CHROMOMETHYLTRANSFERASE3/ KRYPTONITE maintain the sulfurea paramutation in Solanum lycopersicum

Abstract

Paramutation involves the transfer of a repressive epigenetic mark from a silent allele to an active homologue and, consequently, non-Mendelian inheritance. In tomato the sulfurea (sulf) paramutation is associated with a high level of CHG hypermethylation in a region overlapping the transcription start site of the SlTAB2 gene that affects chlorophyll synthesis. The CCG sub-context hypermethylation is under-represented at this region relative to CTG or CAG implicating the CHROMOMETHYLTRANSFERASE3 (CMT3) in paramutation at this locus. Consistent with this interpretation, loss of CMT3 function leads to loss of the sulf chlorosis, the associated CHG hypermethylation and paramutation. Loss of KRYPTONITE (KYP) histone methyl transferase function has a similar effect linked to reduced H3K9me2 at the promoter region of SlTAB2 and a shift in higher order chromatin structure at this locus. Mutation of the largest subunit of RNA polymerase V (PolV) in contrast does not affect sulf paramutation. These findings indicate the involvement of a CMT3/KYP dependent feedback rather than the PolV-dependent pathway leading to RNA directed DNA methylation (RdDM) in the maintenance of paramutation.

Will epigenetics be a key player in crop breeding?

“…A fuller understanding of the similarities and differences between species will allow development of a more accurate general model of the biology of paramutation, than would studies of maize alone (Gouil et al, 2016). This remains an active field of research, with recent progress ranging from studies of the original model, the rogue phenotype in pea (Pereira and Leitão, 2021), to studies in tomato (Martinho et al, 2022), A. thaliana (Bente et al, 2021), and continuing studies in maize (Deans et al, 2020). The studies in cultivated species like pea, tomato, and maize illustrate that paramutation is not just an interesting epigenetic phenomenon but has substantial econom ic and c ultural importance.…”

“…Interestingly, the penetrance of the non-rouge mutation was not complete and paramutation could still be observed in some exceptional cases, indicating that the paramutation system in pea may differ in part from that in maize. Additional examples of continuing genetics progress also demonstrated inter-species functional conservation (Deans et al, 2020;Martinho et al, 2022). Deans et al (2020) demonstrated that the maize ortholog of the A. thaliana PICKLE-like helicase DNA-binding 3 protein, CHD3, plays a role in the maintenance of the purple plant 1 (pl1) paramutant alleles, and also in supporting both normal somatic development and gametophyte function, via the maintenance of hypermethylated "off" states of given alleles.…”

“…Furthermore, since they both function to maintain "off" states, CHDs and the RNA polymerase II catalytic subunit RPD1, which plays a role in generating the small RNAs important to paramutation, are mechanistically linked. Martinho et al (2022) demonstrated that the sulfurea paramutation in the tomato is dependent on the function of the tomato ortholog of A. thaliana's KYP and CMT3. Furthermore, this result indicates that models of paramutation should include CMT3/KYP and its role in changing the chromatin structure, in addition to mechanisms that involve small RNAs and the RdDM pathways, and that these models should accommodate both locus-specific and species-specific mechanisms.…”

An RNA World

“…My lab, at Cambridge University since 2007, continues to be interested in the genetics of epigenetics, and we are exploiting the potential of plant systems to identify features of and cofactors involved in the separate establishment and maintenance phases (41,42,69,75,78,111). Although the biology in our systems is specific to plants, the concepts and some of the mechanisms are common to animals and other organisms (49).…”