Abstract
Plants possess sophisticated surveillance and response systems against potential pathogens. In most cases, the genes underlying plant disease resistance encode nucleotide-binding leucine-rich repeat (NB-LRR) proteins. While the single gene nature of NB-LRR genes makes them widely accessible for plant improvement, the potential for rapid pathogen adaptation and, thus, reduced resistance durability is high. Few disease resistance genes of known function have been cloned in the Rosaceae but several have been mapped, with associated markers available for marker-aided selection. In strawberry, resistance to red stele root rot (Phytophthora fragariae var. fragariae), anthracnose (Colletotrichum acutatum), and angular leaf spot (Xanthomonas fragariae) have all been the targets of genetic mapping. In Rubus, gene H conditions pubescence in raspberry is associated with resistance to gray mold (Botrytis cinerea), spur blight (Didymella applanata), cane blight (Leptosphaeria coniothyrium), and cane spot (Elsinoë veneta). It is unclear whether pubescence acts as a preformed physical barrier to infection or if gene H is physically linked to NB-LRR genes conditioning the various resistances. Resistance to Raspberry bushy dwarf virus has been genetically mapped and markers associated with resistance to the aphids Amphoromphora idaei and Amphorophora agathonica, vectors of important raspberry viruses, have been identified. Candidate gene approaches including PCR-based methods for generating resistance gene fragments hold some potential for development of markers useful in strawberry and raspberry breeding. Finally, the availability of whole genome sequences from Fragaria and Rubus species enables in silico discovery of NB-LRR genes and visualization of evolutionary relationships and physical genome distribution, a focus of research in our research laboratory.
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References
Aarts MGM, te Hekkert BL, Holub EB et al (1998) Identification of R gene homologous DNA fragments genetically linked to disease resistance loci in Arabidopsis thaliana. Mol Plant-Microbe Interact 11:251–258. https://doi.org/10.1094/MPMI.1998.11.4.251
Afanador-Kafuri L, Mejía JF, González A, Álvarez E (2015) Identifying and analyzing the diversity of resistance gene analogs in Colombian Rubus genotypes. Plant Dis 99:994–1001. https://doi.org/10.1094/PDIS-05-14-0475-RE
Arya P, Kumar G, Acharya V, Singh AK (2014) Genome-wide identification and expression analysis of NBS-encoding genes in Malus x domestica and expansion of NBS genes family in Rosaceae. PLoS ONE 9:e107987. https://doi.org/10.1371/journal.pone.0107987
Bernoux M, Ve T, Williams S et al (2011) Structural and functional analysis of a plant resistance protein TIR domain reveals interfaces for self-association, signaling, and autoregulation. Cell Host Microbe 9:200–211. https://doi.org/10.1016/j.chom.2011.02.009
Boyd LA, Ridout C, O’Sullivan DM et al (2013) Plant–pathogen interactions: disease resistance in modern agriculture. Trends Genet 29:233–240. https://doi.org/10.1016/j.tig.2012.10.011
Briggs JB (1965) The distribution, abundance, and genetic relationships of four strains of the Rubus aphid (Amphorophora rubi (Kalt.)) in relation to raspberry breeding. J Hortic Sci 40:109–117. https://doi.org/10.1080/00221589.1965.11514125
Bushakra JM, Bryant DW, Dossett M et al (2015) A genetic linkage map of black raspberry (Rubus occidentalis) and the mapping of Ag 4 conferring resistance to the aphid Amphorophora agathonica. Theor Appl Genet 128:1631–1646. https://doi.org/10.1007/s00122-015-2541-x
Bushakra JM, Stephens MJ, Atmadjaja AN et al (2012) Construction of black (Rubus occidentalis) and red (R. idaeus) raspberry linkage maps and their comparison to the genomes of strawberry, apple, and peach. Theor Appl Genet 125:311–327. https://doi.org/10.1007/s00122-012-1835-5
Cesari S, Bernoux M, Moncuquet P et al (2014) A novel conserved mechanism for plant NLR protein pairs: the “integrated decoy” hypothesis. Front Plant Sci 5:606. https://doi.org/10.3389/fpls.2014.00606
Chen X-R, Brurberg MB, Elameen A et al (2016) Expression of resistance gene analogs in woodland strawberry (Fragaria vesca) during infection with Phytophthora cactorum. Mol Genet Genomics 291:1967–1978. https://doi.org/10.1007/s00438-016-1232-x
Chisholm ST, Coaker G, Day B, Staskawicz BJ (2006) Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124:803–814. https://doi.org/10.1016/j.cell.2006.02.008
Collins NC, Webb CA, Seah S et al (1998) The isolation and mapping of disease resistance gene analogs in maize. Mol Plant-Microbe Interact 11:968–978. https://doi.org/10.1094/MPMI.1998.11.10.968
Denoyes B, Baudry A (1995) Species identification and pathogenicity study of French Colletotrichum strains isolated from strawberry using morphological and cultural characteristics. Phytopathology 85:53. https://doi.org/10.1094/Phyto-85-53
Denoyes-Rothan B, Guérin G, Lerceteau-Köhler E, Risser G (2005) Inheritance of resistance to Colletotrichum acutatum in Fragaria × ananassa. Phytopathology 95:405–412. https://doi.org/10.1094/PHYTO-95-0405
Dodds PN, Lawrence GJ, Catanzariti A-M et al (2006) Direct protein interaction underlies gene-for-gene specificity and coevolution of the flax resistance genes and flax rust avirulence genes. Proc Natl Acad Sci U S A 103:8888–8893. https://doi.org/10.1073/pnas.0602577103
Dodds PN, Rathjen JP (2010) Plant immunity: towards an integrated view of plant–pathogen interactions. Nat Rev Genet 11:539–548. https://doi.org/10.1038/nrg2812
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
Dossett M, Finn CE (2010) Identification of resistance to the large raspberry aphid in black raspberry. J Am Soc Hortic Sci 135:438–444
Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797. https://doi.org/10.1093/nar/gkh340
Finn RD, Bateman A, Clements J et al (2014) Pfam: the protein families database. Nucleic Acids Res 42:D222–D230. https://doi.org/10.1093/nar/gkt1223
Flor HH (1955) Host-parasite interaction in flax rust—its genetics and other implications. Phytopathology 45:680–685
Graham J, Smith K, Tierney I et al (2006) Mapping gene H controlling cane pubescence in raspberry and its association with resistance to cane botrytis and spur blight, rust and cane spot. Theor Appl Genet 112:818–831. https://doi.org/10.1007/s00122-005-0184-z
Haymes KM, Henken B, Davis TM, van de Weg WE (1997) Identification of RAPD markers linked to a Phytophthora fragariae resistance gene (Rpf1) in the cultivated strawberry. Theor Appl Genet 94:1097–1101. https://doi.org/10.1007/s001220050521
Haymes KM, Hokanson SC, Salazar K, Maas J (1998) Molecular markers linked to Phytophthora fragariae resistance genes in strawberry. HortScience 33:500
Haymes KM, Van De Weg WE, Arens P et al (2000) Development of SCAR markers linked to a Phytophthora fragariae resistance gene and their assessment in European and North American strawberry genotypes. J Am Soc Hortic Sci 125:330–339
Hirakawa H, Shirasawa K, Kosugi S et al (2014) Dissection of the octoploid strawberry genome by deep sequencing of the genomes of Fragaria species. DNA Res 21:169–181. https://doi.org/10.1093/dnares/dst049
Hokanson SC, Maas JL (2010) Strawberry biotechnology. In: Janick J (ed) Plant breeding reviews. Wiley, Oxford, UK, pp 139–180
Jia Y, Yuan Y, Zhang Y et al (2015) Extreme expansion of NBS-encoding genes in Rosaceae. BMC Genet 16:1–12. https://doi.org/10.1186/s12863-015-0208-x
Jones AT, Murant AF, Jennings DL, Wood GA (1982) Association of raspberry bushy dwarf virus with raspberry yellows disease; reaction of Rubus species and cultivars, and the inheritance of resistance. Ann Appl Biol 100:135–147. https://doi.org/10.1111/j.1744-7348.1982.tb07200.x
Jones JDG, Dangl JL (2006) The plant immune system. Nature 444:323–329. https://doi.org/10.1038/nature05286
Jung S, Ficklin SP, Lee T et al (2014) The Genome Database for Rosaceae (GDR): year 10 update. Nucleic Acids Res 42:1237–1244. https://doi.org/10.1093/nar/gkt1012
Kanazin V, Marek LF, Shoemaker RC (1996) Resistance gene analogs are conserved and clustered in soybean. Proc Natl Acad Sci USA 93:11746–11750
Kobe B, Kajava A (2001) The leucine-rich repeat as a protein recognition motif. Curr Opin Struct Biol 11:725–732
Leister D, Ballvora A, Salamini F, Gebhardt C (1996) A PCR–based approach for isolating pathogen resistance genes from potato with potential for wide application in plants. Nat Genet 14:421–429. https://doi.org/10.1038/ng1296-421
Lerceteau-Köhler E, Guérin G, Denoyes-Rothan B (2005) Identification of SCAR markers linked to Rca2 anthracnose resistance gene and their assessment in strawberry germplasm. Theor Appl Genet 111:862–870. https://doi.org/10.1007/s00122-005-0008-1
Li J, Zhang Q-Y, Gao Z-H et al (2013) Genome-wide identification and comparative expression analysis of NBS–LRR-encoding genes upon Colletotrichum gloeosporioides infection in two ecotypes of Fragaria vesca. Gene 527:215–227. https://doi.org/10.1016/j.gene.2013.06.008
Lightle DM, Dossett M, Backus EA, Lee JC (2012) Location of the mechanism of resistance to Amphorophora agathonica (Hemiptera: Aphididae) in red raspberry. J Econ Entomol 105:1465–1470. https://doi.org/10.1603/EC11405
Lupas A, Van Dyke M, Stock J (1991) Predicting coiled coils from protein sequences. Science 252:1162–1164. https://doi.org/10.1126/science.252.5009.1162
Maas JL, Gouin CC, Hokanson SC, Hartung JS (2002) Strawberry parent clones US 4808 and US 4809 resistant to bacterial angular leafspot disease caused by Xanthomonas fragariae. HortScience 37:716–717
Mackey D, Holt BF, Wiig A, Dangl JL (2002) RIN4 interacts with Pseudomonas syringae Type III effector molecules and is required for RPM1-mediated resistance in Arabidopsis. Cell 108:743–754. https://doi.org/10.1016/S0092-8674(02)00661-X
Maekawa T, Cheng W, Spiridon LN et al (2011) Coiled-coil domain-dependent homodimerization of intracellular barley immune receptors defines a minimal functional module for triggering cell death. Cell Host Microbe 9:187–199. https://doi.org/10.1016/j.chom.2011.02.008
Martínez Zamora MG, Castagnaro AP, Díaz Ricci JC (2004) Isolation and diversity analysis of resistance gene analogues (RGAs) from cultivated and wild strawberries. Mol Genet Genomics 272:480–487. https://doi.org/10.1007/s00438-004-1079-4
Ntoukakis V, Saur IM, Conlan B, Rathjen JP (2014) The changing of the guard: the Pto/Prf receptor complex of tomato and pathogen recognition. Curr Opin Plant Biol 20:69–74. https://doi.org/10.1016/j.pbi.2014.04.002
Panstruga R, Dodds PN (2009) Terrific protein traffic: the mystery of effector protein delivery by filamentous plant pathogens. Science 324:748–750. https://doi.org/10.1126/science.1171652
Pattison JA, Samuelian SK, Weber CA (2007) Inheritance of Phytophthora root rot resistance in red raspberry determined by generation means and molecular linkage analysis. Theor Appl Genet 115:225–236. https://doi.org/10.1007/s00122-007-0558-5
Price MN, Dehal PS, Arkin AP (2009) FastTree: computing large minimum evolution trees with profiles instead of a distance matrix. Mol Biol Evol 26:1641–1650. https://doi.org/10.1093/molbev/msp077
Roach JA, Verma S, Peres NA et al (2016) FaRXf1: a locus conferring resistance to angular leaf spot caused by Xanthomonas fragariae in octoploid strawberry. Theor Appl Genet 129:1191–1201. https://doi.org/10.1007/s00122-016-2695-1
Samuelian SK, Baldo AM, Pattison JA, Weber CA (2008) Isolation and linkage mapping of NBS-LRR resistance gene analogs in red raspberry (Rubus idaeus L.) and classification among 270 Rosaceae NBS-LRR genes. Tree Genet Genomes 4:881–896. https://doi.org/10.1007/s11295-008-0160-2
Sargent DJ, Fernández-Fernández F, Rys A et al (2007) Mapping of A1 conferring resistance to the aphid Amphorophora idaei and dw (dwarfing habit) in red raspberry (Rubus idaeus L.) using AFLP and microsatellite markers. BMC Plant Biol 7:15. https://doi.org/10.1186/1471-2229-7-15
Sarris PF, Duxbury Z, Huh SU et al (2015) A plant immune receptor detects pathogen effectors that target WRKY transcription factors. Cell 161:1089–1100. https://doi.org/10.1016/j.cell.2015.04.024
Sasnauskas A, Rugienius R, Gelvonauskiené D et al (2007) Screening of strawberries with the red stele (Phytophthora fragariae) resistance gene Rpf1 using sequence specific DNA markers. Acta Hortic 760:165–169. https://doi.org/10.17660/ActaHortic.2007.760.21
Shulaev V, Sargent DJ, Crowhurst RN et al (2011) The genome of woodland strawberry (Fragaria vesca). Nat Genet 43:109–116. https://doi.org/10.1038/ng.740
Stephens M, Buck E, Tahir J (2016) Mapping a potential resistance gene for Raspberry bushy dwarf virus in red raspberry. Acta Hortic 18:121–128. https://doi.org/10.17660/ActaHortic.2016.1133.18
Takken FL, Albrecht M, Tameling WIL (2006) Resistance proteins: molecular switches of plant defence. Curr Opin Plant Biol 9:383–390. https://doi.org/10.1016/j.pbi.2006.05.009
Takken FL, Goverse A (2012) How to build a pathogen detector: structural basis of NB-LRR function. Curr Opin Plant Biol 15:375–384. https://doi.org/10.1016/j.pbi.2012.05.001
Tennessen JA, Govindarajulu R, Ashman T-L, Liston A (2014) Evolutionary origins and dynamics of octoploid strawberry subgenomes revealed by dense targeted capture linkage maps. Genome Biol Evol 6:3295–3313. https://doi.org/10.1093/gbe/evu261
Terefe-Ayana D, Kaufmann H, Linde M, Debener T (2012) Evolution of the Rdr1 TNL-cluster in roses and other Rosaceous species. BMC Genom 13:409. https://doi.org/10.1186/1471-2164-13-409
Van de Weg WE (1989) Cultivar-race interactions of the strawberry-Phytophthora fragariae system with regard to a gene-for-gene model. Acta Hortic 265:203–206. https://doi.org/10.17660/actahortic.1989.265.29
Van de Weg WE (1997) A gene-for-gene model to explain interactions between cultivars of strawberry and races of Phytophthora fragariae var. fragariae. Theor Appl Genet 94:445–451. https://doi.org/10.1007/s001220050435
Van der Biezen EA, Jones JD (1998) The NB-ARC domain: a novel signalling motif shared by plant resistance gene products and regulators of cell death in animals. Curr Biol 8:R226–R227
VanBuren R, Bryant D, Bushakra JM et al (2016) The genome of black raspberry (Rubus occidentalis). Plant J 87:535–547. https://doi.org/10.1111/tpj.13215
Vos P, Simons G, Jesse T et al (1998) The tomato Mi-1 gene confers resistance to both root-knot nematodes and potato aphids. Nat Biotechnol 16:1365–1369. https://doi.org/10.1038/4350
Ward JA, Bhangoo J, Fernández-Fernández F et al (2013) Saturated linkage map construction in Rubus idaeus using genotyping by sequencing and genome-independent imputation. BMC Genom 14:2. https://doi.org/10.1186/1471-2164-14-2
Ward JA, Boone WE, Moore PP, Weber CA (2012) Developing molecular markers for marker assisted selection for resistance to Raspberry bushy dwarf virus (RBDV) in red raspberry. Acta Hortic, 61–66. https://doi.org/10.17660/actahortic.2012.946.6
Whitham S, Dinesh-Kumar SP, Choi D et al (1994) The product of the tobacco mosaic virus resistance gene N: similarity to Toll and the Interleukin-1 receptor. Cell 78:1101–1115. https://doi.org/10.1016/0092-8674(94)90283-6
Williamson B, Jennings DL (1992) Resistance to cane and foliar diseases in red raspberry (Rubus idaeus) and related species. Euphytica 63:59–70. https://doi.org/10.1007/BF00023912
Yu YG, Buss GR, Saghai Maroof MA (1996) Isolation of a superfamily of candidate disease-resistance genes in soybean based on a conserved nucleotide-binding site. Proc Natl Acad Sci USA 93:11751–11756
Zhong Y, Yin H, Sargent DJ et al (2015) Species-specific duplications driving the recent expansion of NBS-LRR genes in five Rosaceae species. BMC Genom 16:1–16. https://doi.org/10.1186/s12864-015-1291-0
Zipfel C (2014) Plant pattern-recognition receptors. Trends Immunol 35:345–351. https://doi.org/10.1016/j.it.2014.05.004
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van Eck, L., Bradeen, J.M. (2018). The NB-LRR Disease Resistance Genes of Fragaria and Rubus. In: Hytönen, T., Graham, J., Harrison, R. (eds) The Genomes of Rosaceous Berries and Their Wild Relatives. Compendium of Plant Genomes. Springer, Cham. https://doi.org/10.1007/978-3-319-76020-9_6
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