A non-canonical histone acetyltransferase targets intragenic enhancers and regulates plant architecture

Abstract

31Axillary meristem development determines both plant architecture and crop yield; this 32 critical process is regulated by the TCP transcription factor (TF) family, including the 33 maize TB1 and Arabidopsis BRC1. Studies have shown that both TB1 and AtBRC1 can 34 target the gene body regions of some target genes and activate their expression; 35 however, the regulatory mechanisms remain largely unknown. Here, we show that a 36 cucumber CYC/TB1 homologue, TEN, controls the identity and mobility of tendrils. 37Through its C-terminus, TEN binds at intragenic enhancers of target genes; its N-38 terminal domain functions as a novel, non-canonical histone acetyltransferase (HAT) 39 to preferentially act on lysine 56 and 122, of the histone H3 globular domain. This HAT 40 activity is responsible for chromatin loosening and host gene activation. The N-termini 41 of all tested CYC/TB1-like proteins contain an intrinsically disordered region (IDR), 42 and despite their sequence divergence, they have conserved HAT activity. This study 43 discovered a non-canonical class of HATs, and as well, provides a mechanism by which 44 modification at the H3 globular domain is integrated with the transcription process. 45 4 TEOSINTE BRANCHED 1 (TB1), CYCLOIDEA (CYC), and PROLIFERATING 46 CELL FACTORS (TCP) transcription factors (TFs) constitute a plant-specific gene 47 family involved in a broad range of developmental processes 1 . Among them, the 48 CYC/TB1 clade of the TCP proteins plays central roles in controlling development of 49 axillary buds that give rise to either flowers or lateral shoots 1,2 . In maize (Zea mays L.), 50 the major domestication gene, TB1, suppresses branch outgrowth, a crucial 51 architectural modification that transformed teosinte into a viable crop 3 . Subsequent 52 studies on its homologues in rice 4 and Arabidopsis thaliana 5 identified their similar 53 essential roles in repressing axillary bud growth. 54Recently, a genome-wide binding profile uncovered a genetic pathway putatively 55 regulated by TB1 6 . The study reported that TB1 binds mainly to promoters, with only 56 a few peaks located within gene body regions. Nevertheless, other studies have also 57 shown that TB1, and its homologue BRANCHED1 in Arabidopsis, can bind to the gene 58 bodies of the target genes Tassels Replace Upper Ears1 (Tru1) 7 and HOMEOBOX 59 PROTEIN53 8 , respectively, to activate their expression. However, the mechanism 60 underlying how the intragenic binding of CYC/TB1-like TFs regulates gene expression 61 is still unclear. Understanding the conserved regulatory mechanism, associated with the 62 function of these CYC/TB1-like proteins, would provide insight into their core role in 63 signal integration of axillary bud repression. Such knowledge could broadly benefit 64 crop breeding programs for tailored plant architecture. 65In eukaryotes, enhancers are cis-acting DNA sequences which, when bound by 66 specific TFs, increase the transcription in a manner that is independent of their 67 orientation and distance relative to...

A gene regulatory network critical for axillary bud dormancy directly controlled by Arabidopsis BRANCHED1

“…This distribution was comparable to that found for ChIP-seq performed on other Arabidopsis TFs (e.g. 12,13 ), but divergent from that described for cucumber TEN, a closely related TCP factor, for which a large proportion of binding sites are localised in gene bodies 14 .…”