Abstract
Incompatibility in European hazelnut (Corylus avellana L.) is sporophytic and under the control of a single locus on linkage group 5 between markers G05-510 and AU02-1350. In this study, two rounds of marker development and a population of 192 seedlings with known S-alleles that showed recombination between the flanking markers were used for fine map**. Using the sequences of random amplified polymorphic DNA and simple sequence repeat (SSR) markers and bacterial artificial chromosome end sequences, 36 contigs from the genome sequence of “Jefferson” hazelnut were identified for pursuit. Di-nucleotide SSR markers in those contigs were developed, characterized, and mapped. This reduced the size to a region of 500 kb that contained the S-locus and 50 predicted genes, in which single-nucleotide polymorphism and additional SSR markers were developed. When the new markers were used in fine map**, they fully exploited all recombination in the fine map** population and reduced the region to 193.5 kb containing 18 genes. This 193.5-kb region most likely contains the S1 haplotype. A second region, 2 Mbp away from the first in the “Jefferson” genome (V3), is predicted to represent the S3 haplotype based on SSR marker allele sizes and the ratio of parental reads that align to them. Although they appear side-by-side in the “Jefferson” genome (V3), the mapped markers appear in both sequences in the same order. Gene annotations in the S1 and S3 haplotypes are highly similar and include five probable leucine-rich repeat receptor-like protein kinases with homology to Arabidopsis thaliana genes At1g35710 and three probable receptor-like serine/threonine protein kinases with homology to At5g15080 (PIX7).
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
Marker sequences were deposited in GenBank. Additional data is available upon request.
References
Bhattarai G, Mehlenbacher SA (2017) In-silico development and characterization of tri-nucleotide simple sequence repeat markers in hazelnut (Corylus avellana L.). PLoS One 12(5):e01780610. https://doi.org/10.1371/journal.pone.0178061
Bhattarai G, Mehlenbacher SA (2018) Discovery, characterization, and linkage map** of simple sequence repeat markers in hazelnut. J Amer Soc Hort Sci 143(5):347–362. https://doi.org/10.21273/JASHS04461-18
Catchen J, Hohenlohe PA, Bassham S, Amores A, Cresko WA (2013) Stacks: an analysis tool set for population genomics. Mol Ecol 22(11):3124–3140. https://doi.org/10.1111/mec.12354
Colburn BC, Mehlenbacher SA, Sathuvalli VR (2017) Development and map** of microsatellite markers from transcriptome sequences of European hazelnut (Corylus avellana L.) and use for germplasm characterization. Mol Breed 37(2):16. https://doi.org/10.1007/s11032-016-0616-2
Coleman AD, Raasch L, Maroschek J, Ranf S, Hückelhoven R (2019) The Arabidopsis leucine-rich repeat receptor kinase MIK2 is a crucial component of pattern-triggered immunity responses to Fusarium fungi. BioRxiv 720037 https://doi.org/10.1101/720037
Ding Y, Johnson MD, Chen WQ, Wong D, Chen YJ, Benson SC, Lam JY, Kim YM, Shizuya H (2001) Five-color-based high-information-content fingerprinting of bacterial artificial chromosome clones using type IIS restriction endonucleases. Genomics 74(2):142–154. https://doi.org/10.1006/geno.2001.6547
Glenn TC, Nilsen RA, Kieran TJ, Sanders JG, Bayona-Vásquez NJ, Finger JW, Pierson TW, Bentley KE, Hoffberg SL, Louha S, Garcia-de Leon FJ, del Rio Portilla MA, Reed KD, Anderson JL, Meece JK, Aggrey SE, Rekaya R, Alabady M, Belanger M, Winker K, Faircloth BC (2019) Adapterama I: universal stubs and primers for 384 unique dual-indexed or 147,456 combinatorially-indexed Illumina libraries (iTru & iNext). PeerJ 7:e7755. https://doi.org/10.7717/peerj.7755
Gürcan K, Mehlenbacher SA (2010) Development of microsatellite marker loci for European hazelnut (Corylus avellana L.) from ISSR fragments. Mol Breed 26:551–559. https://doi.org/10.1007/s11032-010-9464-7
Guy E, Lautier M, Chabannes M, Roux B, Lauber E, Arlat M, and Noël LD (2013) xopAC-triggered immunity against Xanthomonas depends on Arabidopsis receptor-like cytoplasmic kinase genes PBL2 and RIPK. PLOS ONE 8(8) https://doi.org/10.1371/journal.pone.0073469
Hampson CR, Coleman GD, Azarenko AN (1996) Does the genome of Corylus avellana L. contain sequences homologous to the self-incompatibility gene of Brassica? Theoret Appl Genetics 93:759–764. https://doi.org/10.1007/BF00224073
Higashiyama T, Yang W (2017) Gametophytic pollen tube guidance: attractant peptides, gametic controls, and receptors. Plant Physiol 173(1):112–121. https://doi.org/10.1104/pp.16.01571
Julkowska MM, Klei K, Fokkens L, Haring MA, Schranz ME, Testerink C (2016) Natural variation in rosette size under salt stress conditions corresponds to developmental differences between Arabidopsis accessions and allelic variation in the LRR-KISS gene. J Exp Bot 67(8):2127–2138. https://doi.org/10.1093/jxb/erw015
Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program CERVUS accommodates genoty** error increases success in paternity assignment. Mol Ecol 16:1099–1106. https://doi.org/10.1111/j.1365-294X.2007.03089.x
Koseva B, Crawford DJ, Brown KE, Mort ME, Kelly JK (2017) The genetic breakdown of sporophytic self-incompatibility in Tolpis coronopifolia (Asteraceae). New Phytol 216:1256–1267. https://doi.org/10.1111/nph.14759
Li H (2013) Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. ar**v:1303.3997v2 [q-bio.GN]
Li H, Handsaker B, Wysoker A, Fennel T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, 1000 Genome Project Data Processing Subgroup (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25(16):2078–2079. https://doi.org/10.1093/bioinformatics/btp352
Liu K, Muse SV (2005) PowerMarker: Integrated analysis environment for genetic marker data. Bioinformatics 21(9):2128–2129. https://doi.org/10.1093/bioinformatics/bti282
Lunde CF, Mehlenbacher SA, Smith DC (2000) Survey of hazelnut cultivars for response to eastern filbert blight inoculation. HortScience 35:729–731. https://doi.org/10.21273/HORTSCI.35.4.729
Mehlenbacher SA (1997) Testing compatibility of hazelnut crosses using fluorescence microscopy. Acta Hortic 445:167–171. https://doi.org/10.17660/ActaHortic.1997.445.22
Mehlenbacher SA (2014) Geographic distribution of incompatibility alleles in cultivars and selections of European hazelnut. J Amer Soc Hort Sci 139:191–212
Mehlenbacher SA, Bhattarai G (2018) An updated linkage map for hazelnut with new simple sequence repeat markers. Acta Hortic 1226:31–38. https://doi.org/10.17660/ActaHortic.2018.1226.4
Mehlenbacher SA, Brown RN, Nouhra ER, Gökirmak T, Bassil NV, Kubisiak TL (2006) A genetic linkage map for hazelnut (Corylus avellana L.) based on RAPD and SSR markers. Genome 49:122–133. https://doi.org/10.1139/g05-091
Mehlenbacher SA, Smith DC (2006) Self-compatible seedlings of the cutleaf hazelnut. HortScience 41:482–483. https://doi.org/10.21273/HORTSCI.41.2.482
Milne I, Stephen G, Bayer M, Cock PJA, Pritchard L, Cardle L, Shaw PD, Marshall D (2012) Using Tablet for visual exploration of second-generation sequencing data. Brief Bioinform 14(2):193–202. https://doi.org/10.1093/bib/bbs012
Nasrallah JB, Rundle SJ, Nasrallah ME (1994) Genetic evidence for the requirement of the Brassica S-locus receptor kinase gene in the self-incompatibility response. Plant J 5:373–384. https://doi.org/10.1111/j.1365-313X.1994.00373.x
Rahman MH, Uchiyama M, Kuno M, Hirashima N, Suwabe K, Tsuchiya T, Kagaya Y, Kobayashi I, Kakeda K, Kowyama Y (2007) Expression of stigma- and anther-specific genes located in the S locus region of Ipomoea trifida. Sex Plant Reprod 20:73–85. https://doi.org/10.1007/s00497-007-0045-9
Rochette NC, Rivera-Colón A, Catchen JM (2019) Stacks 2: Analytical methods for paired-end sequencing improve RADseq-based population genomics. Mol Ecol 28(21):4737–4754. https://doi.org/10.1111/mec.15253
Rowley ER, Fox SE, Bryant DW, Sullivan CM, Priest HD, Givan SA, Mehlenbacher SA, Mockler TC (2012) Assembly and characterization of the European hazelnut ‘Jefferson’ transcriptome. Crop Sci 52:2679–2686. https://doi.org/10.2135/cropsci2012.02.0065
Rowley ER, VanBuren R, Bryant DW, Priest HD, Mehlenbacher SA, and Mockler TC (2018) A draft genome and high-density genetic map of European hazelnut (Corylus avellana L.). BioRxiv 469015 https://doi.org/10.1101/469015
Sathuvalli VR, Mehlenbacher SA (2011) A bacterial artificial chromosome library for ‘Jefferson’ hazelnut and identification of clones associated with eastern filbert blight resistance and pollen–stigma incompatibility. Genome 54:862–867. https://doi.org/10.1139/g11-048
Schopfer CR, Nasrallah ME, Nasrallah JB (1999) The male determinant of self-incompatibility in Brassica. Science 286(5445):1697–1700. https://doi.org/10.1126/science.286.5445.1697
Snelling JW, Sathuvalli VR, Colburn BC, Bhattarai G, Rowley ER, Mockler TC, Saski CA, Copetti D, Mehlenbacher SA (2018) Genomic resource development in hazelnut breeding. Acta Hortic 1226:39–46. https://doi.org/10.17660/ActaHortic.2018.1226.5
Stephenson AJ, Doughty J, Dixon S, Elleman CJ, Hiscock SJ, Dickinson HG (1997) The male determinant of self-incompatibility in Brassica oleracea is located in the pollen-coating. Plant J 12(6):1351–1359. https://doi.org/10.1046/j.1365-313x.1997.12061351.x
Takasaki T, Hatakeyama K, Suzuki G, Watanabe M, Isogai A, Hinata K (2000) The S receptor kinase determines self-incompatibility in Brassica stigma. Nature 403:913–916. https://doi.org/10.1038/35002628
Takayama S, Shiba H, Iwano M, Shimosato H, Che F, Kai N, Watanabe M, Suzuki G, Hinata K, Isogai A (2000) The pollen determinant of self-incompatibility in Brassica campestris. PNAS 97(4):1920–1925. https://doi.org/10.1073/pnas.040556397
Tello D, Gil J, Loaiza CD, Riascos JJ, Cardozo N, Duitama J (2019) NGSEP3: accurate variant calling across species and sequencing protocols. Bioinformatics 35(22):4716–4723. https://doi.org/10.1093/bioinformatics/btz275
Van der Does D, Boutrot F, Engelsdorf T et al (2017) The Arabidopsis leucine-rich repeat receptor kinase MIK2/LRR-KISS connects cell wall integrity sensing, root growth and response to abiotic and biotic stresses. PLoS Genet 13(6):e1006832. https://doi.org/10.1371/journal.pgen.1006832
Van Ooijen JW (2018) JoinMap® 5, Software for the calculation of genetic linkage maps in experimental populations of diploid species. Kyazama B.V, Wageningen
Wang X, Lu P, Luo Z (2013) GMATo: A novel tool for the identification and analysis of microsatellites in large genomes. Bioinformation 9(10):541–544. https://doi.org/10.6026/97320630009541
**n Z, Chen J (2012) A high throughput DNA extraction method with high yield and quality. Plant Methods 8:26
You FM, Huo N, Qiang Gu Y, Luo M, Ma Y, Hane D, Lazo GR, Dvorak J, Anderson OD (2008) BatchPrimer3: A high throughput web application for PCR and sequencing primer design. BMC Bioinformatics 9:253. https://doi.org/10.1186/1471-2105-9-253
Funding
This study was supported by the Oregon Hazelnut Commission, United States Department of Agriculture–National Institute of Food and Agriculture-Specialty Crops Research Initiative Grant 2016-51181-25412, a Specific Cooperative Agreement with the United States Department of Agriculture for eastern filbert blight research, and the Oregon Agricultural Experiment Station.
Author information
Authors and Affiliations
Contributions
Data collection and analyses were performed by Ryan J. Hill and Claudia Baldassi. Research materials, experimental design, funding, and supervision were supplied by Shawn A. Mehlenbacher. Shawn A. Mehlenbacher also identified the S-alleles of 192 recombinant seedlings. Kelly J. Vining annotated genome sequences. Jacob W. Snelling aligned BAC end and genome sequences to identify contigs associated with the S-locus. Jacob W. Snelling also aligned the “Jefferson” S1 and S3 haplotype sequences with Illumina reads of parents OSU 252.146 and OSU 414.062. Ryan J. Hill wrote the first draft of the manuscript with input from the other authors. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflicts of interest
None
Additional information
Communicated by C. Chen
Data archiving statement
Sequences from which HRM and SSR markers were developed are deposited in GenBank as accession numbers MT181674 through MT181749.
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Hill, R.J., Baldassi, C., Snelling, J.W. et al. Fine map** of the locus controlling self-incompatibility in European hazelnut. Tree Genetics & Genomes 17, 6 (2021). https://doi.org/10.1007/s11295-020-01485-5
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11295-020-01485-5