Characterization of tomato canal-1 mutant using a multi-omics approach

The recently described canal-1 tomato mutant, which has a variegated leaf phenotype, has been shown to affect canalization of yield. The corresponding protein is orthologous to AtSCO2 - SNOWY COTYLEDON2, which has suggested roles in thylakoid biogenesis. Here we characterize the canal-1 mutant through a multi-omics approach, by comparing mutant to wild-type tissues. While white canal-1 leaves are devoid of chlorophyll, green leaves of the mutant appear wild-type-like, despite an impaired protein function. Transcriptomic data suggest that green mutant leaves compensate for this impaired protein function by upregulation of transcription of photosystem assembly and photosystem component genes, thereby allowing adequate photosystem establishment, which is reflected in their wild-type-like proteome. White canal-1 leaves, however, likely fail to reach a certain threshold enabling this overcompensation, and plastids get trapped in an undeveloped state, while additionally suffering from high light stress, indicated by the overexpression of ELIP homolog genes. The metabolic profile of white and to a lesser degree also green tissues revealed upregulation of amino acid levels, that was at least partially mediated by transcriptional and proteomic upregulation. These combined changes are indicative of a stress response and suggest that white tissues behave as carbon sinks. In summary, our work demonstrates the relevance of the SCO2 protein in both photosystem assembly and as a consequence in the canalization of yield. Significance statementThe variegated canalized-1 tomato mutant was recently described and the underlying gene SCO2 suggested to be a yield canalization gene. Through a multi-omics approach we show that mutants require a transcriptional upregulation of photosystem components and assembly components, likely as overcompensation for partially impaired SCO2 function, to produce a wild type-like proteome and functional photosynthetic tissue Our data, furthermore, suggest that variation of green to white leaf area from plant to plant leads to the yield variation.