Heterosis for capsacinoids accumulation in chili pepper hybrids is dependent on parent-of-origin effect

Heterosis for agronomic traits is a widespread phenomenon that underpins hybrid crop breeding. However, heterosis at the level of cellular metabolites has not yet been fully explored. Some metabolites are highly sought after, like capsaicinoids found in peppers of the Capsicum genus, which confer the characteristic pungent (‘hot’) flavour of the fruits. We analysed the metabolic profile of the fruit placenta and pericarp of inter- and intra-specific hybrids of two species of Capsicum peppers, C. chinense (cv. Habanero and cv. Biquinho) and C. annuum var. annuum (cv. Jalapeño and cv. Cascadura Ikeda) in complete diallel crosses with reciprocals. The parents and hybrids were grown in a glasshouse and the profile of primary metabolites (sugars, amino acids and organic acids) and capsaicinoids was generated via gas chromatography–time of flight-mass spectrometry (GC–TOF-MS) and ultra-performance liquid chromatography coupled to a mass spectrometer (UPLC-MS), respectively. We found considerable heterotic effects specifically for capsaicinoids accumulation in the fruit placenta of the hybrids, including those derived from non-pungent parents. Furthermore, a large fraction of fruit primary metabolism was influenced by the specific cross combination, with marked parent-of-origin effects, i.e. whether a specific genotype was used as the pistillate or pollen parent. The differences in metabolite levels between the hybrids and their parents provide a snapshot of heterosis for primary and secondary metabolites and may contribute to explain the manifestation of whole-plant heterotic phenotypes.