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Large-scale gene gains and losses molded the NLR defense arsenal during the Cucurbita evolution

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Large-scale gene gains and losses molded the NLR defense arsenal during the Cucurbita evolution

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Andolfo, G.; Sáez-Sánchez, C.; Cañizares Sales, J.; Picó Sirvent, MB.; Ercolano, MR. (2021). Large-scale gene gains and losses molded the NLR defense arsenal during the Cucurbita evolution. Planta. 254(4):1-14. https://doi.org/10.1007/s00425-021-03717-x

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Title: Large-scale gene gains and losses molded the NLR defense arsenal during the Cucurbita evolution
Author: Andolfo, Guisseppe Sáez-Sánchez, Cristina Cañizares Sales, Joaquín Picó Sirvent, María Belén Ercolano, Maria R.
UPV Unit: Universitat Politècnica de València. Departamento de Biotecnología - Departament de Biotecnologia
Issued date:
Abstract:
[EN] Main conclusion Genome-wide annotation reveals that the gene birth-death process of the Cucurbita R family is associated with a species-specific diversification of TNL and CNL protein classes. The Cucurbitaceae family ...[+]
Subjects: Diversifying selection , Orthology relations , Phylogeny , R-genes , Transcriptomes
Copyrigths: Reconocimiento (by)
Source:
Planta. (issn: 0032-0935 )
DOI: 10.1007/s00425-021-03717-x
Publisher:
Springer-Verlag
Publisher version: https://doi.org/10.1007/s00425-021-03717-x
Project ID:
info:eu-repo/grantAgreement/GENERALITAT VALENCIANA//PROMETEO%2F2017%2F078//SELECCION DE VARIEDADES TRADICIONALES Y DESARROLLO DE NUEVAS VARIEDADES DE CUCURBITACEAS ADAPTADAS A LA PRODUCCION ECOLOGICA./
info:eu-repo/grantAgreement/AGENCIA ESTATAL DE INVESTIGACION//RTA2017-00061-C03-03//AVANCES EN EL CONTROL DE LOS VIRUS TOLCNDV Y CGMMV EN CUCURBITACEAS MEDIANTE MEJORA GENÉTICA/
Thanks:
Open access funding provided by Universita degli Studi di Napoli Federico II within the CRUI-CARE Agreement.
Type: Artículo

References

Andolfo G, Ercolano MR (2015) Plant innate immunity multicomponent model. Front Plant Sci 6:987. https://doi.org/10.3389/fpls.2015.00987

Andolfo G, Sanseverino W, Rombauts S et al (2013) Overview of tomato (Solanum lycopersicum) candidate pathogen recognition genes reveals important Solanum R locus dynamics. New Phytol 197:223–237. https://doi.org/10.1111/j.1469-8137.2012.04380.x

Andolfo G, Ferriello F, Tardella L et al (2014a) Tomato genome-wide transcriptional responses to Fusarium wilt and Tomato Mosaic Virus. PLoS ONE 9(5):e94963. https://doi.org/10.1371/journal.pone.0094963 [+]
Andolfo G, Ercolano MR (2015) Plant innate immunity multicomponent model. Front Plant Sci 6:987. https://doi.org/10.3389/fpls.2015.00987

Andolfo G, Sanseverino W, Rombauts S et al (2013) Overview of tomato (Solanum lycopersicum) candidate pathogen recognition genes reveals important Solanum R locus dynamics. New Phytol 197:223–237. https://doi.org/10.1111/j.1469-8137.2012.04380.x

Andolfo G, Ferriello F, Tardella L et al (2014a) Tomato genome-wide transcriptional responses to Fusarium wilt and Tomato Mosaic Virus. PLoS ONE 9(5):e94963. https://doi.org/10.1371/journal.pone.0094963

Andolfo G, Jupe F, Witek K et al (2014b) Defining the full tomato NB-LRR resistance gene repertoire using genomic and cDNA RenSeq. BMC Plant Biol 14:120. https://doi.org/10.1186/1471-2229-14-120

Andolfo G, Di Donato A, Darrudi R et al (2017) Draft of Zucchini (Cucurbita pepo L.) proteome: a resource for genetic and genomic studies. Front Genet 8:181. https://doi.org/10.3389/fgene.2017.00181

Andolfo G, Di Donato A, Chiaiese P et al (2019) Alien domains shaped the modular structure of plant NLR proteins. Genome Biol Evol 11:3466–3477. https://doi.org/10.1093/gbe/evz248

Andolfo G, Villano C, Errico A et al (2020) Inferring RPW8-NLRs’s evolution patterns in seed plants: case study in Vitis vinifera. Planta 251:32. https://doi.org/10.1007/s00425-019-03324-x

Andolfo G, D’agostino N, Frusciante L, Ercolano MR (2021) The tomato interspecific NB-LRR gene arsenal and its impact on breeding strategies. Genes (basel) 12:1–12. https://doi.org/10.3390/genes12020184

Bailey TL, Williams N, Misleh C, Li WW (2006) MEME: Discovering and analyzing DNA and protein sequence motifs. Nucl Acids Res 34:369–373. https://doi.org/10.1093/nar/gkl198

Barchi L, Pietrella M, Venturini L et al (2019) A chromosome-anchored eggplant genome sequence reveals key events in Solanaceae evolution. Sci Rep 9:11769. https://doi.org/10.1038/s41598-019-47985-w

Barrera-Redondo J, Ibarra-Laclette E, Vázquez-Lobo A et al (2019) The genome of Cucurbita argyrosperma (silver-seed gourd) reveals faster rates of protein-coding gene and long noncoding RNA turnover and neofunctionalization within Cucurbita. Mol Plant 12:506–520. https://doi.org/10.1016/j.molp.2018.12.023

Barrera-Redondo J, Sánchez-de la Vega G, Aguirre-Liguori JA et al (2021) The domestication of Cucurbita argyrosperma as revealed by the genome of its wild relative. Hortic Res 8:109. https://doi.org/10.1038/s41438-021-00544-9

Bayer PE, Edwards D, Batley J (2018) Bias in resistance gene prediction due to repeat masking. Nat Plants 4:762–765. https://doi.org/10.1038/s41477-018-0264-0

Blanca J, Cañizares J, Roig C et al (2011) Transcriptome characterization and high throughput SSRs and SNPs discovery in Cucurbita pepo (Cucurbitaceae). BMC Genom 12:104. https://doi.org/10.1186/1471-2164-12-104

Bonardi V, Tang S, Stallmann A et al (2017) Correction: Expanded functions for a family of plant intracellular immune receptors beyond specific recognition of pathogen effectors. Proc Natl Acad Sci USA 108:16463–16468. https://doi.org/10.1073/pnas.1620070114

Capuozzo C, Formisano G, Iovieno P et al (2017) Inheritance analysis and identification of SNP markers associated with ZYMV resistance in Cucurbita pepo. Mol Breed 37:99. https://doi.org/10.1007/s11032-017-0698-5

Castellanos-Morales G, Paredes-Torres LM, Gámez N et al (2018) Historical biogeography and phylogeny of Cucurbita: insights from ancestral area reconstruction and niche evolution. Mol Phylogenet Evol 128:38–54. https://doi.org/10.1016/j.ympev.2018.07.016

D’Esposito D, Cappetta E, Andolfo G et al (2019) Deciphering the biological processes underlying tomato biomass production and composition. Plant Physiol Biochem 143:50–60. https://doi.org/10.1016/j.plaphy.2019.08.010

De Bie T, Cristianini N, Demuth JP, Hahn MW (2006) CAFE: a computational tool for the study of gene family evolution. Bioinformatics 22:1269–1271. https://doi.org/10.1093/bioinformatics/btl097

Delport W, Poon AFY, Frost SDW, Kosakovsky Pond SL (2010) Datamonkey 2010: a suite of phylogenetic analysis tools for evolutionary biology. Bioinformatics 26:2455–2457. https://doi.org/10.1093/bioinformatics/btq429

Di Donato A, Andolfo G, Ferrarini A et al (2017) Investigation of orthologous pathogen recognition gene-rich regions in solanaceous species. Genome 60:850–859. https://doi.org/10.1139/gen-2016-0217

Dogimont C, Chovelon V, Pauquet J et al (2014) The Vat locus encodes for a CC-NBS-LRR protein that confers resistance to Aphis gossypii infestation and A. gossypii-mediated virus resistance. Plant J 80:993–1004. https://doi.org/10.1111/tpj.12690

Finn RD, Clements J, Eddy SR (2011) HMMER web server: interactive sequence similarity searching. Nucleic Acids Res 39:29–37. https://doi.org/10.1093/nar/gkr367

Garcia-Mas J, Benjak A, Sanseverino W et al (2012) The genome of melon (Cucumis melo L.). Proc Natl Acad Sci USA 109:11872–11877. https://doi.org/10.1073/pnas.1205415109

Guo YL, Fitz J, Schneeberger K et al (2011) Genome-wide comparison of nucleotide-binding site-leucine-rich repeat-encoding genes in Arabidopsis. Plant Physiol 157:757–769. https://doi.org/10.1104/pp.111.181990

Guo J, Xu W, Hu Y et al (2020) Phylotranscriptomics in Cucurbitaceae reveal multiple whole-genome duplications and key morphological and molecular innovations. Mol Plant 13:1117–1133. https://doi.org/10.1016/j.molp.2020.05.011

Han MV, Thomas GWC, Lugo-Martinez J, Hahn MW (2013) Estimating gene gain and loss rates in the presence of error in genome assembly and annotation using CAFE 3. Mol Biol Evol 30:1987–1997. https://doi.org/10.1093/molbev/mst100

Harris KR, Wechter WP, Levi A (2009) Isolation, sequence analysis, and linkage mapping of nucleotide binding site-leucine-rich repeat disease resistance gene analogs in watermelon. J Am Soc Hortic Sci 134:649–657. https://doi.org/10.21273/jashs.134.6.649

Jia YX, Yuan Y, Zhang Y et al (2015) Extreme expansion of NBS-encoding genes in Rosaceae. BMC Genet 16:48. https://doi.org/10.1186/s12863-015-0208-x

Jones DT, Taylor WR, Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences. Bioinformatics 8:275–282. https://doi.org/10.1093/bioinformatics/8.3.275

Jones P, Binns D, Chang HY et al (2014) InterProScan 5: genome-scale protein function classification. Bioinformatics 30:1236–1240. https://doi.org/10.1093/bioinformatics/btu031

Joobeur T, King JJ, Nolin SJ et al (2004) The fusarium wilt resistance locus Fom-2 of melon contains a single resistance gene with complex features. Plant J 39:283–297. https://doi.org/10.1111/j.1365-313X.2004.02134.x

Joshi RK, Nayak S (2013) Perspectives of genomic diversification and molecular recombination towards R-gene evolution in plants. Physiol Mol Biol Plants 19:1–9. https://doi.org/10.1007/s12298-012-0138-2

Kang YJ, Kim KH, Shim S et al (2012) Genome-wide mapping of NBS-LRR genes and their association with disease resistance in soybean. BMC Plant Biol 12:139. https://doi.org/10.1186/1471-2229-12-139

Kates HR, Soltis PS, Soltis DE (2017) Evolutionary and domestication history of Cucurbita (pumpkin and squash) species inferred from 44 nuclear loci. Mol Phylogenet Evol 111:98–109. https://doi.org/10.1016/j.ympev.2017.03.002

Katoh K, Misawa K, Kuma K, Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucl Acids Res 30:3059–3066. https://doi.org/10.1093/nar/gkf436

Khoury CK, Carver D, Kates HR et al (2020) Distributions, conservation status, and abiotic stress tolerance potential of wild cucurbits ( Cucurbita L.). Plants People Planet 2:269–283. https://doi.org/10.1002/ppp3.10085

Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054

Larkin MA, Blackshields G, Brown NP et al (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948. https://doi.org/10.1093/bioinformatics/btm404

Lin X, Zhang Y, Kuang H, Chen J (2013) Frequent loss of lineages and deficient duplications accounted for low copy number of disease resistance genes in Cucurbitaceae. BMC Genom 14:335. https://doi.org/10.1186/1471-2164-14-335

Madeira F, Park YM, Lee J et al (2019) The EMBL-EBI search and sequence analysis tools APIs in 2019. Nucl Acids Res 47:W636–W641. https://doi.org/10.1093/nar/gkz268

Marchler-Bauer A, Bryant SH (2004) CD-Search: protein domain annotations on the fly. Nucl Acids Res 32:327–331. https://doi.org/10.1093/nar/gkh454

McHale L, Tan X, Koehl P, Michelmore RW (2006) Plant NBS-LRR proteins: adaptable guards. Genome Biol 7:212. https://doi.org/10.1186/gb-2006-7-4-212

Meyers BC, Kozik A, Griego A et al (2003) Genome-wide analysis of NBS-LRR–encoding genes in Arabidopsis. Plant Cell 15:809–834. https://doi.org/10.1105/tpc.009308

Michelmore RW, Christopoulou M, Caldwell KS (2013) Impacts of resistance gene genetics, function, and evolution on a durable future. Annu Rev Phytopathol 51:291–319. https://doi.org/10.1146/annurev-phyto-082712-102334

Montero-Pau J, Blanca J, Bombarely A et al (2018) De novo assembly of the zucchini genome reveals a whole-genome duplication associated with the origin of the Cucurbita genus. Plant Biotechnol J 16:1161–1171. https://doi.org/10.1111/pbi.12860

Moreira X, Abdala-Roberts L, Gols R, Francisco M (2018) Plant domestication decreases both constitutive and induced chemical defences by direct selection against defensive traits. Sci Rep 8:12678. https://doi.org/10.1038/s41598-018-31041-0

Nguyen QM, Iswanto ABB, Son GH, Kim SH (2021) Recent advances in effector-triggered immunity in plants: new pieces in the puzzle create a different paradigm. Int J Mol Sci 22(9):4709. https://doi.org/10.3390/ijms22094709

Obrero Á, Die JV, Román B et al (2011) Selection of reference genes for gene expression studies in zucchini (Cucurbita pepo) using qPCR. J Agric Food Chem 59:5402–5411. https://doi.org/10.1021/jf200689r

Ortiz D, de Guillen K, Cesari S et al (2017) Recognition of the Magnaporthe oryzae effector AVR-Pia by the decoy domain of the rice NLR immune receptor RGA5. Plant Cell 29:156–168. https://doi.org/10.1105/tpc.16.00435

Osuna-Cruz CM, Paytuvi-Gallart A, Di Donato A et al (2018) PRGdb 3.0: a comprehensive platform for prediction and analysis of plant disease resistance genes. Nucl Acids Res 46:D1197–D1201. https://doi.org/10.1093/nar/gkx1119

Peart JR, Mestre P, Lu R et al (2005) NRG1, a CC-NB-LRR protein, together with N, a TIR-NB-LRR protein, mediates resistance against tobacco mosaic virus. Curr Biol 15:968–973. https://doi.org/10.1016/j.cub.2005.04.053

Pond KSL, Frost SDW (2005) Datamonkey: rapid detection of selective pressure on individual sites of codon alignments. Bioinformatics 21:2531–2533. https://doi.org/10.1093/bioinformatics/bti320

Renner SS, Schaefer H (2016) Phylogeny and Evolution of the Cucurbitaceae. Genet Genom Cucurbitaceae. https://doi.org/10.1007/7397_2016_14

Richly E, Kurth J, Leister D (2002) Mode of amplification and reorganization of resistance genes during recent Arabidopsis thaliana evolution. Mol Biol Evol 19:76–84. https://doi.org/10.1093/oxfordjournals.molbev.a003984

Román B, Gómez P, Picó B, Die JV (2020) The NBS-LRR gene class is a small family in Cucurbita pepo. Preprints. https://doi.org/10.20944/preprints202001.0048.v1

Sanjur OI, Piperno DR, Andres TC, Wessel-Beaver L (2002) Phylogenetic relationships among domesticated and wild species of Cucurbita (Cucurbitaceae) inferred from a mitochondrial gene: Implications for crop plant evolution and areas of origin. Proc Natl Acad Sci USA 99:535–540. https://doi.org/10.1073/pnas.012577299

Sarris PF, Cevik V, Dagdas G et al (2016) Comparative analysis of plant immune receptor architectures uncovers host proteins likely targeted by pathogens. BMC Biol 14:8. https://doi.org/10.1186/s12915-016-0228-7

Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative CT method. Nat Protoc 3:1101–1108. https://doi.org/10.1038/nprot.2008.73

Shao ZQ, Xue JY, Wu P et al (2016) Large-scale analyses of angiosperm nucleotide-binding site-leucine-rich repeat genes reveal three anciently diverged classes with distinct evolutionary patterns. Plant Physiol 170:2095–2109. https://doi.org/10.1104/pp.15.01487

Smith BD (1997) The initial domestication of Cucurbita pepo in the Americas 10,000 years ago. Science (80-) 276:932–934. https://doi.org/10.1126/science.276.5314.932

Soltis PS, Soltis DE (2016) Ancient WGD events as drivers of key innovations in angiosperms. Curr Opin Plant Biol 30:159–165. https://doi.org/10.1016/j.pbi.2016.03.015

Sun H, Wu S, Zhang G et al (2017) Karyotype stability and unbiased fractionation in the paleo-allotetraploid Cucurbita genomes. Mol Plant 10:1293–1306. https://doi.org/10.1016/j.molp.2017.09.003

Tamura K, Nei M, Kumar S (2004) Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc Natl Acad Sci USA 101:11030–11035. https://doi.org/10.1073/pnas.0404206101

Tian D, Traw MB, Chen JQ et al (2003) Fitness costs of R-gene-mediated resistance in Arabidopsis thaliana. Nature 423:74–77. https://doi.org/10.1038/nature01588

Untergasser A, Nijveen H, Rao X et al (2007) Primer3Plus, an enhanced web interface to Primer3. Nucl Acids Res 35:71–74. https://doi.org/10.1093/nar/gkm306

Wan H, Yuan W, Ye Q et al (2012) Analysis of TIR- and non-TIR-NBS-LRR disease resistance gene analogous in pepper: characterization, genetic variation, functional divergence and expression patterns. BMC Genom 13:502. https://doi.org/10.1186/1471-2164-13-502

Wang Z, Gerstein M, Snyder M (2009) RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet 10:57–63. https://doi.org/10.1038/nrg2484

Wu C-H, Derevnina L, Kamoun S (2018) Receptor networks underpin plant immunity. Science (80-) 360:1300–1301. https://doi.org/10.1126/science.aat2623

Xanthopoulou A, Montero-Pau J, Mellidou I et al (2019) Whole-genome resequencing of Cucurbita pepo morphotypes to discover genomic variants associated with morphology and horticulturally valuable traits. Hortic Res 6:94. https://doi.org/10.1038/s41438-019-0176-9

Yang S, Feng Z, Zhang X et al (2006) Genome-wide investigation on the genetic variations of rice disease resistance genes. Plant Mol Biol 62:181–193. https://doi.org/10.1007/s11103-006-9012-3

Zhang N, Zeng L, Shan H, Ma H (2012) Highly conserved low-copy nuclear genes as effective markers for phylogenetic analyses in angiosperms. New Phytol 195:923–937. https://doi.org/10.1111/j.1469-8137.2012.04212.x

Zheng Y, Wu S, Bai Y et al (2019) Cucurbit Genomics Database (CuGenDB): a central portal for comparative and functional genomics of cucurbit crops. Nucl Acids Res 47:D1128–D1136. https://doi.org/10.1093/nar/gky944s

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