Development in higher plants depends on the activity of meristems, formative regions that continuously initiate new organs at their flanks. Meristems must maintain a balance between stem cell renewal and organ initiation. In fasciated mutants, organ initiation fails to keep pace with meristem proliferation. The thick tassel dwarf1 (td1) mutation of maize affects both male and female inflorescence development. The female inflorescence, which results in the ear, is fasciated, with extra rows of kernels. The male inflorescence, or tassel, shows an increase in spikelet density. Floral meristems are also affected in td1 mutants; for example, male florets have an increase in stamen number. These results suggest that td1 functions in the inflorescence to limit meristem size. In addition, td1 mutants are slightly shorter than normal siblings, indicating that td1 also plays a role in vegetative development. td1 encodes a leucine-rich repeat receptorlike kinase (LRR-RLK) that is a putative ortholog of the Arabidopsis CLAVATA1 protein. These results complement previous work showing that fasciated ear2 encodes a CLAVATA2-like protein, and suggest that the CLAVATA signaling pathway is conserved in monocots. td1 maps in the vicinity of quantitative trait loci that affect seed row number, spikelet density and plant height. We discuss the possible selection pressures on td1 during maize domestication.Key words: Meristem, Stem cells, Inflorescence, thick tassel dwarf1, Maize Summary thick tassel dwarf1 encodes a putative maize ortholog of the Arabidopsis
Missouri 63121 (S.M., E.K.)Organogenesis in plants is controlled by meristems. Axillary meristems, which give rise to branches and flowers, play a critical role in plant architecture and reproduction. Maize (Zea mays) and rice (Oryza sativa) have additional types of axillary meristems in the inflorescence compared to Arabidopsis (Arabidopsis thaliana) and thus provide an excellent model system to study axillary meristem initiation. Previously, we characterized the barren inflorescence2 (bif2) mutant in maize and showed that bif2 plays a key role in axillary meristem and lateral primordia initiation in the inflorescence. In this article, we cloned bif2 by transposon tagging. Isolation of bif2-like genes from seven other grasses, along with phylogenetic analysis, showed that bif2 is a co-ortholog of PINOID (PID), which regulates auxin transport in Arabidopsis. Expression analysis showed that bif2 is expressed in all axillary meristems and lateral primordia during inflorescence and vegetative development in maize and rice. Further phenotypic analysis of bif2 mutants in maize illustrates additional roles of bif2 during vegetative development. We propose that bif2/PID sequence and expression are conserved between grasses and Arabidopsis, attesting to the important role they play in development. We provide further support that bif2, and by analogy PID, is required for initiation of both axillary meristems and lateral primordia.
Plant architecture is dictated by precise control of meristematic activity. In the shoot, an imbalance in positive or negative maintenance signals can result in a fasciated or enlarged meristem phenotype. fasciated ear4 (fea4) is a semidwarfed mutant with fasciated ears and tassels as well as greatly enlarged vegetative and inflorescence meristems. We identified FEA4 as a bZIP transcription factor, orthologous to Arabidopsis thaliana PERIANTHIA. FEA4 was expressed in the peripheral zone of the vegetative shoot apical meristem and in the vasculature of immature leaves and conspicuously excluded from the stem cell niche at the tip of the shoot apical meristem and from incipient leaf primordia. Following the transition to reproductive fate, FEA4 was expressed throughout the entire inflorescence and floral meristems. Native expression of a functional YFP:FEA4 fusion recapitulated this pattern of expression. We used chromatin immunoprecipitation-sequencing to identify 4060 genes proximal to FEA4 binding sites, including ones that were potentially bound and modulated by FEA4 based on transcriptional changes in fea4 mutant ears. Our results suggest that FEA4 promotes differentiation in the meristem periphery by regulating auxin-based responses and genes associated with leaf differentiation and polarity, potentially in opposition to factors such as KNOTTED1 and WUSCHEL.
One-sentence summary: Maize GIF1 promotes meristematic function in leaves and stems but restricts indeterminacy in the inflorescence by regulating the expression of several known inflorescence architecture-related genes.The authors responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantcell.org) are: Zuxin Zhang (zuxinzhang@mail.hzau.edu.cn) and Sarah Hake (hake@berkeley.edu). ABSTRACTPlant architecture results from a balance of indeterminate and determinate cell fates. Cells with indeterminate fates are located in meristems, comprising groups of pluripotent cells that produce lateral organs. Meristematic cells are also found in intercalary stem tissue, which provides cells for internodes, and at leaf margins to contribute to leaf width. We identified a maize (Zea mays) mutant that has a defect in balancing determinacy and indeterminacy. The mutant has narrow leaves and short internodes, suggesting a reduction in indeterminate cells in the leaf and stem. In contrast, the mutants fail to control indeterminacy in shoot meristems. Inflorescence meristems are fasciated, and determinate axillary meristems become indeterminate. Positional cloning identified growth regulating factor-interacting factor1 (gif1) as the responsible gene. gif1 mRNA accumulates in distinct domains of shoot meristems, consistent with tissues affected by the mutation. We determined which GROWTH REGULATING FACTORs (GRFs) interact with GIF1 and carried out RNA-seq analysis. Many genes known to play roles in inflorescence architecture were differentially expressed in gif1. Chromatin immunoprecipitation identified some differentially expressed genes as direct targets of GIF1. The interactions with these
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