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Gene coding for an elongation factor is involved in resistance against powdery mildew in common bean

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Genetic control of the resistance response against powdery mildew in common bean was studied combining genetic, genomic and transcriptomic analyses. A candidate resistance gene in cultivar Porrillo Sintetico was proposed.

Abstract

The species causing the fungal disease powdery mildew (PM) in the local common bean crop was identified as Erysiphe polygoni through the molecular analysis of the internal transcribed spacer region. A genetic analysis of the resistance in cultivar Porrillo Sintetico was conducted using different F2:3 populations, and a dominant gene conferring total resistance against a local PM isolate was physically located between 84,188 and 218,664 bp of chromosome Pv04. An in silico analysis of this region, based on the common bean reference sequence, revealed four genes candidate to be involved in the resistance reaction. Relative expression levels of these genes after PM infection showed a significant over-expression of the candidate gene Phvul.004G001500 in the resistant genotype Porrillo Sintetico. This gene was re-sequenced in the parental genotypes X2776 and Porrillo Sintetico to explain their different phenotypic responses against PM. Several substitutions where identified in exon regions, all of them synonymous, so differences in the produced amino acid sequence were not expected. However, a total of 37 mutations were identified in non-coding regions of the gene sequence, suggesting that intron variation could be responsible for the different gene expression levels after PM infection. No evidence of other regulatory mechanisms, such as alternative splicing or methylation, was identified. Candidate resistance gene Phvul.004G001500 codes for an elongation factor that is not a typical gene related to recognition of specific pathogens in plants, suggesting its involvement in the resistance through plant immune system.

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References

  • Almeida AMR, Binneck E, Piuga FF, Marin SRR, Ribeiro do Valle PRZ, Silveira CA (2008) Characterization of powdery mildews strains from soybean, bean, sunflower, and weeds in Brazil using rDNA-ITS sequences. Trop Plant Pathol 33:20–26

    Article  Google Scholar 

  • Bilas R, Szafran K, Hnatuszko-Konka, Kononowicz (2016) Cis-regulatory elements used to control gene expression in plants. Plant Cell Tiss Organ Cult 127:269–287

    Article  CAS  Google Scholar 

  • Borges A, Tsai SM, Caldas DGG (2012) Validation of reference genes for RT-qPCR normalization in common bean during biotic and abiotic stresses. Plant Cell Rep 31:827–838

    Article  CAS  PubMed  Google Scholar 

  • Broughton WJ, Hernández G, Blair M, Beebe S, Gepts P, Vanderleyden J (2003) Bean (Phaseolus spp.)—model food legumes. Plant Soil 252:55–128

    Article  CAS  Google Scholar 

  • Büschges R, Hollricher K, Panstruga R, Simons G, Wolter M, Frijters A et al (1997) The barley Mlo gene: a novel control element of plant pathogen resistance. Cell 88:695–705

    Article  PubMed  Google Scholar 

  • Campa A, Rodríguez-Suárez C, Giraldez R, Ferreira JJ (2014) Genetic analysis of the response to eleven Colletotrichum lindemuthianum races in a RIL population of common bean (Phaseolus vulgaris L.). BMC Plant Biol 14:115

    Article  PubMed  PubMed Central  Google Scholar 

  • Chinnusamy V, Zhu J-K (2009) Epigenetic regulation of stress responses in plants. Curr Opin Plant Biol 12:133–139

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chung E, Cho CW, So HA, Yun BH, Lee JH (2009) Differential expression of soybean SLTI100 gene encoding translation elongation factor 1 A by abiotic stresses. J Plant Biotechnol 36:255–260

    Article  Google Scholar 

  • Colot V, Rossignol J-L (1999) Eukaryotic DNA methylation as an evolutionary device. Bioessays 21:42–411

    Article  Google Scholar 

  • Condeelis J (1995) Elongation factor 1 alpha, translation and the cytoskeleton. Trends Biochem Sci 20:169–170

    Article  CAS  PubMed  Google Scholar 

  • Dangl JL, Jones JDG (2001) Plant pathogens and integrated defense responses to infection. Nature 411:826–833

    Article  CAS  PubMed  Google Scholar 

  • David P, Chen NWG, Pedrosa-Harand A, Thareau V, Sévignac M, Cannon SB et al (2009) A nomadic subtelomeric disease resistance gene cluster in common bean. Plant Physiol 151:1048–1065

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dinesh-Kumar SP, Baker BJ (2000) Alternatively spliced N resistance gene transcripts: their possible role in tobacco mosaic virus resistance. Proc Natl Acad Sci USA 97:1908–1913

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dodds PN, Rathjen JP (2010) Plant immunity: towards an integrated view of plant–pathogen interactions. Nat Rev Genet 11:539–548

    Article  CAS  PubMed  Google Scholar 

  • Dowen RH, Pelizzola M, Schmitz RJ, Lister R, Dowen JM, Nery JR et al (2012) Widespread dynamic DNA methylation in response to biotic stress. Proc Natl Acad Sci USA 109:e2183–e2191

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dundas B (1936) Inheritance of resistance to powdery mildew in beans. Hilgardia 10:243–253

    Article  Google Scholar 

  • Dundas B (1941) Further studies on the inheritance of resistance to powdery mildews of beans. Hilgardia 13:551–565

    Article  Google Scholar 

  • Eichmann R, Hückelhoven R (2008) Accommodation of powdery mildew fungi in intact plant cells. J Plant Physiol 165:5–18

    Article  CAS  PubMed  Google Scholar 

  • Ejiri S (2002) Moonlighting functions bundling to zinc finger of polypeptide elongation factor 1: from actin protein Rl-associated nuclear localization. Biosci Biotechnol Biochem 66:1–21

    Article  CAS  PubMed  Google Scholar 

  • FAO (1999). Database. http://www.fao.org/3/a-av015e.pdf

  • Ferreira JJ, Campa A, Kelly JD (2013) Organization of genes conferring resistance to anthracnose in common bean. In: Varshney RK, Tuberosa R (eds) Translational genomics for crop breeding: biotic stress, vol 1. Wiley, pp 151–182.

  • Ferrier-Cana E, Geffroy V, Macadré C, Creusot F, Imbert-Bollore P, Sévignac M et al (2003) Characterization of expressed NBS-LRR resistance gene candidates from common bean. Theor Appl Genet 106:251–261

    Article  CAS  PubMed  Google Scholar 

  • Fiume E, Christou P, Giani S, Breviario D (2004) Introns are key regulatory elements of rice tubulin expression. Planta 218:693–703

    Article  CAS  PubMed  Google Scholar 

  • Fritzemeier K-H, Cretin C, Kombrink E, Rohwer F, Taylor J, Scheel D et al (1987) Transient induction of phenylalanine ammonia-lyase and 4-coumarate: CoA ligase mRNAs in potato leaves infected with virulent or avirulent races of Phytophthora infestans. Plant Physiol 85:34–41

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fu J, Momcilovic I, Prasad PVV (2012) Roles of protein synthesis elongation factor EF-Tu in heat tolerance in plants. J Bot. doi:10.1155/2012/835836

    Google Scholar 

  • Furukawa T, Inagaki H, Takai R, Hirai H, Che F-S (2014) Two distinct EF-Tu epitopes induce immune responses in rice and Arabidopsis. MPMI 27:113–124

    Article  CAS  PubMed  Google Scholar 

  • Glawe DA (2008) The powdery mildews. A review of the world’s most familiar (yet poorly known) plant pathogens. Ann Rev Phytopathol 46:27–51

    Article  CAS  Google Scholar 

  • Goodstein DM, Shu S, Howson R, Neupane R, Hayes RD, Fazo J et al (2012) Phytozome: a comparative platform for green plant genomics. Nucl Acids Res 40:1–9

    Article  Google Scholar 

  • Gross SR, Kinzy TG (2005) Translation elongation factor 1 A is essential for regulation of the actin cytoskeleton and cell morphology. Nat Struct Mol Biol 12:772–778

    Article  CAS  PubMed  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Heath MC (2000) Nonhost resistance and nonspecific plant defenses. Curr Opin Plant Biol 3:315–319

    Article  CAS  PubMed  Google Scholar 

  • Hnatuszko-Konka K, Kowalczyk T, Gerszberg A, Wiktorek-Smagur A, Kononowicz AK (2014) Phaseolus vulgaris-recalcitrant potential. Biotechnol Adv 32:1205–1215

    Article  PubMed  Google Scholar 

  • Hückelhoven R (2005) Powdery mildew susceptibility and biotrophic infection strategies. FEMS Microbiol Lett 245:9–17

    Article  PubMed  Google Scholar 

  • Hückelhoven R, Panstruga R (2011) Cell biology of the plant-powdery mildew interaction. Curr Opin Plant Biol 14:738–746

    Article  PubMed  Google Scholar 

  • Janda M, Matousková J, Burketová L, Valentová O (2014) Interconnection between actin cytoskeleton and plant defense signaling. Plant Signal Behav 9:e976486

    Article  PubMed  PubMed Central  Google Scholar 

  • Jones JDG, Dangl JL (2006) The plant immune system. Nature 444:323–329

    Article  CAS  PubMed  Google Scholar 

  • Jordan T, Schornack S, Lahaye T (2002) Alternative splicing of transcripts encoding Toll-like plant resistance proteins—what’s the functional relevance to innate immunity? Trends Plant Sci 7:392–398

    Article  CAS  PubMed  Google Scholar 

  • Kõljalg U, Nilsson RH, Abarenkov K, Tedersoo L, Taylor AF, Bahram M et al (2013) Towards a unified paradigm for sequence-based identification of fungi. Mol Ecol 22:5271–5277

    Article  PubMed  Google Scholar 

  • Kunze G, Zipfel C, Robarzek S, Niehaus K, Boller T, Felix G (2004) The N terminus of bacterial elongation factor Tu elicits innate immunity in Arabidopsis plants. Plant Cell 16:3496–3507

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lacombe S, Rougon-Cardoso A, Sherwood E, Peeters N, Dahlbeck D, van Esse HP et al (2010) Interfamily transfer of a plant pattern-recognition receptor confers broad-spectrum bacterial resistance. Nat Biotechnol 28:365–369

    Article  CAS  PubMed  Google Scholar 

  • Lander ES, Green P, Abrahamson J, Baarlow A, Daly MJ, Lincoln SE, et al (1987) MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1:174–181

    Article  CAS  PubMed  Google Scholar 

  • Li LC, Dahiya R (2002) MethPrimer: designing primers for methylation PCRs. Bioinformatics 18:1427–1431

    Article  CAS  PubMed  Google Scholar 

  • Li L, Hong H, Luan G, Mosel M, Malik M, Drlica K, et al (2014) Ribosomal elongation factor 4 promotes cell death associated with lethal stress. mBio 5:e01708–14

    CAS  PubMed  PubMed Central  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2–∆∆Ct method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Lu F, Wang H, Wang S, Jiang W, Shan C, Yang J et al (2015) Enhancement of innate immune system in monocot rice by transferring the dicotyledonous elongation factor Tu receptor EFR. JIPB 57:641–652

    CAS  PubMed  Google Scholar 

  • Marone D, Russo MA, Laido G, Leonardis AM, Mastrangelo AM (2013) Plant nucleotide binding site-leucine-rich repeat (NBS-LRR) genes: active guardians in host defense response. Int J Mol Sci 14:7302–7326

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mascarenhas D, Mettler IJ, Pierce DA, Lowe HW (1990) Intron-mediated enhancement of heterologous gene expression in maize. Plant Mol Biol 15:913–920

    Article  CAS  PubMed  Google Scholar 

  • Meziadi C, Richard MMS, Derquennes A, Thareau V, Blanchet S, Gratias A et al (2016) Development of molecular markers linked to disease resistance genes in common bean based on whole genome sequence. Plant Sci 242:351–357

    Article  CAS  PubMed  Google Scholar 

  • Moghaddam SM, Song Q, Mamidi S, Schmutz J, Lee R, Cregan P et al (2014) Developing market class specific InDel markers from next generation sequence data in Phaseolus vulgaris L. Front Plant Sci 5:185

    Article  PubMed  PubMed Central  Google Scholar 

  • Morales FJ, Singh SP (1991) Genetics of resistance to bean golden mosaic virus inPhaseolus vulgarisL. Euphytica 52:113–117

    Google Scholar 

  • Muktar MS, Lübeck J, Strahwald J, Gebhardt C (2015) Selection and validation of potato candidate genes for maturity corrected resistance to Phytophthora infestans based on differential expression combined with SNP association and linkage mapping. Front Genet 6:294

    Article  PubMed  PubMed Central  Google Scholar 

  • Nilsson RH, Ryberg M, Kristiansson E, Abarenkov K, Larsson K-H, Kõljalg U (2006) Taxonomic reliability of DNA sequences in public sequence databases: a fungal perspective. Plos One 1:e59

    Article  PubMed  PubMed Central  Google Scholar 

  • Panduranga S, Diapari M, Yin F, Munholland S, Perry GE, Chapman BP et al (2016) Genomic analysis of storage protein deficiency in genetically related lines of common bean (Phaseolus vulgaris). Front Plant Sci 7:389

    Google Scholar 

  • Pérez-Vega E, Trabanco N, Campa A, Ferreira JJ (2013) Mapping of two genes conferring resistance to powdery mildew in common bean (Phaseolus vulgaris L.). Theor Appl Genet 126:1503–1512

    Article  PubMed  Google Scholar 

  • Rezende VF, Patto RMA, Corte H (1999) Genetic control of common bean (Phaseolus vulgaris L.) resistance to powdery mildew (Erysiphe polygoni). Genet Mol Biol 22:233–236

    Article  Google Scholar 

  • Ristic Z, Bukovnik U, Momčilović I, Fu J, Vara Prasad PV (2008) Heat-induced accumulation of chloroplast protein synthesis elongation factor, EF-Tu, in winter wheat. J Plant Physiol 165:192–202

    Article  CAS  PubMed  Google Scholar 

  • Sasikumar AN, Perez WB, Kinzy TG (2012) The many roles of the Eukaryotic elongation factor 1 complex. Wiley Interdiscip Rev. RNA 3(4):543–555

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schmutz J, McClean PE, Mamidi S, Wu GA, Cannon SB, Grimwood J et al (2014) A reference genome for common bean and genome-wide analysis of dual domestications. Nat Genet 46:707–713

    Article  CAS  PubMed  Google Scholar 

  • Schoch CL, Seifert KA, Huhndorf S, Robert V, Spouge JL, Levesque CA et al (2012) Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. Proc Natl Acad Sci USA 109:6241–6246

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schoonbeek HJ, Wang HH, Stefanato FL, Craze M, Bowden S, Wallington E et al (2015) Arabidopsis EF-Tu receptor enhances bacterial disease resistance in transgenic wheat. New Phytol 206:606–613

    Article  CAS  PubMed  Google Scholar 

  • Schwartz HF, Katherman MJ, Thung MDT (1981) Yield response and resistance of dry beans to powdery mildew in Colombia. Plant Dis 65:737–738

    Article  Google Scholar 

  • Schwartz HF, Steadman JR, Hall R, Forster RL (2005) Compendium of bean diseases. 2nd edition. The American Phytopathology Society, pp 36–37

  • Simpson GG, Filipowicz W (1996) Splicing of precursors to mRNA in higher plants: mechanism, regulation and sub-nuclear organisation of the spliceosomal machinery. Plant Mol Biol 32:1–41

    Article  CAS  PubMed  Google Scholar 

  • Singh BN, Mishra RN, Agarwal PK, Goswami M, Nair S, Sopory SK et al (2004) A pea chloroplast translation elongation factor that is regulated by abiotic factors. Biochem Biophys Res Commun 320:523–530

    Article  CAS  PubMed  Google Scholar 

  • Somssich IE, Schmelzer E, Bollmann J, Hahlbrock K (1986) Rapid activation by fungal elicitor of genes encoding “pathogenesis-related” proteins in cultured parsley cells. Proc Natl Acad Sci USA 83:2427–2430

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takemoto D, Hardham AR (2004) The cytoskeleton as a regulator and target of biotic interactions in plants. Plant Physiol 136:3864–3876

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Trabanco N, Pérez-Vega E, Campa A, Rubiales D, Ferreira JJ (2012) Genetic resistance to powdery mildew in common bean. Euphytica 186:875–882

    Article  Google Scholar 

  • Vlasova A, Capella-Gutiérrez S, Rendón-Anaya M, Hernández-Oñate M, Minoche AE, Erb I et al (2016) Genome and and transcriptome analysis of the Mesoamerican common bean and the role of gene duplications in establishing tissue and temporal specialization of genes. Genome Biol 17:32

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang WM, Wen YQ, Berkey R, Xiao SY (2009) Specific targeting of the Arabidopsis resistance protein RPW8.2 to the interfacial membrane encasing the fungal haustorium renders broad-spectrum resistance to powdery mildew. Plant Cell 21:2898–2913

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • White TJ, Bruns TD, Lee SB, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis DH, Gelfand DH, Sinsky JJ, White TJ (eds) PCR - Protocols and applications. Academic Press, New York, pp 315–322

    Google Scholar 

  • Xiao SY, Ellwood S, Calis O, Patrick E, Li TX, Coleman M, Turner JG (2001) Broad-spectrum mildew resistance in Arabidopsis thaliana mediated by RPW8. Science 291:118–120

    Article  CAS  PubMed  Google Scholar 

  • Yoder JA, Walsh CP, Bestor TH (1997) Cytosine methylation and the ecology of intragenomic parasites. Trends Genet 13:335–340

    Article  CAS  PubMed  Google Scholar 

  • You FM, Huo N, Gu YQ, Luo M, Ma Y, Hane D et al (2008) BatchPrimer3: a high throughput web application for PCR and sequencing primer design. BMC Bioinform 9:253

    Article  Google Scholar 

  • Young ND (2000) The genetic architecture of resistance. Curr Opin Plant Biol 3:285–290

    Article  CAS  PubMed  Google Scholar 

  • Zipfel C, Kunze G, Chinchilla D, Caniard A, Jones JDG, Boller T et al (2006) Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell 125:749–760

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This work was supported by Grant RTA2012-0052 from INIA- Ministerio Economía y Competitividad (Spanish Government), cofinanced from FEDER funds. Ana Campa is recipient of a salary from the Instituto de Investigación y Tecnología Agraria y Alimentaria INIA-CCAA (DR13-0222), Spain. Authors thank Marcos Bueno for his technical assistance and the help of DREAMgenics S.L. (Asturias, Spain) in the genomic interpretation of the common bean sequences.

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  1. Plant Genetics, Area of Horticultural and Forest Crops, SERIDA, Asturias, Spain

    Ana Campa & Juan José Ferreira

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  1. Ana Campa
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Correspondence to Ana Campa.

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Communicated by David A. Lightfoot.

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Campa, A., Ferreira, J.J. Gene coding for an elongation factor is involved in resistance against powdery mildew in common bean. Theor Appl Genet 130, 849–860 (2017). https://doi.org/10.1007/s00122-017-2864-x

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