Pedigree analysis of 220 almond genotypes reveals two world mainstream breeding lines based on only three different cultivars

Abstract

Loss of genetic variability is an increasing challenge in tree breeding programs due to the repeated use of a reduced number of founder genotypes. However, in almond, little is known about the genetic variability in current breeding stocks, although several cases of inbreeding depression have been reported. To gain insights into the genetic structure in modern breeding programs worldwide, marker-verified pedigree data of 220 almond cultivars and breeding selections were analyzed. Inbreeding coefficients, pairwise relatedness, and genetic contribution were calculated for these genotypes. The results reveal two mainstream breeding lines based on three cultivars: “Tuono”, “Cristomorto”, and “Nonpareil”. Descendants from “Tuono” or “Cristomorto” number 76 (sharing 34 descendants), while “Nonpareil” has 71 descendants. The mean inbreeding coefficient of the analyzed genotypes was 0.041, with 14 genotypes presenting a high inbreeding coefficient, over 0.250. Breeding programs from France, the USA, and Spain showed inbreeding coefficients of 0.075, 0.070, and 0.037, respectively. According to their genetic contribution, modern cultivars from Israel, France, the USA, Spain, and Australia trace back to a maximum of six main founding genotypes. Among the group of 65 genotypes carrying the S_f allele for self-compatibility, the mean relatedness coefficient was 0.125, with “Tuono” as the main founding genotype (24.7% of total genetic contribution). The results broaden our understanding about the tendencies followed in almond breeding over the last 50 years and will have a large impact into breeding decision-making process worldwide. Increasing current genetic variability is required in almond breeding programs to assure genetic gain and continuing breeding progress.

References

[1] Int. Nut Dried Fruit Counc. Nuts & Dried Fruits Statistical Yearbook 2018/2019. https://www.nutfruit.org/files/tech/1553521370_INC_Statistical_Yearbook_2018.pdf (Reus, 2019).

[2] Grasselly, C. & Crossa-Raynaud, P. The Almond Tree (Maisonneuve et Larose, Paris, 1980).

[3] Zeinalabedini, M., Khayam-Nekoui, M., Grigorian, V., Gradziel, T. M. & Martínez-Gómez, P . The origin and dissemination of the cultivated almond as determined by nuclear and chloroplast SSR marker analysis. Sci. Hortic. 125, 593-601 (2010).

[4] Alioto, T. et al. Transposons played a major role in the diversification between the closely related almond and peach genomes: results from the almond genome sequence. Plant J. 101, 455-472 (2020).

[5] Velasco, D., Hough, J., Aradhya, M. & Ross-Ibarra, J. Evolutionary genomics of peach and almond domestication. G3 Genes Genomics Genet. 6, 3985-3993 (2016).

[6] Kester, D. E., Gradziel, T. M. & Grasselly, C. Almonds (Prunus). Genet. Resourc. Temper. Fruit Nut. Crops. 290, 701-760 (1991).

[7] Arulsekar, S., Parfitt, D. E. & Kester, D. E. Comparison of isozyme variability in peach and almond cultivars. J. Hered. 77, 272-274 (1986).

[8] Arús, P., Gradziel, T., Oliveira, M. M. & Tao, R. Genomics of almond. In Genetics and Genomics of Rosaceae (eds Folta, K.M. & Gardiner, S.E.). 187-219 (Springer, New York, 2009).

[9] Fernández i Martí, A. et al. Molecular analyses of evolution and population structure in a worldwide almond [Prunus dulcis (Mill.) D.A. Webb syn. P. amygdalus Batsch] pool assessed by microsatellite markers. Genet Resour. Crop Evol. 62, 205-219 (2015).

[10] Byrne, D. H. Isozyme variability in four diploid stone fruits compared with other woody perennial plants. J. Hered. 81, 68-71 (1990).

[11] Mnejja, M., Garcia-Mas, J., Audergon, J. M. & Arús, P. Prunus microsatellite marker transferability across rosaceous crops. Tree Genet Genomes 6, 689-700 (2010).

[12] Gradziel, T. M., Curtis, R. & Socias i Company, R. Production and growing regions. In Almonds: Botany, Production and Uses (ed Gradziel, T.M.). 70-86 (CABI, Boston, 2017).

[13] Batlle, I. et al. Classical genetics and breeding. In Almonds: Botany, Production and Uses (ed Gradziel, T.M.). 111-148 (CABI, Boston, 2017).

[14] López, M., Vargas, F. J. & Batlle, I. Self-(in)compatibility almond genotypes: a review. Euphytica 150, 1-16 (2006).

[15] Socias i Company, R. Pollen-style (in)compatibility: development of autogamous cultivars. In Almonds: Botany, Production and Uses (ed Gradziel, T.M.). 188-208 (CABI, Boston, 2017).

[16] Grasselly, C. & Olivier, G. Demonstration of some self-compatible types among almond cultivars (P. amygdalus Batsch) of the population of Puglia. Ann. Amel Plant 26, 107-113 (1976).

[17] Grasselly, C. & Olivier, G. Difficulty of survival of young almond seedlings in some progenies. Options Mediterr. 81, 65-70 (1981).

[18] Socias i Company, R. Breeding self-compatible almonds. Plant Breed. Rev. 8, 313-338 (2011).

[19] Martínez-García, P. J., Dicenta, F. & Ortega, E. Anomalous embryo sac development and fruit abortion caused by inbreeding depression in almond (Prunus dulcis). Sci. Hortic. 133, 23-30 (2012).

[20] Alonso, J. & Socias i Company, R. Self-incompatibility expression in self-compatible almond genotypes may be due to inbreeding. J. Am. Soc. Hortic. Sci. 130, 865-869 (2005).

[21] Ortega, E. & Dicenta, F. Inheritance of self-compatibility in almond: breeding strategies to assure self-compatibility in the progeny. Theor. Appl. Genet. 106, 904-911 (2003).

[22] Keneni, G., Bekele, E., Imtiaz, M. & Dagne, K. Genetic vulnerability of modern crop cultivars: causes, mechanism and remedies. Int. J. Plant Res. 2, 69-79 (2012).

[23] Van De Wouw, M., Kik, C., Van Hintum, T., Van Treuren, R. & Visser, B. Genetic erosion in crops: concept, research results and challenges. Plant Genet. Resour. Characterisation Util. 8, 1-15 (2010).

[24] Halász, J. et al. Genetic variability is preserved among strongly differentiated and geographically diverse almond germplasm: an assessment by simple sequence repeat markers. Tree Genet. Genomes 15, 1-13 (2019).

[25] Cabrita, L., Apostolova, E., Neves, A., Marreiros, A. & Leitão, J. Genetic diversity assessment of the almond (Prunus dulcis (Mill.) D.A. Webb) traditional germplasm of Algarve, Portugal, using molecular markers. Plant Genet. Resour. Characterisation Util. 12, S164-S167 (2014).

[26] Gouta, H. et al. Assessment of genetic diversity and relatedness among Tunisian almond germplasm using SSR markers. Hereditas 147, 283-292 (2010).

[27] Kardos, M., Luikart, G. & Allendorf, F. W. Measuring individual inbreeding in the age of genomics: marker-based measures are better than pedigrees. Heredity 115, 63-72 (2015).

[28] Wang, J. Pedigrees or markers: which are better in estimating relatedness and inbreeding coefficient? Theor. Popul. Biol. 107, 4-13 (2016).

[29] Son, K. M., Kwon, S. I. L. & Choi, C. Inbreeding, coancestry, and founding clones of apple cultivars released from Korea. Hortic. Environ. Biotechnol. 53, 404-409 (2012).

[30] Debuse, C. J., Shaw, D. V. & Dejong, T. M. Response to inbreeding of seedling traits in a Prunus domestica L. breeding population. J. Am. Soc. Hortic. Sci. 130, 904-911 (2005).

[31] Choi, C. & Kappel, F. Inbreeding, coancestry, and founding clones of sweet cherries from North America. J. Am. Soc. Hortic. Sci. 129, 535-543 (2004).

[32] Marrano, A. et al. A new genomic tool for walnut (Juglans regia L.): development and validation of the high-density Axiom^TM J. regia 700K SNP genotyping array . Plant Biotechnol. J. 17, 1027-1036 (2019).

[33] Lansari, A., Kester, D. E. & Iezzoni, A. F. Inbreeding, coancestry, and founding clones of almonds of California, Mediterranean shores, and Russia. J. Am. Soc. Hortic. Sci. 119, 1279-1285 (1994).

[34] Wright, S. Coefficients of inbreeding and relationship. Am. Nat. 56, 330-338 (1922).

[35] Sjulin, T. & Dale, A. Genetic diversity of North American strawberry cultivars. J. Am. Soc. J. Am. Soc. 112, 375-385 (1987).

[36] Dicenta, F. et al. The origin of the self-compatible almond ‘Guara’. Sci. Hortic. 197, 1-4 (2015).

[37] Marchese, A., Bošković, R. I., Martínez-García, P. J. & Tobutt, K. R. The origin of the self-compatible almond ‘Supernova’. Plant Breed. 127, 105-107 (2008).

[38] Wood, M. N. Almond Varieties in the United States (US Department of Agriculture, Washington D.C., 1925).

[39] Kester, D. E. & Gradziel, T. M. Almonds in fruit breeding, Vol. 3. In Nuts (eds Janick, J. & Moore, J.N.). 1-97 (John Wiley and Sons Inc, New York, 1996).

[40] Bartolozzi, F., Warburton, M. L., Arulsekar, S. & Gradziel, T. M. Genetic characterization and relatedness among california almond cultivars and breeding lines detected by randomly amplified polymorphic DNA (RAPD) analysis. J. Am. Soc. Hortic. Sci. 123, 381-387 (1998).

[41] Rikhter, A. Biological basis for the creation of almond cultivars and commercial orchards. Akad Nauk SSSR (1972).

[42] Byrne, D. Inbreeding, coancestry, and founding clones of Japanese-type plums of California and the southeastern United States. J. Am. Soc. Hortic. Sci. (1989).

[43] Noiton, D. & Alspach, P. Founding clones, inbreeding, coancestry, and status number of modern apple cultivars. J. Am. Soc. Hortic. Sci. 121, 773-782 (1996).

[44] Scorza, R., Mehlenbacher, S. & Lightner, G. Inbreeding and coancestry of freestone peach cultivars of the eastern United States and implications for peach germplasm improvement. J. Am. Soc. Hortic. Sci. (1985).

[45] Gradziel, T., Beres, W. & Pelletreau, K. Inbreeding in California canning clingstone peach cultivars. Fruit Var. J. (1993).

[46] Almond Board of Calirfornia . Almond Almanac 2019. https://www.almonds.com/sites/default/files/2020-04/2019_Almanac.pdf (Modesto, 2019).

[47] Almond Board of Australia . Annual Report 2018/2019. https://2q1ee4456oc52trll42uctl1-wpengine.netdna-ssl.com/wp-content/uploads/2019/10/ABA-AnnReport-2018-19-1.pdf (Loxton, 2019).

[48] Zaurov, D. et al. Genetic resources of almond species in the former USSR. J. Am. Soc. Hortic. Sci. 50, 18-29 (2015).

[49] Elhamzaoui, A., Oukabli, A., Charafi, J. & Moumni, M. Assessment of genetic diversity of Moroccan cultivated almond (Prunus dulcis Mill. DA Webb) in its area of extreme diffusion, using nuclear microsatellites. Am. J. Plant Sci. 3, 1294-1303 (2012).

[50] Hamadeh, B., Chalak, L., Coppens d’Eeckenbrugge, G., Benoit, L. & Joly, H. I. Evolution of almond genetic diversity and farmer practices in Lebanon: impacts of the diffusion of a graft-propagated cultivar in a traditional system based on seed-propagation. BMC Plant Biol. 18, 1-18 (2018).

[51] Muranty, H. et al. Using whole-genome SNP data to reconstruct a large multi-generation pedigree in apple germplasm. BMC Plant Biol. 20, 1-18 (2020).

[52] Sánchez-Pérez, R. et al. Mutation of a bHLH transcription factor allowed almond domestication. Science 364, 1095-1098 (2019).

[53] Martínez-Gómez, P., Arulsekar, S., Potter, D. & Gradziel, T. M. An extended interspecific gene pool available to peach and almond breeding as characterized using simple sequence repeat (SSR) markers. Euphytica 131, 313-322 (2003).