Defying Mendel's laws: sulfurea paramutation unveils new principles of epigenetic inheritance in tomato

Paramutation represents a clear exception to the principles of inheritance established by Gregor Mendel in the 19th century. It involves the transfer of repressive epigenetic marks from a silent to an active allele and thereby violates Mendel's first law of independent allele segregation. By violating Mendel's first law of independent allele segregation, paramutation results from the transfer of repressive epigenetic marks from silent to active homologous alleles. It is best known from conspicuous pigmentation phenotypes in maize but the Paramutation phenomena was also reported across diverse plant and animal species. Paramutation-like events are common in tomato hybrids suggesting that paramutation may be less exceptional and rather a frequently co-occurring process during cross-hybridisation.

Here we use the classic example of paramutation in tomato – sulfurea (sulf), an understudied chlorosis phenotype associated with transgenerationally dependent allele segregation patterns – to dissect the epigenetic- and transgenerational mechanisms underlying paramutation in tomato plants. Our results show that the DNA- and histone-methyl transferases CMT3 and KYP are required for the maintenance of paramutation and that there is a change in chromatin architecture associated with the silent epiallele. We further demonstrate that in tomato the developmental and transgenerational maintenance of paramutation might be independent of sRNAs, which were previously suggested to explain the trans-communication between homologues as well as the maintenance of silent paramutated states across mitotic and meiotic divisions in maize. Together, our data significantly extends the current understanding of the paramutation model in plants by integrating existing concepts into a revised framework of non-Mendelian heredity.