Abstract
Capsicum baccatum var. pendulum is a valuable source of disease resistance and fruit quality traits that could play an important role in the genetic improvement and safeguard of local varieties of common peppers. However, its use for C. annuum var. annuum breeding has been scarce due to postzygotic incompatibilities. In this work, we obtained seven interspecific hybrids between the Italian landrace ‘Friariello’ of C. annuum var. annuum and C. baccatum var. pendulum through embryo rescue. The F1 hybrids were verified by SSR markers and by in situ hybridization, which confirmed their hybrid status and provided evidence for differences in the repetitive content between the parental genomes. These hybrids were vigorous and, for several morphological traits, were intermediate between their parents. However, they were male sterile. The cytological analysis revealed several abnormalities occurring at various stages of the male meiosis. A number of these anomalies were likely the result of structural differences (e.g. a reciprocal translocation, a paracentric inversion) between the two genomes. Due to hybrid pollen sterility, backcross progenies (BC1) were obtained when hybrids were used as female parents. A partial restoration of the fertility in BC1 makes promising the exploitation of this material in breeding programs.
Similar content being viewed by others
References
Alexander MP (1969) Differential staining of aborted and non aborted pollen. Stain Technol 44:117–122
Bai Y, Lindhout P (2007) Domestication and breeding of tomatoes: what have we gained and what can we gain in the future? Ann Bot 100:1085–1094. https://doi.org/10.1093/aob/mcm150
Basu SK, De AK (2003) Capsicum: historical and botanical perspectives. In: De AK (ed) Capsicum: the genus Capsicum. Taylor & Francis Ltd, London, pp 1–15
Carputo D, Aversano R, Barone A, Di Matteo A et al (2009) Resistance to Ralstonia solanacearum of sexual hybrids between Solanum commersonii and S. tuberosum. Am J Potato Res 86:196–202. https://doi.org/10.1007/s12230-009-9072-4
Carrizo García C, Barfuss MHJ, Sehr EM, Barboza GE et al (2016) Phylogenetic relationships, diversification and expansion of chili peppers (Capsicum, Solanaceae). Ann Bot 118(1):35–51. https://doi.org/10.1093/aob/mcw079
Collonnier C, Fock I, Daunay MI et al (2003) Somatic hybrids between Solanum melongena and S. sisymbrifolium, as a useful source of resistance against bacterial and fungal wilts. Plant Sci 164:849–861. https://doi.org/10.1016/S0168-9452(03)00075-X
De Storme N, Geelen D (2013) Pre-meiotic endomitosis in the cytokinesis-defective tomato mutant pmcd1 generates tetraploid meiocytes and diploid gametes. Exp Bot 64(8):2345–2358. https://doi.org/10.1093/jxb/ert091
Di Dato F, Parisi M, Cardi T, Tripodi P (2015) Genetic diversity and assessment of markers linked to resistance and pungency genes in Capsicum germplasm. Euphytica 1:103–119. https://doi.org/10.1007/s10681-014-1345-4
Dong F, Mcgrath JM, Helgeson JP, Jiang J (2001) The genetic identity of alien chromosomes in potato breeding lines revealed by sequential GISH and FISH analyses using chromosome-specific cytogenetic DNA markers. Genome 44:729–734. https://doi.org/10.1139/g01-043
Egawa Y, Tanaka C (1986) Cytogenetical study of the interspecific hybrid between Capsicum annuum and C. baccatum. Jpn J Breed 36:16–21. https://doi.org/10.1270/jsbbs1951.36.16
Eggink PM, Tikunov Y, Maliepaard C et al (2014) Capturing flavors from Capsicum baccatum by introgression in sweet pepper. Theor Appl Genet 127:373–390. https://doi.org/10.1007/s00122-013-2225-3
Eshbaugh WH (2012) The taxonomy of the genus Capsicum. In: Russo VM (ed) Peppers: botany, production and uses. CABI International, Wallingford, pp 14–28. https://doi.org/10.1079/9781845937676.0000
IPGRI, AVRDC and CATIE (1995) Descriptors for Capsicum (Capsicum spp.). International Plant Genetic Resources Institute, Rome, Italy; the Asian Vegetable Research and Development Center, Taipei, Taiwan, and the Centro Agronómico Tropical de Investigación y Enseñanza, Turrialba, Costa Rica
Ji Y, Chetelat RT (2007) GISH analysis of meiotic chromosome pairing in Solanum lycopersicoides introgression lines of cultivated tomato. Genome 50(9):825–833. https://doi.org/10.1139/G07-069
Jiang J, Gill BS, Wang GL, Ronald PC, Ward DC (1995) Metaphase and interphase fluorescence in situ hybridisation mapping of rice genome with bacterial artificial chromosomes. Proc Natl Acad Sci USA 92:4487–4491
Kim S, Park J, Yeom SI et al (2017) New reference genome sequences of hot pepper reveal the massive evolution of plant disease-resistance genes by retroduplication. Genome Biol 18(1):210. https://doi.org/10.1186/s13059-017-1341-9
Kollmannsberger H, Rodriguez-Burruezo A, Nitz S, Nuez F (2011) Volatile and capsaicinoid composition of aji (Capsicum baccatum) and rocoto (Capsicum pubescens), two Andean species of chile peppers. J Sci Food Agric 91:1598–1611. https://doi.org/10.1002/jsfa.4354
Kumar OA, Panda RC, Raja Rao KG (1987) Cytogenetic studies of the F1 hybrids of Capsicum annuum with C. chinense and C. baccatum. Theor Appl Genet 74(2):242–246. https://doi.org/10.1007/s11032-016-0485-8
Lee YR, Yoon JB, Lee J (2016) A SNP-based genetic linkage map of Capsicum baccatum and its comparison to the Capsicum annuum reference physical map. Mol Breed 36:1–11. https://doi.org/10.1007/BF00289975
Mahasuk P, Taylor PWJ, Mongkolporn O (2009) Identification of two new genes conferring resistance to Colletotrichum acutatum in Capsicum baccatum. Phytopathology 99:1100–1104. https://doi.org/10.1094/PHYTO-99-9-1100
Manzur JP, Penella C, Rodríguez-Burruezo A (2013) Effect of the genotype, developmental stage and medium composition on the in vitro culture efficiency of immature zygotic embryos from genus Capsicum. Sci Hortic 161:181–187. https://doi.org/10.1016/j.scienta.2013.06.036
Manzur JP, Fita A, Prohens J, Rodríguez-Burruezo A (2015) Successful wide hybridization and introgression breeding in a diverse set of common peppers (Capsicum annuum) using different cultivated Ají (C. baccatum) accessions as donor parents. PLoS ONE 10(12):e0144142. https://doi.org/10.1371/journal.pone.0144142
Martins KC, Pereira TNS, Souza SAM, Rodrigues R, Junior Amaral ATD (2015) Crossability and evaluation of incompatibility barriers in crosses between Capsicum species. Crop Breed Appl Biotechnol 15:139–145. https://doi.org/10.1590/1984-70332015v15n3a25
Mennella G, D’Alessandro A, Francese G, Fontanella D et al (2018) Occurrence of variable levels of health-promoting fruit compounds in horn-shaped Italian sweet pepper varieties assessed by a comprehensive approach. J Sci Food Agric 98(9):3280–3289. https://doi.org/10.1002/jsfa.8831
Minamiyama Y, Tsuro M, Hirai M (2006) An SSR-based linkage map of Capsicum annuum. Mol Breed 18:157–169. https://doi.org/10.1007/s11032-006-9024-3
Mongkolporn O, Taylor PWJ (2011) Capsicum. In: Kole C (ed) Wild crop relatives: genomic and breeding resources, vegetables. Springer, Berlin, pp 43–57. https://doi.org/10.1007/978-3-642-20450-0
Parisi M, Di Dato F, Ricci S et al (2017) A multi-trait characterization of the ‘Friariello’ landrace: a Mediterranean resource for sweet pepper breeding. Plant Genet Resour 15:165–176. https://doi.org/10.1017/S1479262115000490
Särkinen T, Bohs L, Olmstead RG, Knapp S (2013) A phylogenetic framework for evolutionary study of the nightshades (Solanaceae): a dated 1000-tip tree. BMC Evol Biol 13:214. https://doi.org/10.1186/1471-2148-13-214
Scaldaferro MA, Romero da Cruz MV, Cecchini NM, Moscone EA (2015) FISH and AgNor mapping of the 45S and 5S rRNA genes in wild and cultivated species of Capsicum (Solananceae). Genome 59:95–113. https://doi.org/10.1139/gen-2015-0099
Shopova M (1966) Studies in the genus Capsicum: II. Irregularities in the pollen mother cells. Chromosoma 19:349–356
Soler S, Debreczeni D, Vidal E et al (2015) A new Capsicum baccatum accession shows tolerance to wild-type and resistance-breaking isolates of Tomato spotted wilt virus. Ann Appl Biol 167:343–353. https://doi.org/10.1111/aab.12229
Souza VL, Café-Filho AC (2003) Resistance to Leveillula taurica in the genus Capsicum. Plant Pathol 52:613–619. https://doi.org/10.1046/j.1365-3059.2003.00920.x
Souza MM, Pereira TSN, Sudré CP, Rodrigues R (2012) Meiotic irregularities in Capsicum L. species. Crop Breed Appl Biotechnol 12:138–144. https://doi.org/10.1590/S1984-70332012000200007
Spalink D, Stoffel K, Walden GK, Hulse-Kemp AM et al (2018) Comparative transcriptomics and genomic patterns of discordance in Capsiceae (Solanaceae). Mol Phylogenet Evol 126:293–302. https://doi.org/10.1016/j.ympev.2018.04.030
Tiwari JK, Devi S, Ali N (2018) Progress in somatic hybridization research in potato during the past 40 years. Plant Cell Tiss Organ Cult 132:225–238. https://doi.org/10.1007/s11240-017-1327-z
Varshney RK, Graner A, Sorrells ME (2005) Genomics-assisted breeding for crop improvement. Trends Plant Sci 10(12):621–630. https://doi.org/10.1016/j.tplants.2005.10.004
Yoon JB, Do JW, Yang DC, Park HG (2004) Interspecific cross compatibility among five domesticated species of Capsicum genus. J Korean Soc Hortic Sci 45:324–329
Yoon JB, Yang DC, Park HG (2005) Irregular meiosis and degenerated tapetum layer are the dual causes of hybrid sterility in interspecific hybridization between Capsicum annuum and C. baccatum. J Korean Soc Hortic Sci 46:231–235
Acknowledgements
The authors gratefully acknowledge Dr. Francesco di Dato (CREA Research Centre for Vegetable and Ornamental Crops, Pontecagnano, Italy) and Prof. Adrián Rodríguez Burruezo (COMAV, Institute for Conservation and Improvement of Valencian Agrodiversity, Valencia, Spain) for the invaluable help with the embryo rescue technique, Gaetano Guarino for help with figure preparation, Max Rankenburg for linguistic editing, and anonymous reviewers for their constructive comments. The authors would also like to thank PONa3_00025-BIOforIU for funding the acquisition of a fluorescence microscope. The authors wish to acknowledge CGN (http://www.cgn.wur.nl), for providing the seeds of C. baccatum var. pendululm. This work was partially supported by the GenHort Project funded by the Italian Minister of University and research MIUR (PON02_00395_3215002).
Author information
Authors and Affiliations
Corresponding authors
Electronic supplementary material
Below is the link to the electronic supplementary material.
10681_2018_2211_MOESM1_ESM.tif
Figure S1. Hybridity test using SSR marker CAMS-117 (Minamiyama et al. 2006). M = 1 Kb plus ladder (Invitrogen); P1 = C. annuum var. annuum landrace ‘Friariello’ (FRP); P2 = C. baccatum var. pendulum acc. P04 (BACP04); F1 = FRP x BACP04 F1 hybrids. Polymorphic bands are indicated by asterisks. (TIFF 2980 kb)
10681_2018_2211_MOESM2_ESM.tif
Figure S2. Morphology of the fruits from the parental genotypes, C. annuum var. annuum landrace ‘Friariello’ (FRP) and C. baccatum var. pendulum acc. P04 (BACP04), the F1 hybrids (FRP x BACP04) and their BC1 progeny (FRP x F1). (TIFF 11811 kb)
10681_2018_2211_MOESM3_ESM.tif
Figure S3. FISH mapping of 5S rDNA (green) and 45S rDNA (red) on the metaphase chromosomes of the parental genotypes C. baccatum var. pendulum acc. P04 (BACP04) (A) and C. annuum var. annuum landrace ‘Friariello’ (FRP) (B), and FRP x BACP04 hybrids (C). The insets show a close-up of the chromosome pair carrying the 5S rDNA signals that, in BACP04, co-localize with 45S rDNA signals. Bar scale=5 μm. (TIFF 12719 kb)
Rights and permissions
About this article
Cite this article
Cremona, G., Iovene, M., Festa, G. et al. Production of embryo rescued hybrids between the landrace “Friariello” (Capsicum annuum var. annuum) and C. baccatum var. pendulum: phenotypic and cytological characterization. Euphytica 214, 129 (2018). https://doi.org/10.1007/s10681-018-2211-6
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s10681-018-2211-6