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1. Antagonizing cis- regulatory elements of a conserved flowering gene mediate developmental robustness

   https://doi.org/10.1073/pnas.2421990122  

   Lanctot, Amy; Hendelman, Anat; Udilovich, Peter; Robitaille, Gina M; Lippman, Zachary B (February 2025, Proceedings of the National Academy of Sciences)

   Developmental transitions require precise temporal and spatial control of gene expression. In plants, such regulation is critical for flower formation, which involves the progressive maturation of stem cell populations within shoot meristems to floral meristems, followed by rapid sequential differentiation into floral organs. Across plant taxa, these transitions are orchestrated by the F-box transcriptional cofactor geneUNUSUAL FLORAL ORGANS(UFO). The conserved and pleiotropic functions ofUFOoffer a useful framework for investigating how evolutionary processes have shaped the intricatecis-regulation of key developmental genes. By pinpointing a conserved promoter sequence in an accessible chromatin region of the tomato ortholog ofUFO, we engineered in vivo a series ofcis-regulatory alleles that caused both loss- and gain-of-function floral defects. These mutant phenotypes were linked to disruptions in predicted transcription factor binding sites for known transcriptional activators and repressors. Allelic combinations revealed dosage-dependent interactions between opposing alleles, influencing the penetrance and expressivity of gain-of-function phenotypes. These phenotypic differences support that robustness in tomato flower development requires precise temporal control ofUFOexpression dosage. Bridging our analysis toArabidopsis, we found that although homologous sequences to the tomato regulatory region are dispersed within theUFOpromoter, they maintain similar control over floral development. However, phenotypes from disrupting these sequences differ due to the differing expression patterns ofUFO. Our study underscores the complexcis-regulatory control of dynamic developmental genes and demonstrates that critical short stretches of regulatory sequences that recruit both activating and repressing machinery are conserved to maintain developmental robustness. 

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2. Idiosyncratic and dose-dependent epistasis drives variation in tomato fruit size

   https://doi.org/10.1126/science.adi5222  

   Aguirre, Lyndsey; Hendelman, Anat; Hutton, Samuel F; McCandlish, David M; Lippman, Zachary B (October 2023, Science)

   Epistasis between genes is traditionally studied with mutations that eliminate protein activity, but most natural genetic variation is in cis-regulatory DNA and influences gene expression and function quantitatively. In this study, we used natural and engineered cis-regulatory alleles in a plant stem-cell circuit to systematically evaluate epistatic relationships controlling tomato fruit size. Combining a promoter allelic series with two other loci, we collected over 30,000 phenotypic data points from 46 genotypes to quantify how allele strength transforms epistasis. We revealed a saturating dose-dependent relationship but also allele-specific idiosyncratic interactions, including between alleles driving a step change in fruit size during domestication. Our approach and findings expose an underexplored dimension of epistasis, in which cis-regulatory allelic diversity within gene regulatory networks elicits nonlinear, unpredictable interactions that shape phenotypes. 

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3. Innovation, conservation, and repurposing of gene function in root cell type development

   https://doi.org/doi.org/10.1016/j.cell.2021.04.024  

   Kaisa, K; Gouran, M.; Shaar-Moshe, L; Mason, G.A.; Rodriguez-Medina, J.; Kawa, D.; Pauluzzi, G.; Reynoso, M.; Canto-Pastor, A.; Manzano, C.; et al (June 2021, Cell)

   Plant species have evolved myriads of solutions, including complex cell type development and regulation, to adapt to dynamic environments. To understand this cellular diversity, we profiled tomato root cell type translatomes. Using xylem differentiation in tomato, examples of functional innovation, repurposing, and conservation of transcription factors are described, relative to the model plant Arabidopsis. Repurposing and innovation of genes are further observed within an exodermis regulatory network and illustrate its function. Comparative translatome analyses of rice, tomato, and Arabidopsis cell populations suggest increased expression conservation of root meristems compared with other homologous populations. In addition, the functions of constitutively expressed genes are more conserved than those of cell type/tissue-enriched genes. These observations suggest that higher order properties of cell type and pan-cell type regulation are evolutionarily conserved between plants and animals. 

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4. Structural variation at the maize WUSCHEL1 locus alters stem cell organization in inflorescences

   https://doi.org/10.1038/s41467-021-22699-8  

   Chen, Zongliang; Li, Wei; Gaines, Craig; Buck, Amy; Galli, Mary; Gallavotti, Andrea (April 2021, Nature Communications)

   Abstract Structural variation in plant genomes is a significant driver of phenotypic variability in traits important for the domestication and productivity of crop species. Among these are traits that depend on functional meristems, populations of stem cells maintained by the CLAVATA-WUSCHEL (CLV-WUS) negative feedback-loop that controls the expression of the WUS homeobox transcription factor. WUS function and impact on maize development and yield remain largely unexplored. Here we show that the maize dominantBarren inflorescence3(Bif3) mutant harbors a tandem duplicated copy of theZmWUS1gene,ZmWUS1-B, whose novel promoter enhances transcription in a ring-like pattern. Overexpression ofZmWUS1-Bis due to multimerized binding sites for type-B RESPONSE REGULATORs (RRs), key transcription factors in cytokinin signaling. Hypersensitivity to cytokinin causes stem cell overproliferation and major rearrangements ofBif3inflorescence meristems, leading to the formation of ball-shaped ears and severely affecting productivity. These findings establishZmWUS1as an essential meristem size regulator in maize and highlight the striking effect of cis-regulatory variation on a key developmental program. 

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5. ERECTA family signaling constrains CLAVATA3 and WUSCHEL to the center of the shoot apical meristem

   https://doi.org/10.1242/dev.189753  

   Zhang, Liang; DeGennaro, Daniel; Lin, Guangzhong; Chai, Jijie; Shpak, Elena D. (March 2021, Development)

   null (Ed.)

   ABSTRACT The shoot apical meristem (SAM) is a reservoir of stem cells that gives rise to all post-embryonic above-ground plant organs. The size of the SAM remains stable over time owing to a precise balance of stem cell replenishment versus cell incorporation into organ primordia. The WUSCHEL (WUS)/CLAVATA (CLV) negative feedback loop is central to SAM size regulation. Its correct function depends on accurate spatial expression of WUS and CLV3. A signaling pathway, consisting of ERECTA family (ERf) receptors and EPIDERMAL PATTERNING FACTOR LIKE (EPFL) ligands, restricts SAM width and promotes leaf initiation. Although ERf receptors are expressed throughout the SAM, EPFL ligands are expressed in its periphery. Our genetic analysis of Arabidopsis demonstrated that ERfs and CLV3 synergistically regulate the size of the SAM, and wus is epistatic to ERf genes. Furthermore, activation of ERf signaling with exogenous EPFLs resulted in a rapid decrease of CLV3 and WUS expression. ERf-EPFL signaling inhibits expression of WUS and CLV3 in the periphery of the SAM, confining them to the center. These findings establish the molecular mechanism for stem cell positioning along the radial axis. 

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