JMJ30‐mediated demethylation of H3K9me3 drives tissue identity changes to promote callus formation in Arabidopsis

Abstract

Plant somatic cells can be reprogrammed by in vitro tissue culture methods, and massive genome-wide chromatin remodeling occurs, particularly during callus formation. Since callus tissue resembles root primordium, conversion of tissue identity is essentially required when leaf explants are used. Consistent with the fact that the differentiation state is defined by chromatin structure, which permits limited gene profiles, epigenetic changes underlie cellular reprogramming for changes to tissue identity. Although a histone methylation process suppressing leaf identity during leaf-to-callus transition has been demonstrated, the epigenetic factor involved in activation of root identity remains elusive. Here, we report that JUMONJI C DOMAIN-CONTAINING PROTEIN 30 (JMJ30) stimulates callus formation by promoting expression of a subset of LATERAL ORGAN BOUNDARIES-DOMAIN (LBD) genes that establish root primordia. The JMJ30 protein binds to promoters of the LBD16 and LBD29 genes along with AUXIN RESPONSE FACTOR 7 (ARF7) and ARF19 and activates LBD expression. Consistently, the JMJ30-deficient mutant displays reduced callus formation with low LBD transcript levels. The ARF-JMJ30 complex catalyzes the removal of methyl groups from H3K9me3, especially at the LBD16 and LBD29 loci to activate their expression during leaf-to-callus transition. Moreover, the ARF-JMJ30 complex further recruits ARABIDOPSIS TRITHORAX-RELATED 2 (ATXR2), which promotes deposition of H3K36me3 at the LBD16 and LBD29 promoters, and the tripartite complex ensures stable LBD activation during callus formation. These results indicate that the coordinated epigenetic modifications promote callus formation by establishing root primordium identity.

Transcriptome Profiling Predicts New Genes to Promote Maize Callus Formation and Transformation

“…In A. thaliana, overexpression of LBD16, LBD17, LBD18, and LBD29 were enough to induce callus with a similar appearance to the callus induced on callus-inducing-medium (Fan et al, 2012). With the exception of the ARF transcription factor, WUSCHEL-related homeobox 11 (WOX11) and JUMONJI C DOMAIN-CONTAINING PROTEIN 30 (JMJ30) can also regulate the LBD genes in A. thaliana (Liu et al, 2014;Lee et al, 2018). It was reported that LBD proteins interact with the basic leucine zipper (bZIP) transcription factor to promote callus formation (Xu et al, 2018).…”

Submergence deactivates wound-induced plant defence against herbivores

“…These results suggest that submergence epigenetically regulates the OPR3 gene to inactivate gene expression before wounding. To find genes responsible for submergence-mediated histone modifications, we analysed expression of the OPR3 gene in the mutants that are deficient in a histone deacetylase ( axe1-5 ) 44 , a histone demethylase ( jmj30-2 ) 45 , and histone methyltransferases ( atx1-2 atx2-1 ) 46 . However, expression of the OPR3 gene in these mutants was similar to that in Col-0 seedlings (Supplementary Fig.…”

Natural Variation in Plant Pluripotency and Regeneration

“…Auxin accumulation in the founder cells mediates degradation of IAA14/SLR, which releases ARF7 and ARF19 that upregulate LBD16-18 and LBD29, involving ATXR2-mediated H3K36me3 deposition [ 4 , 41 , 42 ]. JUMONJI C DOMAIN-CONTAINING PROTEIN 30 (JMJ30) also associates with the ARF-ATXR2 complex to promote LBD expression by removing repressive H3K9me3 marks [ 43 ], while the BRASSINOSTEROID INSENSITIVE 2 (BIN2) kinase integrates temperature sensitivity into this cascade by enhancing the transcriptional activity of ARF7&19 and LBD genes [ 44 ]. In turn, LBD18 reinforces the auxin signal by promoting ARF7&19, and, together with LBD33, it triggers cell proliferation via transcriptional activation of E2 PROMOTER BINDING FACTOR a ( E2Fa ), which associates with DIMERIZATION PARTNERs (DPs) to stimulate DNA replication genes [ 7 , 11 ].…”