Conserved pleiotropy of an ancient plant homeobox gene uncovered by cis-regulatory dissection

Hendelman, Anat; Zebell, Sophia G.; Rodríguez-Leal, Daniel; Dukler, Noah; Robitaille, Gina; Wu, Xuelin; Kostyun, Jamie L.; Tal, Lior; Wang, Peipei; Bartlett, Madelaine; Eshed, Yuval; Efroni, Idan; Lippman, Zachary B.

doi:10.1016/j.cell.2021.02.001

Cited by 116 publications

(87 citation statements)

References 104 publications

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“…Indeed, with the rapid development of CRISPR/Cas9 technology, it is now possible to apply genome editing to noncoding cis-elements [ 35 ]. In a recent report, cis-regulatory mutagenesis via CRISPR/Cas9 in a plant homeobox gene uncovered the pleiotropy in plant architecture [ 36 ]. Quantitative trait locus (QTL) mapping studies or genome-wide association studies (GWASs) usually focus on the coding genes for elucidating causal polymorphisms.…”

Section: Discussionmentioning

confidence: 99%

Genomic Features of Open Chromatin Regions (OCRs) in Wild Soybean and Their Effects on Gene Expressions

Huang

Zhang

Zhou

et al. 2021

Genes

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Transcription activation is tightly associated with the openness of chromatin, which allows direct contact between transcriptional regulators, such as transcription factors, and their targeted DNA for downstream gene activation. However, the annotation of open chromatin regions (OCRs) in the wild soybean (Glycine soja) genome is limited. We performed assay for transposase-accessible chromatin using sequencing (ATAC-seq) and successfully identified 22,333 OCRs in the leaf of W05 (a wild soybean accession). These OCRs were enriched in gene transcription start sites (TSS) and were positively correlated with downstream gene expression. Several known transcription factor (TF)-binding motifs were also enriched at the OCRs. A potential regulatory network was constructed using these transcription factors and the OCR-marked genes. Furthermore, by overlapping the OCR distribution with those of histone modifications from chromatin immunoprecipitation followed by sequencing (ChIP-seq), we found that the distribution of the activation histone mark, H3K4me3, but not that of the repressive H3K27me3 mark, was closely associated with OCRs for gene activation. Several putative enhancer-like distal OCRs were also found to overlap with LincRNA-encoding loci. Moreover, our data suggest that homologous OCRs could potentially influence homologous gene expression. Hence, the duplication of OCRs might be essential for plant genome architecture as well as for regulating gene expression.

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Section: Discussionmentioning

confidence: 99%

Genomic Features of Open Chromatin Regions (OCRs) in Wild Soybean and Their Effects on Gene Expressions

Huang

Zhang

Zhou

et al. 2021

Genes

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“…This delay in meristem maturation causes individual apical meristems to release more than one lateral inflorescence meristem, which results in the development of branch points in the s mutant inflorescence ( Lippman et al, 2008 ; Park et al, 2012 ). Complete loss of S/SlWOX9 activity in apical meristems results in an arrest of meristem maturation and excessive overproliferation of inflorescence meristems on cauliflower-like inflorescence tissue, demonstrating that S/SlWOX9 is essential for inflorescence meristem differentiation ( Park et al, 2012 ; Rodríguez-Leal et al, 2017 ; Hendelman et al, 2021 ). S/SlWOX9 activity is required for the proper expression of ANANTHA (AN) , which is a homolog of Arabidopsis UNUSUAL FLORAL ORGANS and encodes an F-box protein that interacts with the transcription factor FA to form a floral specification complex and trigger floral differentiation ( Allen and Sussex, 1996 ; Lippman et al, 2008 ).…”

Section: Optimizing Inflorescence Architecture By Tuning the Rate Of Meristem Maturationmentioning

confidence: 99%

Meristem transitions and plant architecture—learning from domestication for crop breeding

2021

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“…This deep homology of plant organs suggests that there may be additional cases of developmental genes seemingly functioning in discrete contexts, but whose pleiotropy is masked. Indeed, thorough genetic and phenotypic analyses continue to expose pleiotropy of developmental regulators (63)(64)(65)(66)(67). Recent examples include WUSCHEL-like HOMEOBOX9 (WOX9), which controls both inflorescence branching and embryo development (66), and THORN IDENTITY1, which controls thorn development and branching in citrus (67).…”

Section: Discussionmentioning

confidence: 99%

“…Indeed, thorough genetic and phenotypic analyses continue to expose pleiotropy of developmental regulators (63)(64)(65)(66)(67). Recent examples include WUSCHEL-like HOMEOBOX9 (WOX9), which controls both inflorescence branching and embryo development (66), and THORN IDENTITY1, which controls thorn development and branching in citrus (67). Detailed dissection of gene function -alone, in the context of other genes, and in different developmental contexts -is likely to reveal that this pleiotropy is widespread.…”

Section: Discussionmentioning

confidence: 99%

Recruitment of an ancient branching program to suppress carpel development in maize flowers

Klein

Gallagher

Demesa-Arévalo

et al. 2021

Preprint

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Floral morphology is immensely diverse. One developmental process acting to shape this diversity is growth suppression. For example, grass flowers exhibit extreme diversity in floral sexuality, arising through differential suppression of stamens or carpels. In maize, carpels undergo programmed cell death in half of the flowers initiated in ears and in all flowers in tassels. The HD-ZIP I transcription factor gene GRASSY TILLERS1 (GT1) is one of only a few genes known to regulate this process. To identify additional regulators of carpel suppression, we performed a gt1 enhancer screen, and found a genetic interaction between gt1 and ramosa3 (ra3). RA3 is a classic inflorescence meristem determinacy gene that encodes a trehalose-6-phosphate (T6P) phosphatase (TPP). Dissection of floral development revealed that ra3 single mutants have partially derepressed carpels, whereas gt1; ra3 double mutants have completely derepressed carpels. Surprisingly, gt1 suppresses ra3 inflorescence branching, revealing a role for gt1 in meristem determinacy. Supporting these genetic interactions, GT1 and RA3 proteins colocalize to carpel nuclei in developing flowers. Global expression profiling revealed common genes misregulated in single and double mutant flowers, as well as in derepressed gt1 axillary meristems. Indeed, we found that ra3 enhances gt1 vegetative branching, similar to the roles for the trehalose pathway and GT1 homologs in the eudicots. This functional conservation over ~160 million years of evolution reveals ancient roles for GT1-like genes and the trehalose pathway in regulating axillary meristem suppression, later recruited to mediate carpel suppression. Our findings expose hidden pleiotropy of classic maize genes, and show how an ancient developmental program was redeployed to sculpt floral form.

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Conserved pleiotropy of an ancient plant homeobox gene uncovered by cis-regulatory dissection

Cited by 116 publications

References 104 publications

Genomic Features of Open Chromatin Regions (OCRs) in Wild Soybean and Their Effects on Gene Expressions

Genomic Features of Open Chromatin Regions (OCRs) in Wild Soybean and Their Effects on Gene Expressions

Meristem transitions and plant architecture—learning from domestication for crop breeding

Recruitment of an ancient branching program to suppress carpel development in maize flowers

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