Gynandropsis gynandra (Spider plant) is an African leafy vegetable rich in minerals, vitamins, and health-promoting compounds with great potential in addressing malnutrition. The species is used as food and medicine and provides substantial incomes for smallholder’s farmers with an increasing interest for its cultivation in Africa. Spider plant is also an important resource for pharmaceutical industries. However, its production is still hampered by low leaf yield, early flowering, pests and disease and poor seed germination, resulting from the lack of improved cultivars. Our study intended to develop high yielding and nutrient-dense cultivars for farmers through merging modern molecular and classical plant breeding tools to increase income generation and improve nutrition and health. Specifically, the study: i) assessed the phenotypic variability among advanced lines of spider plant using biomass and related traits; ii) profiled the leaf mineral content among advanced lines of G. gynandra; iii) determined the combining ability, gene action and heterosis of mineral content in spider plant; iv) identified the genetics of the inheritance of biomass and related traits in spider plant; and v) deciphered genomic regions associated with combining ability and heterosis of biomass and related traits in G. gynandra. The evaluation of 71 advanced lines of spider plant derived from accessions originating from Asia, East, Southern and West Africa using biomass and related traits revealed significant difference among lines and principal component analysis grouped them into three clusters: Asia (Cluster 1), West Africa (Cluster 2), and East/Southern Africa (Cluster 3). The West and East/Southern African groups were comparable in biomass productivity and superior to the Asian group. Specifically, the West African group had high dry matter content and flowered early while the East/Southern African group was characterized by broad leaves and late flowering. The maintenance of lines’ membership to their group of origin strengthens the hypothesis of geographical signature in cleome diversity as genetic driver of the observed variation. The leaf mineral profile of 70 advanced lines of spider plant derived from accessions originating from Asia, East, Southern and West Africa revealed significant variation among lines and zinc, calcium, phosphorus, copper, magnesium, and manganese as landmark elements in the genotypes. East and Southern African genotypes were clustered together in group 1 with higher phosphorus, copper and zinc contents than Asian and West African lines, which clustered in group 2 and were characterized by higher calcium, magnesium and manganese contents. An additional outstanding group 3 of six genotypes (three, two, and one from Asia, Southern Africa and Eastern Africa, respectively) was identified with high iron, zinc, magnesium, manganese and calcium contents and potential candidates for cultivar release. Significant differences (P < 0.001) were observed among and between experimental hybrids and parents for the levels of all mineral contents. Significant general and specific combining ability effects together with variance components analysis revealed that both additive and nonadditive gene action controlled mineral content with a predominance of nonadditive gene action. Mid- and best-parent heterosis ranged from -84.98 and 404.79% for minerals. Parents with good general combining ability were identified, as well as crosses with high specific combining ability and heterosis. There were significant and moderate to strong correlations between mean hybrid performance, specific combining ability effects and heterosis levels and low to moderate correlations between general combining ability and mean parents’ performance. Similar to leaf mineral content, significant differences (P < 0.001) were observed among and between hybrids and parents for fourteen agronomic traits. Hybrids outperformed their parents with more than 50% for total and edible fresh biomass, showing the existence of hybrid vigour. Mid- and best-parent heterosis varied between -51.89% and 192.10% with only positive heterosis effects for leaf area and total fresh biomass, characterized by an average mid-parent heterosis greater than 50%. Significant general and specific combining ability (GCA and SCA) effects together with variance component analysis revealed that both additive and nonadditive gene action, controlled biomass and related traits in the species with the predominance of additive gene action. Moderate to high broad- and narrow-sense heritability was observed for most agronomic traits, except for dry matter content. The environment significantly interacted with genotype, GCA and SCA. Parents with good GCA and crosses with high SCA and heterosis were identified. There were significant changes from parents to hybrids in the association of harvest index and time to 50% flowering with biomass per plant and leaf traits on the one hand and between harvest index and dry matter content on the other hand. A core set of 594 diversity array technology sequencing (DArt-seq) markers were identified and differentiated the 38 parental lines into three clusters linked with the provenance of the original accession. Using this set of markers, a genome-wide association analysis revealed two markers linked to heterosis level for flowering time, a single marker for edible biomass, one marker for total fresh biomass and one marker for the number of primary branches. Specifically, the marker MABiomLa1 was a pleiotropic marker and was associated with heterosis level for biomass and leaf area. In contrast, no consistent markers associated with combining ability were observed for general combining ability and might be due to the low number of parents and the density of markers used. The study thus revealed that reciprocal recurrent selection would be a sound breeding strategy for G. gynandra improvement with the development of hybrid cultivars to exploit heterosis. These findings showed that G. gynandra could be used as a model plant to study the genetic mechanism underlying heterosis in orphan leafy vegetables. The identified markers open room for implementing marker-assisted selection in the species for better exploitation of heterosis.

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