCN1 and GCN20, translational regulators of GCN4, function on elongating ribosomes in activation of eIF2alpha kinase GCN2. Mol Cell Biol 17:4474–4489

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Monaghan J, Li X (2010) The HEAT repeat protein ILITYHIA is required for plant immunity. Plant Cell Physiol 51:742–753

    Article  CAS  PubMed  Google Scholar 

  • Moons A (2003) Ospdr9, which encodes a PDR-type ABC transporter, is induced by heavy metals, hypoxic stress and redox perturbations in rice roots 1. FEBS Lett 553:370–376

    Article  CAS  PubMed  Google Scholar 

  • Natarajan K, Meyer MR, Jackson BM, Slade D, Roberts C, Hinnebusch AG, Marton MJ (2001) Transcriptional profiling shows that GCN4p is a master regulator of gene expression during amino acid starvation in yeast. Mol Cell Biol 21:4347–4368

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Niimi Y, Han DS, Mori S, Kobayashi H (2003) Detection of Cucumber mosaic virus, Lily symptomless virus and Lily mottle virus in Lilium species by RT-PCR technique. Sci Hortic 97:57–63

    Article  CAS  Google Scholar 

  • Pierik R, Tholen D, Poorter H, Visser EJ, Voesenek LA (2006) The Janus face of ethylene: growth inhibition and stimulation. Trends Plant Sci 11:176–183

    Article  CAS  PubMed  Google Scholar 

  • Ramaswamy SV, Reich, RDou SJ, Jasperse L, Pan X, Wanger A, Quitugua T, Graviss EA (2003) Single nucleotide polymorphisms in genes associated with isoniazid resistance in Mycobacterium tuberculosis. Antimicrob Agents Chemother 47:1241–1250

  • Rao J, Liu D, Zhang N, He H, Ge F, Chen C (2013) Identification of genes differentially expressed in a resistant reaction to Fusarium oxysporum in Lilium regale by SSH. IERI Procedia 5:95–101

    Article  Google Scholar 

  • Reid MS, Chen JC, Jiang CZ (2009) Virus-induced gene silencing for functional characterization of genes in petunia. In: Gerats T, Strommer J (eds) petunia. Springer, New York, pp 381–394

    Chapter  Google Scholar 

  • Ryman K, Meier K, Nangle E, Ragsdale S, Korneeva N, Rhoads R, MacDonald M, Klimstra W (2005) Sindbis virus translation is inhibited by a PKR/RNase L-independent effector induced by alpha/beta interferon priming of dendritic cells. J Virol 79:1487–1499

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sánchez-Fernández R, Davies TE, Coleman JO, Rea PA (2001) The Arabidopsis thaliana ABC protein superfamily, a complete inventory. J Biol Chem 276:30231–30244

    Article  PubMed  Google Scholar 

  • Schneider E, Hunke S (1998) ATP-binding-cassette (ABC) transport systems: functional and structural aspects of the ATP-hydrolyzing subunits/domains. FEMS Microbiol Rev 22:1–20

    Article  CAS  PubMed  Google Scholar 

  • Servet C, Benhamed M, Latrasse D, Kim W, Delarue M, Zhou DX (2008) Characterization of a phosphatase 2C protein as an interacting partner of the histone acetyltransferase GCN5 in Arabidopsis. Biochim Biophys Acta (BBA) Gene Regul Mech 1779:376–382

  • Shang J, Xi DH, Xu F, Wang SD, Cao S, Xu MY, Zhao PP, Wang JH, Jia SD, Zhang ZW (2011) A broad-spectrum, efficient and nontransgenic approach to control plant viruses by application of salicylic acid and jasmonic acid. Planta 233:299–308

    Article  CAS  PubMed  Google Scholar 

  • Sharma A, Mahinghara B, Singh A, Kulshrestha S, Raikhy G, Singh L, Verma N, Hallan V, Ram R, Zaidi A (2005) Identification, detection and frequency of lily viruses in Northern India. Sci Hortic 106:213–227

    Article  Google Scholar 

  • Siljak-Yakovlev S, Peccenini S, Muratovic E, Zoldos V, Robin O, Valles J (2003) Chromosomal differentiation and genome size in three European mountain Lilium species. Plant Syst Evol 236:165–173

    Article  CAS  Google Scholar 

  • Stukkens Y, Bultreys A, Grec S, Trombik T, Vanham D, Boutry M (2005) NpPDR1, a pleiotropic drug resistance-type ATP-binding cassette transporter from Nicotiana plumbaginifolia, plays a major role in plant pathogen defense. Plant Physiol 139:341–352

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun DY, Nandety RS, Zhang YL, Reid MS, Niu LX, Jiang CZ (2016) A petunia ethylene-responsive element binding factor, PhERF2, plays an important role in antiviral RNA silencing. J Exp Bot 67:3353–3365

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tzin V, Galili G (2010) The biosynthetic pathways for shikimate and aromatic amino acids in Arabidopsis thaliana. The Arabidopsis Book, pp e0132

  • Van Tuyl J, Boon E (1997) Variation in DNA-content in the genus Lilium. Acta Hort 430:829–836

    Article  Google Scholar 

  • Verrier PJ, Bird D, Burla B, Dassa E, Forestier C, Geisler M, Klein M, Kolukisaoglu Ü, Lee Y, Martinoia E (2008) Plant ABC proteins-a unified nomenclature and updated inventory. Trends Plant Sci 13:151–159

    Article  CAS  PubMed  Google Scholar 

  • Vlachonasios KE, Thomashow MF, Triezenberg SJ (2003) Disruption mutations of ADA2b and GCN5 transcriptional adaptor genes dramatically affect Arabidopsis growth, development, and gene expression. Plant Cell 15:626–638

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang XZ, Zhang YL, Niu LX, Wu YF, Xie SL (2008) Identification of three kinds of viruses, and the preliminary evaluation on the resistance to the virus in six wild Lilium species from Qin-ba mountains under the nursery field. Sci Agri Sin 11:025

    Google Scholar 

  • Wang WK, Liu CC, Chiang TY, Chen MT, Chou CH, Yeh CH (2011) Characterization of expressed sequence tags from flower buds of alpine Lilium formosanum using a subtractive cDNA library. Plant Mol Biol Rep 29:88–97

    Article  CAS  Google Scholar 

  • Wang H, Stier G, Lin J, Liu G, Zhang Z, Chang Y, Reid MS, Jiang CZ (2013) Transcriptome changes associated with delayed flower senescence on transgenic petunia by inducing expression of etr1-1, a mutant ethylene receptor. PLoS One 8:e65800

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wek R, Jiang H, Anthony T (2006) Coping with stress: eIF2 kinases and translational control. Biochem Soc T 34:7–11

    Article  CAS  Google Scholar 

  • Won S, Eidenschenk C, Arnold CN, Siggs OM, Sun L, Brandl K, Mullen TM, Nemerow GR, Moresco EMY, Beutler B (2012) Increased susceptibility to DNA virus infection in mice with a GCN2 mutation. J Virol 86:1802–1808

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yin J, Chang X, Kasuga T, Bui M, Reid M, Jiang CZ (2015) A basic helix-loop-helix transcription factor, PhFBH4, regulates flower senescence by modulating ethylene biosynthesis pathway in petunia. Hortic Res 2:15059

    Article  PubMed  PubMed Central  Google Scholar 

  • Yuan L, Liu Q, Liu Q (2011) Conservation, evaluation and enhancement of wild lily germplasm in China. Acta Hort 900:53–57

    Article  Google Scholar 

  • Zeng WQ, Brutus A, Kremer JM, Withers JC, Gao XL, Jones AD, He SY (2011) A genetic screen reveals Arabidopsis stomatal and/or apoplastic defenses against Pseudomonas syringae pv. tomato DC3000. PLoS Pathog 7:e1002291

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang YH, Wang YF, Kanyuka K, Parry MA, Powers SJ, Halford NG (2008) GCN2-dependent phosphorylation of eukaryotic translation initiation factor-2α in Arabidopsis. J Exp Bot 59:3131–3141

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang N, Liu D, Zheng W, He H, Ji B, Han Q, Ge F, Chen C (2014) A bZIP transcription factor, LrbZIP1, is involved in Lilium regale Wilson defense responses against Fusarium oxysporum f. sp. lilii. Genes Genom 36:789–798

    Article  CAS  Google Scholar 

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Acknowledgments

We thank Min Jin and Xuhong Zhang for experimental assistance in inoculation with B. cinerea. We are grateful to Weixing Shan’s favor for conducting some of the experiments in his laboratory. We appreciate Ran Wan for kindly providing B. cinerea strains. This study was partially supported by The National High Technology Research and Development Program (863 Program) of China (Grant no. 2011AA100208) and United States Department of Agriculture (USDA) CRIS project 5306-21000-019-00D.

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    Authors and Affiliations

    1. College of Landscape Architecture and Arts, Northwest A&F University, Yangling, Shaanxi, 712100, People’s Republic of China

      Daoyang Sun, Xinguo Zhang, Shaohua Li, Yanlong Zhang & Lixin Niu

    2. Crops Pathology and Genetic Research Unit, United States Department of Agriculture, Agricultural Research Service, Davis, CA, 95616, USA

      Cai-Zhong Jiang

    3. Department of Plant Sciences, University of California at Davis, Davis, CA, 95616, USA

      Cai-Zhong Jiang

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    1. Daoyang Sun
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    2. Xinguo Zhang
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    3. Shaohua Li
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    4. Cai-Zhong Jiang
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    5. Yanlong Zhang
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    Correspondence to Cai-Zhong Jiang, Yanlong Zhang or Lixin Niu.

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    Daoyang Sun and Xinguo Zhang contributed equally to this work.

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    Sun, D., Zhang, X., Li, S. et al. LrABCF1, a GCN-type ATP-binding cassette transporter from Lilium regale, is involved in defense responses against viral and fungal pathogens. Planta 244, 1185–1199 (2016). https://doi.org/10.1007/s00425-016-2576-5

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