Genetic diversity, population structure and selection signatures in Enset (Ensete ventricosum, (Welw.) Cheesman), an underutilized and key food security crop in Ethiopia

Genet Resour Crop Evol https://doi.org/10.1007/s10722-023-01683-9 RESEARCH ARTICLE Genetic diversity, population structure and selection signatures in Enset (Ensete ventricosum, (Welw.) Cheesman), an underutilized and key food security crop in Ethiopia Alye Tefera Haile · Mallikarjuna Rao Kovi · Sylvia Sagen Johnsen · Bizuayehu Tesfaye · Trine Hvoslef‑Eide · Odd Arne Rognli Received: 9 March 2023 / Accepted: 10 July 2023 © The Author(s) 2023 Abstract Enset (Ensete ventricosum (Welw.) Cheesman) is a multipurpose, drought-tolerant and a key food security crop, which is the staple food for peoples in the south and southwestern parts of Ethiopia. In this study, we characterized genetic diversity, population structure and selection signatures in 226 cultivated and 10 wild enset accessions collected from diverse enset growing regions of Ethiopia using 3505 high-quality single nucleotide polymorphism (SNP) markers obtained from double-digest restriction-site associated DNA (ddRAD) sequences. The population structure and cluster analyses clearly distinguished between cultivated and wild enset. The analysis of molecular variance (AMOVA) revealed higher levels of genetic diversity within populations and regions (91.2 and 92.4%, respectively) than between populations and regions (8.8 and 7.6%, respectively). This Supplementary Information The online version contains supplementary material available at https://doi. org/10.1007/s10722-023-01683-9. A. T. Haile · M. R. Kovi · S. S. Johnsen · T. Hvoslef‑Eide · O. A. Rognli (*) Department of Plant Sciences, Faculty of Biosciences, Norwegian University of Life Sciences, P.O. Box 5003, 1432 Ås, Norway e-mail: A. T. Haile · B. Tesfaye School of Plant and Horticultural Science, Faculty of Agriculture, Hawassa University, P.O. Box 05, Awassa, Ethiopia shows that the region of origin and environmental heterogeneity have little influence on the genetic diversity. However, the genetic differentiation between regions was moderate to large (FST = 0.06–0.17). The genetic structure of enset was mainly shaped by ecogeographic factors, mode of propagation and cultivation status. Six genes potentially involved in sexual reproduction and flowering signalling, which are key processes underlying domestication and adaptation, were under positive selection demonstrating that sexual reproduction plays an important role in shaping enset diversity. A lot of unexplored diversity is available for improving enset in Ethiopia, with patterns of diversity consistent with divergent selection on adaptive traits. This diversity also shows potential for introducing enset as a more food secure crop for the food insecure regions in the dry north of Ethiopia. Keywords Ensete ventricosum · ddRAD · Population structure · SNPs · Food security Introduction Enset (Ensete ventricosum, (Welw.) Cheesman), commonly known as false banana or Abyssinian banana, is a perennial diploid (2n = 18), monocarpic species belonging to the family Musaceae in the genus Ensete (Westphal et al. 1975). Enset, banana and plantains are the most important cultivated members of the family; all with high global and local economic as Vol.: (0123456789) 13 Genet Resour Crop Evol well as food security importance (Baker and Simmonds 1953; Simmonds 1962). The genus Ensete consists of three species with extensive geographical distribution, E. ventricosum and E. livingstonianum in Africa and E. glaucum in Asia, and five other localized endemics or near-endemic species (Borrell et al. 2019). Enset (Ensete ventricosum, (Welw.) Cheesman) is the only cultivated species of the genus Ensete and its domestication and utilization as a food and fiber crop is so far restricted to Ethiopia. It was domesticated in Ethiopia as early as 10,000 years ago (Brandt et al. 1997). Enset is highly drought tolerant with a wide agroecological distribution and is cultivated only with household-produced inputs (Brandt et al. 1997; Tsegaye and Struik 2002). It is unknown whether its wide distribution across a range of altitudes involves genetic or phenotypic adaptation (Tsegaye 2002). Eighty percent of the enset production is concentrated in the southern and southwestern part of Ethiopia (Bezuneh et al. 1967), where it serves as a staple and co-staple food for about 25 mill people (Borrell et al. 2020; Brandt et al. 1997; Spring et al. 1996). Furthermore, it is used for several other purposes, such as animal feed, fiber, construction material and in traditional medicine. The crop grows best at cooler, higher altitudes and is found mostly between 1200–3100 m above sea level (Brandt et al. 1997). Enset plants grow 4–8 m, sometimes up to 11 m height. Cultivated enset are propagated vegetatively, while wild enset reproduces through seeds (Birmeta et al. 2004; Borrell et al. 2019; Tsegaye and Struik 2001). Enset is usually harvested 4–6 years after transplantation, but age at harvest varies between 3 to 12 years (Borrell et al. 2020; Brandt et al. 1997). Thus, if other crops fail, enset plants can be harvested at any time, providing security against hunger for farmers and their families. This became evident through the great famine in Ethiopia in the years 1888 to 1892 (Tobiaw and Bekele 2011), and is the reason why enset is called “The Tree Against Hunger” (Brandt et al. 1997; Costa 1984). This is an important aspect of introducing enset to other, more food insecure regions in Ethiopia, particularly in the dry north. Ethiopia is the center of origin of many plant species, including enset (Engels and Hawkes 1991). The presence of wild and cultivated enset indicates that Ethiopia is the primary center of origin and center of diversity (Purseglove 1985; Vavilov 1951). Vol:. (1234567890) 13 Ethnic groups in Ethiopia recognize and exploit various enset landraces. Regions in Ethiopia with diverse cultural history have rich biodiversity (Tsegaye 2002). Enset-based farming system is a major agricultural system and farmers cultivate many enset landraces across various climatic and agroecological systems (Borrell et al. 2019). Research on genetic diversity of specific enset accessions from local regions using molecular markers such as amplified fragment length polymorphism (AFLP) (Negash et al. 2002; Tesfamicael et al. 2020), random amplified polymorphic DNA (RAPD) (Birmeta et al. 2004), Inter simple sequence repeats (ISSR) (Tobiaw and Bekele 2011), chloroplast DNA sequences (Bekele and Shigeta 2011), simple sequence repeats (SSR) (Gerura et al. 2019; Getachew et al. 2014; Olango et al. 2015; Biswas et al. 2020; Nuraga et al. 2022) and single nucleotide polymorphisms (SNPs) (Tesfamicael et al. 2020) revealed genetic diversity among and within wild and cultivated enset accessions. SNP markers are powerful tools for estimating genetic similarities and diversity. SNP markers are abundant and robust, suitable for automated high-throughput genotyping of many samples and are able to resolve differences among extremely similar individuals and (...truncated)