The regulatory landscape of a core maize domestication module controlling bud dormancy and growth repression

Dong, Zhaobin; Xiao, Yuguo; Govindarajulu, Rajanikanth; Feil, Regina; Siddoway, Muriel L.; Nielsen, Torrey; Lunn, John E.; Hawkins, Jennifer; Whipple, Clinton; Chuck, George

doi:10.1038/s41467-019-11774-w

Cited by 126 publications

(162 citation statements)

References 79 publications

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“…A recent genome-wide ChIP-seq assay reported that TB1 mainly binds to promoters, and only a few peaks were located within gene body regions 6 . In our study, TEN predominantly bound to the gene body, and this was not unexpected, given that these two genes have diverged over a significant period of evolution.…”

Section: Discussionmentioning

confidence: 99%

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

Yang

Yan

Zhang

et al. 2020

Preprint

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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...

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Section: Discussionmentioning

confidence: 99%

“…Recently, a genome-wide binding profile uncovered a genetic pathway putatively regulated by TB1 6 . The study reported that TB1 binds mainly to promoters, with only a few peaks located within gene body regions.…”

mentioning

confidence: 99%

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

Yang

Yan

Zhang

et al. 2020

Preprint

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“…In isogenic double mutants of Oy1-N1989 allele with gt1 and tb1, vey1 locus that have been previously shown to cause gradual decline in photosynthetic capacity and sugar accumulation of Oy1-N1989 mutants (Khangura et al 2019b) also influenced tiller number in a vey1-dependent manner (Figure 10). A study analyzing young axillary buds of tb1 and gt1 mutants in maize found increased sugar biosynthesis and metabolism to be critical for breaking bud dormancy and that tb1 bound to the promoters of genes encoding enzymes important for energy sensing, such as enzymes involved in trehalose-6-phosphate metabolism (Dong et al 2019). Analysis of transcript abundance in axillary buds of tin1 variants found photosynthesis to be the most enriched gene ontology term and chlorophyll biosynthesis to be highly upregulated in non-dormant tiller buds (Zhang et al 2019).…”

Section: Discussionmentioning

confidence: 99%

Variation in maize chlorophyll biosynthesis alters plant architecture

Khangura

Johal

Dilkes

2020

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Chlorophyll is a tetrapyrrole metabolite essential for photosynthesis in plants. The oil yellow1 (oy1) gene of maize encodes subunit I of Magnesium chelatase, the enzyme catalyzing the first committed step of chlorophyll biosynthesis. A range of chlorophyll contents and net CO2 assimilation rates can be achieved in maize by combining a semi-dominant mutant allele, Oy1-N1989, and cis-regulatory alleles encoded by the Mo17 inbred called very oil yellow1 (vey1). We previously demonstrated that these allelic interactions can delay reproductive maturity. In this study, we demonstrate that multiple gross morphological traits respond to a reduction in chlorophyll. We found that stalk width, number of lateral branches (tillers), and branching of the inflorescence decline with a decrease in chlorophyll level. Chlorophyll variation suppressed tillering in multiple maize mutants including teosinte branched1, grassy tiller1, and Tillering1 as well as the tiller number1 QTL responsible for tillering in many sweet corn varieties. In contrast to these traits, plant height showed a non-linear response to chlorophyll levels. Weak suppression of Oy1-N1989 by vey1 B73 resulted in a significant increase in mutant plant height. This was true in multiple mapping populations, isogenic inbreds, and hybrid backgrounds. Enhancement of the Oy1-N1989 mutants by the vey1 Mo17 allele reduced chlorophyll contents and plant height in mapping populations and isogenic inbred background. We demonstrate that the effects of reduced chlorophyll content on plant growth and development are complex and that the genetic relationship depends on the trait. We propose that growth control for branching and architecture are downstream of energy balance sensing.

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“…There are several examples of class II TCPs regulating plant form in crops; suppression of axillary meristem or tiller outgrowth in grasses by tb1 [25,75], lateral branch angle in maize tassels by wavy auricle on blade 1/ branch angle defective 1 (wab1/ bad1) [76,77], and floral symmetry in sunflower by HaCYC2 [78]. Recently, it was shown that a class II TCP, MULTISEEDED 1 (MSD1), regulates floral fertility and therefore grain number in sorghum, by mediating accumulation of jasmonic acid in the panicle [79].…”

Section: Discussionmentioning

confidence: 99%

The regulatory landscape of early maize inflorescence development

Parvathaneni

Bertolini

Shamimuzzaman

et al. 2019

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The functional genome of agronomically important plant species remains largely unexplored, yet presents a virtually untapped resource for targeted crop improvement. Functional elements of regulatory DNA revealed through profiles of chromatin accessibility can be harnessed for fine-tuning gene expression to optimal phenotypes in specific environments. Here, we investigate the non-coding regulatory space in the maize (Zea mays) genome during early reproductive development of pollen-and grain-bearing inflorescences. Using an assay for differential sensitivity of chromatin to micrococcal nuclease (MNase) digestion, we profiled accessible chromatin and nucleosome occupancy in these largely undifferentiated tissues and classified approximately 1.6 percent of the genome as accessible, with the majority of MNase hypersensitive sites marking proximal promoters, but also 3' ends of maize genes. This approach mapped regulatory elements to footprint-level resolution. Integration of complementary transcriptome profiles and transcription factor (TF) occupancy data were used to annotate regulatory factors, such as combinatorial TF binding motifs and long non-coding RNAs, that potentially contribute to organogenesis, including tissue-specific regulation between male and female inflorescence structures. Finally, genome-wide association studies for inflorescence architecture traits based only on functional regions delineated by MNase hypersensitivity revealed new SNP-trait associations in known regulators of inflorescence development as well as new candidates. These analyses provide a comprehensive look into the cisregulatory landscape during inflorescence differentiation in a major cereal crop, which ultimately shapes architecture and influences yield potential.

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The regulatory landscape of a core maize domestication module controlling bud dormancy and growth repression

Cited by 126 publications

References 79 publications

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

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

Variation in maize chlorophyll biosynthesis alters plant architecture

The regulatory landscape of early maize inflorescence development

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