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Reproductive Compatibility in Capsicum Is Not Reflected in Genetic Or Phenotypic

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Reproductive Compatibility in Capsicum Is Not Reflected in Genetic Or Phenotypic bioRxiv preprint doi: https://doi.org/10.1101/2020.11.30.403691; this version posted November 30, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 1 Reproductive Compatibility in Capsicum is not Reflected in Genetic or Phenotypic 2 Similarity Between Species Complexes 3 Catherine Parry1, Yen-wei Wang2, Shih-wen Lin2, and Derek W. Barchenger2* 4 1 Department of Biology and Biochemistry, University of Bath, Claverton Down, Bath, UK, 5 BA27AY 6 2World Vegetable Center, Shanhua, Tainan, Taiwan, 74151 7 *[email protected] 8 9 Copyright: © 2021 Parry et al. This is an open access article distributed under the terms of 10 the Creative Commons Attribution License, which permits unrestricted use, distribution, and 11 reproduction in any medium, provided the original author and source are credited. 12 Data Availability: The data used in this study are available in the World Vegetable Center 13 repository, HARVEST, doi:10.22001/wvc.73914, https://worldveg.tind.io/record/73914 14 Funding: Funding for this research was provided by the Ministry of Science and Technology 15 (MOST) of Taiwan (Project ID:107-2311-B-125 -001 -MY3) as well as long-term strategic 16 donors to the World Vegetable Center, Taiwan; UK aid from the UK government; U.S. 17 Agency for International Development (USAID); Australian Centre for International 18 Agricultural Research (ACIAR), Germany, Thailand, Philippines, Korea, and Japan. 19 Competing interests: The authors have declared that no competing interests exist. 20 21 Acknowledgments: We thank Dr. Paul Bosland of Chile Pepper Institute, New Mexico State 22 University, USA for providing Capsicum accessions. 23 24 25 26 1 bioRxiv preprint doi: https://doi.org/10.1101/2020.11.30.403691; this version posted November 30, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 27 Additional index words. Pepper, interspecific hybridization, wild relatives, germplasm 28 misidentification. 29 30 Abstract. Wild relatives of domesticated Capsicum represent substantial genetic diversity and 31 thus sources of traits of potential interest. Furthermore, the hybridization compatibility 32 between members of Capsicum species complexes remains unresolved. Improving our 33 understanding of the relationship between Capsicum species relatedness and their ability to 34 form hybrids is a highly pertinent issue. Through the development of novel interspecific 35 hybrids in this study, we demonstrate interspecies compatibility is not necessarily reflected in 36 relatedness according to established Capsicum genepool complexes. Based on a phylogeny 37 constructed by genotyping using single sequence repeat (SSR) markers and with a portion of 38 the waxy locus, and through principal component analysis (PCA) of phenotypic data, we 39 clarify the relationships among wild and domesticated Capsicum species. Together, the 40 phylogeny and hybridization studies provide evidence for the misidentification of a number 41 of species from the World Vegetable Center genebank included in this study. The World 42 Vegetable Center holds the largest collection of Capsicum genetic material globally, 43 therefore this may reflect a wider issue in the misidentification of Capsicum wild relatives. 44 The findings presented here provide insight into an apparent disconnect between 45 compatibility and relatedness in the Capsicum genus, which will be valuable in identifying 46 candidates for future breeding programs. 47 48 49 50 2 bioRxiv preprint doi: https://doi.org/10.1101/2020.11.30.403691; this version posted November 30, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 51 The genus Capsicum is comprised of about 35 species including five domesticated species: 52 C. annuum (L.), C. baccatum (L.), C. chinense (Jacq.), C. frutescens (L.), and C. pubescens 53 (Ruiz & Pav.) (Khoury et al., 2020). The diversity of Capsicum species represents a valuable 54 genetic resource for crop improvement (Barchenger and Bosland, 2019). The primary 55 limitations to improving productivity and quality of Capsicum are abiotic and biotic stresses, 56 many of which lack sources of host tolerance or resistance (Barchenger et al., 2019). 57 Furthermore, as a widely consumed crop with cultural and culinary value across global 58 cuisines, there is high demand for Capsicum (Bosland and Votava, 2012). There is therefore 59 significant incentive to overcome challenges to cultivation, and one means of doing so being 60 the introgression of resistance to the various stresses that limit production of Capsicum 61 species. 62 Understanding interspecies compatibility and identifying barriers to hybridization is 63 essential to the design of introgression breeding programs. Capsicum species are divided 64 among 11 clades (Bosland and Votava, 2012; Carrizo García et al., 2016) and grouped into 65 three complexes - Annuum, Baccatum and Pubescens - based on their relative reproductive 66 compatibility (Tong and Bosland, 1999; Pickersgill, 1971; Emboden Jr., 1962). There is 67 understood to be relatively low reproductive compatibility between species complexes (van 68 Zonneveld et al., 2015). However, a number of cross-complex hybridizations have been 69 achieved (Eggink et al., 2014; Costa et al., 2009; Kamvorn et al., 2014; Yoon et al., 2006; 70 OECD, 2006; Pickersgill, 1991), and the pre- and post-zygotic barriers to hybridization 71 between genetic complexes are not fully understood (Yoon et al., 2006). This suggests 72 isolation between complexes is not total, and there is therefore potential for introgression 73 breeding, or design of genetic bridge strategies in order to best exploit this genetic variation. 74 In contrast to other Solanaceae crops, including tomato (Solanum lycopersicum) (Lin 75 et al., 2014), potato (S. tuberosum) (Hirsch et al., 2013) and to a lesser extent eggplant (S. 3 bioRxiv preprint doi: https://doi.org/10.1101/2020.11.30.403691; this version posted November 30, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 76 melongena) (Gramazio et al., 2017) introgression breeding using wild species has been 77 relatively underutilized in Capsicum; (Mongkolporn and Taylor, 2011). The wild progenitor, 78 C. annuum var. glabriusculum is a potential source of disease resistance, with reported 79 resistance to Beet curly top virus (BCTV: Curtovirus) (Bosland, 2000; Jimenez, 2019). 80 Members of the wild species C. chacoense and C. rhomboideum have been identified as 81 being resistant to powdery mildew (Leveillula taurica) (McCoy and Bosland, 2019). 82 Recently, an accession of C. galapagoense has been proposed to be a potential source of 83 resistance to the insect pest, whitefly, based on trichome density and type (M. Rhaka, pers. 84 comm.). However, despite extensive hybridization no successful progeny have so far been 85 developed (Lin et al., 2020). These results are surprising, because C. galapagoense has been 86 reported as part of the C. annuum clade, and readily hybridize with C. annuum accessions 87 (Carrizo García et al., 2016; Pickersgill, 1971). One reason for unsuccessful hybridization 88 attempts may be misidentification; several genebanks have incorrectly reported accessions 89 identified as C. galapagoense which are, in fact, C. frutescens (P.W. Bosland, pers. comm.). 90 Such misidentification presents a challenge to utilizing knowledge of the relatedness of 91 Capsicum species and their ability to hybridize. Although the genetic diversity and variation 92 within wild populations of Capsicum has been studied (Carrizo García et al., 2016; Cheng et 93 al., 2016; Aguilar Meléndez et al., 2009; Oyama et al., 2006; Votava et al., 2002; Loaiza- 94 Figueroa et al., 1989), the pool of phenotypic data for wild Capsicum species remains limited 95 (Barchenger and Bosland, 2019). There also remains a lack of access to publicly available 96 germplasm representing the diversity of wild Capsicum (Khoury et al., 2020). There is 97 therefore an immediate need to better understand the role of wild Capsicum species in future 98 breeding programs. 99 The objectives of this study were to elucidate the relationship between interspecies 100 compatibility and relatedness through extensive interspecific hybridization and the 4 bioRxiv preprint doi: https://doi.org/10.1101/2020.11.30.403691; this version posted November 30, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 101 construction of a phylogeny. We aimed to clarify the relationships among the wild and 102 domesticated Capsicum species included in the study, and confirm the identities of several 103 World Vegetable Center genebank accessions. 104 105 Materials and Methods
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