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SUMMARY WUSCHEL (WUS) is transcription factor vital for stem cell proliferation in plant meristems. In maize,ZmWUS1is expressed in the inflorescence meristem, including the central zone, the reservoir of stem cells.ZmWUS1overexpression in theBarren inflorescence3mutant leads to defects in inflorescence development. Here, single-cell ATAC-seq analysis shows thatZmWUS1overexpression alters chromatin accessibility throughout the central zone. The CAATAATGC motif, a known homeodomain recognition site, is predominantly observed in the regions with increased chromatin accessibility suggesting ZmWUS1 is an activator in the central zone. Regions with decreased chromatin accessibility feature various motifs and are adjacent toAUXIN RESPONSE FACTORgenes, revealing negative regulation of auxin signaling in the central zone. DAP-seq of ZmWUS1 identified the TGAATGAA motif, abundant in epidermal accessible chromatin compared to the central zone. These findings highlight ZmWUS1’s context-dependent mechanisms for stem cell maintenance in the inflorescence meristem. 

ABSTRACT The formation of the plant body proceeds in a sequential post-embryonic manner through the action of meristems. Tightly coordinated meristem regulation is required for development and reproductive success, eventually determining yield in crop species. In maize, the REL2 family of transcriptional corepressors includes four members, REL2, RELK1 (REL2-LIKE1), RELK2, and RELK3. In a screen forrel2enhancers, we identified shorter double mutants with enlarged female inflorescence meristems (IMs) carrying mutations inRELK1. Expression and genetic analysis indicate thatREL2andRELK1cooperatively regulate female IM development by controlling genes involved in redox balance, hormone homeostasis, and differentiation, ultimately tipping the meristem toward an environment favorable to expanded expression of theZmWUSCHEL1gene, a key stem-cell promoting transcription factor. We further demonstrate thatRELKgenes have partially redundant yet diverse functions in the maintenance of various meristem types during development. By exploiting subtle increases in ear IM size inrel2heterozygous plants, we also show that extra rows of kernels are formed across a diverse set of F1 hybrids. Our findings reveal that the REL2 family maintains development from embryonic initiation to reproductive growth and can potentially be harnessed for increasing seed yield in a major crop species. One sentence summaryREL2-RELKs fine tune hormone and chemical cues to prevent expanded expression of ZmWUSCHEL1 in maize inflorescence meristems, and can potentially be harnessed for increasing seed yield in hybrids. 

Abstract The formation of the plant body proceeds in a sequential postembryonic manner through the action of meristems. Tightly coordinated meristem regulation is required for development and reproductive success, eventually determining yield in crop species. In maize (Zea mays), the RAMOSA1 ENHANCER LOCUS2 (REL2) family of transcriptional corepressors includes four members, REL2, RELK1 (REL2-LIKE1), RELK2, and RELK3. In a screen for rel2 enhancers, we identified shorter double mutants with enlarged ear inflorescence meristems (IMs) carrying mutations in RELK1. Expression and genetic analysis indicated that REL2 and RELK1 cooperatively regulate ear IM development by controlling genes involved in redox balance, hormone homeostasis, and differentiation, ultimately tipping the meristem toward an environment favorable to expanded expression of the ZmWUSCHEL1 gene, which encodes a key stem-cell promoting transcription factor. We further demonstrated that RELK genes have partially redundant yet diverse functions in the maintenance of various meristem types during development. By exploiting subtle increases in ear IM size in rel2 heterozygous plants, we also showed that extra rows of kernels are formed across a diverse set of F1 hybrids. Our findings reveal that the REL2 family maintains development from embryonic initiation to reproductive growth and can potentially be harnessed for increasing seed yield in a major crop species. 

Abstract Mutations in cis-regulatory regions play an important role in the domestication and improvement of crops by altering gene expression. However, assessing the in vivo impact of cis-regulatory elements (CREs) on transcriptional regulation and phenotypic outcomes remains challenging. Previously, we showed that the dominant Barren inflorescence3 (Bif3) mutant of maize (Zea mays) contains a duplicated copy of the homeobox transcription factor gene ZmWUSCHEL1 (ZmWUS1), named ZmWUS1-B. ZmWUS1-B is controlled by a spontaneously generated novel promoter region that dramatically increases its expression and alters patterning and development of young ears. Overexpression of ZmWUS1-B is caused by a unique enhancer region containing multimerized binding sites for type B RESPONSE REGULATORs (RRs), key transcription factors in cytokinin signaling. To better understand how the enhancer increases the expression of ZmWUS1 in vivo, we specifically targeted the ZmWUS1-B enhancer region by CRISPR-Cas9-mediated editing. A series of deletion events with different numbers of type B RR DNA binding motifs (AGATAT) enabled us to determine how the number of AGATAT motifs impacts in vivo expression of ZmWUS1-B and consequently ear development. In combination with dual-luciferase assays in maize protoplasts, our analysis reveals that AGATAT motifs have an additive effect on ZmWUS1-B expression, while the distance separating AGATAT motifs does not appear to have a meaningful impact, indicating that the enhancer activity derives from the sum of individual CREs. These results also suggest that in maize inflorescence development, there is a threshold of buffering capacity for ZmWUS1 overexpression. 

Abstract The domestication and improvement of maize resulted in radical changes in shoot architecture relative to its wild progenitor teosinte. In particular, critical modifications involved a reduction of branching and an increase in inflorescence size to meet the needs for human consumption and modern agricultural practices. Maize is a major contributor to global agricultural production by providing large and inexpensive quantities of food, animal feed, and ethanol. Maize is also a classic system for studying the genetic regulation of inflorescence formation and its enlarged female inflorescences directly influence seed production and yield. Studies on the molecular and genetic networks regulating meristem proliferation and maintenance, including receptor-ligand interactions, transcription factor regulation, and hormonal control, provide important insights into maize inflorescence development and reveal potential avenues for the targeted modification of specific architectural traits. In this review, we summarize recent findings on the molecular mechanisms controlling inflorescence formation and discuss how this knowledge can be applied to improve maize productivity in the face of present and future environmental challenges. 

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.