Abstract
Main conclusion
Genomic and transcriptomic studies in plants and, more in deep, in grapevine reveal that the disease-resistance RNL gene family is highly variable.
Abstract
RNLs (RPW8-NLRs) are a phylogenetically distinct class of nucleotide oligomerization domain (NOD)-like receptors (NLRs) identified in plants. Two RNLs, namely, the NRG1 (N Requirement Gene 1) and the ADR1 (Activated Disease Resistance 1), have been characterized; however, little is known about the RNL evolutionary history in higher plants. To trace the diversification of RNL gene subfamily, we scanned the NLR proteins of 73 plant genomes belonging to 29 taxa, revealing a noticeable diversification across species and within the same genus or botanic family together with a conspicuous expansion in important crop species. To explore the RNL variability in Vitis vinifera and gain information with respect to their structure, evolutionary diversification of five grape genomes (‘Aglianico’, ‘Falanghina’, ‘Sultanina’, ‘Tannat’, and ‘Nebbiolo’) has been compared to the reference genome (‘Pinot Noir’). The number of RNLs ranged from 6 (‘Sultanina’) to 14 (‘Nebbiolo’), in contrast to the 10 ‘Pinot Noir’ RNLs. The phylogenetic study on grapevine RNLs revealed that all collapsed into NRG1-clade, rather than four. To investigate more in depth the means of intraspecific variability of grape RNL copies, a transcriptomic profiling in response to powdery mildew (PM) infection was carried out through qRT-PCRs and public databases interrogation. The RNL expression variability identified in transcriptome data sets supports the hypothesis of a functional expansion/contraction in grapevine varieties. Although no direct correlations between grapevine PM-resistance and RNL expression was identified, our work can provide good candidates for functional studies able to elucidate the putative “helper” role of RNLs in grape immune signalling.
Similar content being viewed by others
Abbreviations
- ADR1:
-
Activated disease resistance 1
- NLRs:
-
Nucleotide oligomerization domain (NOD)-like receptors
- NRG1:
-
N Requirement gene 1
- PM:
-
Powdery mildew
- RNLs:
-
RPW8-NB-LRR
- RPW8:
-
Resistance-to-powdery mildew 8
References
Amrine KC, Blanco-Ulate B, Riaz S et al (2015) Comparative transcriptomics of central Asian Vitis vinifera accessions reveals distinct defense strategies against powdery mildew. Hortic Res 2:15037. https://doi.org/10.1038/hortres.2015.37
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(1):223–237. https://doi.org/10.1111/j.1469-8137.2012.04380.x
Andolfo G, Sanseverino W, Aversano R, Frusciante L, Ercolano MR (2014a) Genome-wide identification and analysis of candidate genes for disease resistance in tomato. Mol Breed 33:227–233. https://doi.org/10.1007/s11032-013-9928-7
Andolfo G, Jupe F, Witek K, Etherington GJ, Ercolano MR, Jones JD (2014b) Defining the full tomato NB-LRR resistance gene repertoire using genomic and cDNA RenSeq. BMC Plant Biol 14(1):120. https://doi.org/10.1186/1471-2229-14-120
Andolfo G, Ruocco M, Di Donato A, Frusciante L, Lorito M, Scala F, Ercolano MR (2015) Genetic variability and evolutionary diversification of membrane ABC transporters in plants. BMC Plant Biol 15(1):51. https://doi.org/10.1186/s12870-014-0323-2
Andolfo G, Di Donato A, Darrudi R, Errico A, Aiese Cigliano R, Ercolano MR (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, Donato AD, Chiaiese P et al (2019) Alien domains shaped the modular structure of plant NLR proteins. Genome Biol Evol. https://doi.org/10.1093/gbe/evz248
Babicki S, Arndt D, Marcu A, Liang Y, Grant JR, Maciejewski A, Wishart DS (2016) Heatmapper: web-enabled heat mapping for all. Nucleic Acids Res 44(W1):W147–W153. https://doi.org/10.1093/nar/gkw419
Baggs E, Dagdas G, Krasileva KV (2017) NLR diversity, helpers and integrated domains: Making sense of the NLR Identity. Curr Opin Plant Biol 38:59–67. https://doi.org/10.1016/j.pbi.2017.04.012
Barragan CA, Wu R, Kim ST (2019) RPW8/HR repeats control NLR activation in Arabidopsis thaliana. PLoS Gen 15(7):e1008313. https://doi.org/10.1371/journal.pgen.1008313
Bonardi V, Tang S, Stallmann A, Roberts M, Cherkis KA, Dangl JL (2011) Expanded functions for a family of plant intracellular immune receptors beyond specific recognition of pathogen effectors. P Natl Acad Sci USA 108:16463–16468. https://doi.org/10.1073/pnas.1113726108
Brulé D, Villano C, Davies LJ et al (2019) The grapevine (Vitis vinifera) LysM receptor kinases VvLYK1-1 and VvLYK1-2 mediate chitooligosaccharide-triggered immunity. Plant Biotechnol J 17(4):812–825. https://doi.org/10.1111/pbi.13017
Castel B, Ngou PM, Cevik V et al (2019) Diverse NLR immune receptors activate defence via the RPW8-NLR NRG-1. New Phytol 222(2):966–980. https://doi.org/10.1111/nph.15659
Collier SM, Hamel LP, Moffett P (2011) Cell death mediated by the N-terminal domains of a unique and highly conserved class of NB-LRR protein. Mol Plant Microbe In 24(8):918–931. https://doi.org/10.1094/MPMI-03-11-0050
Da Silva C, Zamperin G, Ferrarini A et al (2013) The high polyphenol content of grapevine cultivar Tannat berries is conferred primarily by genes that are not shared with the reference genome. Plant Cell 25:4777–4788. https://doi.org/10.1105/tpc.113.118810
Di Genova A, Almeida AM, Muñoz-Espinoza C et al (2014) Whole genome comparison between table and wine grapes reveals a comprehensive catalog of structural variants. BMC Plant Biol 14(1):7. https://doi.org/10.1186/1471-2229-14-7
Di Meo F, Aversano R, Diretto G et al (2019) Anti-cancer activity of grape seed semi-polar extracts in human mesothelioma cell lines. J Funct Foods 61:103515. https://doi.org/10.1016/j.jff.2019.103515
Donald TM, Pellerone F, Adam-Blondon AF, Bouquet A, Thomas MR, Dry IB (2002) Identification of resistance gene analogs linked to a powdery mildew resistance locus in grapevine. Theor Appl Genet 104(4):610–618. https://doi.org/10.1007/s00122-001-0768-1
Dybas JM, Fiser A (2016) Development of a motif-based topology-independent structure comparison method to identify evolutionarily related folds. Proteins 84(12):1859–1874. https://doi.org/10.1002/prot.25169
Esposito S, Aversano R, Bradeen JM, Di Matteo A, Villano C, Carputo D (2018a) Deep-sequencing of Solanum commersonii small RNA libraries reveals riboregulators involved in cold stress response. Plant Biol. https://doi.org/10.1111/plb.12955
Esposito S, Aversano R, D’Amelia V, Villano C, Alioto D, Mirouze M, Carputo D (2018b) Dicer-like and RNA-dependent RNA polymerase gene family identification and annotation in the cultivated Solanum tuberosum and its wild relative S. commersonii. Planta 248:729–743. https://doi.org/10.1007/s00425-018-2937-3
Esposito S, D’Amelia V, Carputo D, Aversano R (2019) Genes involved in stress signals: the CBLs-CIPKs network in cold tolerant Solanum commersonii. Biol Plantarum 63:699–709. https://doi.org/10.32615/bp.2019.072
Esteve-Turrillas FA, Agulló C, Abad-Somovilla A, Mercader JV, Abad-Fuentes A (2016) Fungicide multiresidue monitoring in international wines by immunoassays. Food Chem 196:1279–1286. https://doi.org/10.1016/j.foodchem.2015.10.102
Feechan A, Jermakow AM, Torregrosa L, Panstruga R, Dry IB (2008) Identification of grapevine MLO gene candidates involved in susceptibility to powdery mildew. Funct Plant Biol 35(12):1255–1266. https://doi.org/10.1071/FP08173
Finn RD, Clements J, Eddy SR (2011) HMMER web server: interactive sequence similarity searching. Nucleic Acids Res 39:W29–W37. https://doi.org/10.1093/nar/gkr367
Fung RW, Gonzalo M, Fekete C et al (2008) Powdery mildew induces defense-oriented reprogramming of the transcriptome in a susceptible but not in a resistant grapevine. Plant Physiol 146(1):236–249. https://doi.org/10.1104/pp.107.108712
Gambino G, Dal Molin A, Boccacci P et al (2017) Whole-genome sequencing and SNV genotyping of ‘Nebbiolo’ (Vitis vinifera L) clones. Sci Rep 7(1):17294. https://doi.org/10.1038/s41598-017-17405-y
Goyal N, Bhatia G, Sharma S, Garewal N, Upadhyay A, Upadhyay SK, Singh K (2019) Genome-wide characterization revealed role of NBS-LRR genes during powdery mildew infection in Vitis vinifera. Genomics in press. https://doi.org/10.1016/j.ygeno.2019.02.011
Grant JJ, Chini A, Basu D, Loake GJ (2003) Targeted activation tagging of the Arabidopsis NBS-LRR gene, ADR1, conveys resistance to virulent pathogens. Mol Plant Microbe In 16(8):669–680. https://doi.org/10.1094/MPMI.2003.16.8.669
Hu Y, Li Y, Hou F et al (2018) Ectopic expression of Arabidopsis broad-spectrum resistance gene RPW8.2 improves the resistance to powdery mildew in grapevine (Vitis vinifera). Plant Sci 267:20–31. https://doi.org/10.1016/j.plantsci.2017.11.005
Iovieno P, Andolfo G, Schiavulli A et al (2015) Structure, evolution and functional inference on the Mildew Locus O (MLO) gene family in three cultivated Cucurbitaceae spp. BMC Genomics 16(1):1112. https://doi.org/10.1186/s12864-015-2325-3
Jones DT, Taylor WR, Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences. Bioinformatics 8(3):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(9):1236–1240. https://doi.org/10.1093/bioinformatics/btu031
Jubic LM, Saile S, Furzer OJ, El Kasm F, Dangl JL (2019) Help wanted: helper NLRs and plant immune responses. Curr Opin Plant Biol 50:82–94. https://doi.org/10.1016/j.pbi.2019.03.013
Kersting AR, Bornberg-Bauer E, Moore AD, Grath S (2012) Dynamics and adaptive benefits of protein domain emergence and arrangements during plant genome evolution. Genome Biol Evol 4:316–329. https://doi.org/10.1093/gbe/evs004
Kumar S, Stecher G, Tamura K (2015) MEGA7: Molecular evolutionary genetics analysis version 7.0. Mol Biol Evol 33(7):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(21):2947–2948. https://doi.org/10.1093/bioinformatics/btm404
Lozano R, Hamblin MT, Prochnik S, Jannink JL (2015) Identification and distribution of the NBS-LRR gene family in the Cassava genome. BMC Genomics 16(1):360. https://doi.org/10.1186/s12864-015-1554-9
Marchler-Bauer A, Bryant SH (2004) CD-search: protein domain annotations on the fly. Nucleic Acids Res 32:W327–W331. 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(4):212. https://doi.org/10.1186/gb-2006-7-4-212
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
Ortiz D, Dodds PN (2018) Plant NLR origins traced back to green algae. Trends Plant Sci 23(8):651–654. https://doi.org/10.1016/j.tplants.2018.05.009
Osuna-Cruz CM, Paytuvi-Gallart A, Di Donato A et al (2017) PRGdb 30: a comprehensive platform for prediction and analysis of plant disease resistance genes. Nucleic Acids Res 46(D1):D1197–D1201. https://doi.org/10.1093/nar/gkx1119
Peart JR, Mestre P, Lu R, Malcuit I, Baulcombe DC (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 SLK, Frost SDW (2005) A genetic algorithm approach to detecting lineage-specific variation in selection pressure. Mol Biol Evol 22(4):1157. https://doi.org/10.1093/molbev/msi031
Rinaldi A, Villano C, Lanzillo C et al (2017) Metabolic and RNA profiling elucidates proanthocyanidins accumulation in Aglianico grape. Food Chem 233:52–59. https://doi.org/10.1016/j.foodchem.2017.04.093
Roach MJ, Johnson DL, Bohlmann J et al (2018) Population sequencing reveals clonal diversity and ancestral inbreeding in the grapevine cultivar Chardonnay. PLoS Genet 14(11):e1007807. https://doi.org/10.1371/journal.pgen.1007807
Sanseverino W, Ercolano MR (2012) In silico approach to predict candidate R proteins and to define their domain architecture. BMC Res N 5(1):678. https://doi.org/10.1186/1756-0500-5-678
Sarris PF, Cevik V, Dagdas G, Jones JDG, Krasileva KV (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
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(4):2095–2109. https://doi.org/10.1104/pp.15.01487
Shao ZQ, Xue JY, Wang Q, Wang B, Chen JQ (2019) Revisiting the origin of plant NBS–LRR genes. Trends Plant Sci 24(1):9–12. https://doi.org/10.1016/j.tplants.2018.10.015
Stummer BE, Francis IL, Zanker T, Lattey KA, Scott ES (2005) Effects of powdery mildew on the sensory properties and composition of Chardonnay juice and wine when grape sugar ripeness is standardised. Aust J Grape Wine R 11(1):66–76. https://doi.org/10.1111/j.1755-0238.2005.tb00280.x
Villano C, Rinaldi A, Lanzillo C et al (2017) Polyphenol content and differential expression of flavonoid biosynthetic pathway genes in berries of Aglianico. Acta Hortic 1188:141–148. https://doi.org/10.17660/ActaHortic.2017.1188.19
Wang W, Devoto A, Turner JG, Xiao S (2007) Expression of the membrane-associated resistance protein RPW.8 enhances basal defense against biotrophic pathogens. Mol Plant Microbe In 20(8):966–976. https://doi.org/10.1094/MPMI-20-8-0966
Wang W, Wen Y, Berkey R, Xiao S (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(9):2898–2913. https://doi.org/10.1105/tpc.109.067587
Wang W, Zhang Y, Wen Y et al (2013) A comprehensive mutational analysis of the Arabidopsis resistance protein RPW8.2 reveals key amino acids for defense activation and protein targeting. Plant Cell 25(10):4242–4261. https://doi.org/10.1105/tpc.113.117226
Weng K, Li ZQ, Liu RQ, Wang L, Wang YJ, Xu Y (2014) Transcriptome of Erysiphe necator-infected Vitis pseudoreticulata leaves provides insight into grapevine resistance to powdery mildew. Hort Res 1:14049. https://doi.org/10.1038/hortres.2014.49
Wu CH, Abd-El-Haliem A, Bozkurt TO, Belhaj K, Terauchi R, Vossen JH, Kamoun S (2016) NLR signaling network mediates immunity to diverse plant pathogens. BioRxiv 090449:1–10. https://doi.org/10.1101/090449
Xiao S, Ellwood S, Calis O, Patrick E, Li T, Coleman M, Turner JG (2001) Broad-spectrum mildew resistance in Arabidopsis thaliana mediated by RPW8. Science 291:118–120. https://doi.org/10.1126/science.291.5501.118
Xiao S, Brown S, Patrick E, Brearley C, Turner JG (2003) Enhanced transcription of the Arabidopsis disease resistance genes RPW8.1 and RPW8.2 via a salicylic acid-dependent amplification circuit is required for hypersensitive cell death. Plant Cell 15:33–45. https://doi.org/10.1105/tpc.006940
Zhong Y, Cheng ZMM (2016) A unique RPW8-encoding class of genes that originated in early land plants and evolved through domain fission, fusion, and duplication. Sci Rep 6:32923. https://doi.org/10.1038/srep32923
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Ethics approval and consent to participate
Not applicable. This manuscript does not report on or involve the use of any animal or human data or tissue.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Andolfo, G., Villano, C., Errico, A. et al. Inferring RPW8-NLRs’s evolution patterns in seed plants: case study in Vitis vinifera. Planta 251, 32 (2020). https://doi.org/10.1007/s00425-019-03324-x
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00425-019-03324-x