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 dominant Barren inflorescence3 (Bif3) mutant harbors a tandem duplicated copy of the ZmWUS1 gene, ZmWUS1-B, whose novel promoter enhances transcription in a ring-like pattern. Overexpression of ZmWUS1-B is 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 of Bif3 inflorescence meristems, leading to the formation of ball-shaped ears and severely affecting productivity. These findings establish ZmWUS1 as an essential meristem size regulator in maize and highlight the striking effect of cis-regulatory variation on a key developmental program.
Highlights
Structural variation in plant genomes is a significant driver of phenotypic variability in traits important for the domestication and productivity of crop species
We showed that this causes striking changes in inflorescence meristem (IM) architecture and leads to extreme stem cell proliferation and the formation of spherical meristems, whereby organizing center (OC), CZ, and peripheral zone (PZ) domains become arranged in concentric circles
Since cytokinin is an essential hormone for meristem maintenance, we examined the expression of the LONELY GUY (LOG)[45] maize co-orthologs
Summary
Structural variation in plant genomes is a significant driver of phenotypic variability in traits important for the domestication and productivity of crop species. By characterization of the dominant maize mutant Barren inflorescence[3] (Bif3) we identified a tandemduplicated copy of ZmWUS1 whose expression is dramatically enhanced by the insertion of a short stretch of chimeric proximal promoter sequence We showed that this causes striking changes in inflorescence meristem (IM) architecture and leads to extreme stem cell proliferation and the formation of spherical meristems, whereby OC, CZ, and PZ domains become arranged in concentric circles. We determined that multimerized binding sites of type-B RR TFs at the duplicated ZmWUS1 locus are the underlying cause of its ectopic expression and promote cytokinin hypersensitivity These findings refine the gene-regulatory network of maize meristems placing ZmWUS1 at the center of vegetative and reproductive meristem size regulation, enhancing our ability to exploit variation in the CLV-WUS pathway for diverse agricultural traits and for fast and efficient transformation systems
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