thick tassel dwarf1 encodes a putative maize ortholog of the Arabidopsis CLAVATA1 leucine-rich repeat receptor-like kinase

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 receptor-like 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.     

ARABIDOPSIS THALIANA HOMEOBOX GENE1 establishes the basal boundaries of shoot organs and controls stem growth

Apical meristems play a central role in plant development. Self-renewing cells in the central region of the shoot meristem replenish the cell population in the peripheral region, where organ primordia emerge in a predictable pattern, and in the underlying rib meristem, where new stem tissue is formed. While much is known about how organ primordia are initiated and their lateral boundaries established, development at the interface between the stem and the meristem or the lateral organs is poorly understood. Here, we show that the BELL-type ARABIDOPSIS THALIANA HOMEOBOX GENE1 (ATH1) is required for proper development of the boundary between the stem and both vegetative and reproductive organs and that this role partially overlaps with that of CUP-SHAPED COTYLEDON genes. During the vegetative phase, ATH1 also functions redundantly with light-activated genes to inhibit growth of the region below the shoot meristem. Consistent with a role in inhibiting stem growth, ATH1 is downregulated at the start of inflorescence development and ectopic ATH1 expression prevents growth of the inflorescence stem by reducing cell proliferation. Thus, ATH1 modulates growth at the interface between the stem, meristem, and organ primordia and contributes to the compressed vegetative habit of Arabidopsis thaliana.     

MOSAIC FLORAL ORGANS1, an AGL6-Like MADS Box Gene,Regulates Floral Organ Identity and Meristem Fate in Rice

Floral organ identity and meristem determinacy in plants are controlled by combinations of activities mediated by MADS box genes. AGAMOUS-LIKE6 (AGL6)-like genes are MADS box genes expressed in floral tissues, but their biological functions are mostly unknown. Here, we describe an AGL6-like gene in rice (Oryza sativa), MOSAIC FLORAL ORGANS1 (MFO1/MADS6), that regulates floral organ identity and floral meristem determinacy. In the flower of mfo1 mutants, the identities of palea and lodicule are disturbed, and mosaic organs were observed. Furthermore, the determinacy of the floral meristem was lost, and extra carpels or spikelets developed in mfo1 florets. The expression patterns of floral MADS box genes were disturbed in the mutant florets. Suppression of another rice AGL6-like gene, MADS17, caused no morphological abnormalities in the wild-type background, but it enhanced the phenotype in the mfo1 background, indicating that MADS17 has a minor but redundant function with that of MFO1. Whereas single mutants in either MFO1 or the SEPALLATA-like gene LHS1 showed moderate phenotypes, the mfo1 lhs1 double mutant showed a severe phenotype, including the loss of spikelet meristem determinacy. We propose that rice AGL6-like genes help to control floral organ identity and the establishment and determinacy of the floral meristem redundantly with LHS1.     

Expression of knotted1 marks shoot meristem formation during maize embryogenesis

The formation of shoot and root meristems that ultimately give rise to all tissues of the plant body occurs for the first time during embryogenesis. Meristem formation has traditionally been defined in terms of the appearance of histological features of meristems; this approach has led to varying interpretations of the timing of meristem formation relative to other events in embryogenesis. Markers that would provide more objective criteria for the analysis of meristem formation have not been widely available. The maize homeobox gene, knotted1 (kn1), is expressed in shoot meristems throughout postembryonic stages of shoot development. In order to determine whether this gene is expressed in the shoot meristem from its earliest inception, we examined the expression of kn1 in embryos at a series of stages by in situ hybridization to kn1 mRNA and immunolocalization of KN1 protein. Our results show that the onset of kn1 expression is temporally and spatially coincident with the earliest histologically recognizable signs of shoot meristem formation in the embryo, and thus provides a valuable marker for this process. © 1995 Wiley-Liss, Inc.     

L1 division and differentiation patterns influence shoot apical meristem maintenance

Plant development requires regulation of both cell division and differentiation. The class 1 KNOTTED1-like homeobox (KNOX) genes such as knotted1 (kn1) in maize (Zea mays) and SHOOTMERISTEMLESS in Arabidopsis (Arabidopsis thaliana) play a role in maintaining shoot apical meristem indeterminacy, and their misexpression is sufficient to induce cell division and meristem formation. KNOX overexpression experiments have shown that these genes interact with the cytokinin, auxin, and gibberellin pathways. The L1 layer has been shown to be necessary for the maintenance of indeterminacy in the underlying meristem layers. This work explores the possibility that the L1 affects meristem function by disrupting hormone transport pathways. The semidominant Extra cell layers1 (Xcl1) mutation in maize leads to the production of multiple epidermal layers by overproduction of a normal gene product. Meristem size is reduced in mutant plants and more cells are incorporated into the incipient leaf primordium. Thus, Xcl1 may provide a link between L1 division patterns, hormonal pathways, and meristem maintenance. We used double mutants between Xcl1 and dominant KNOX mutants and showed that Xcl1 suppresses the Kn1 phenotype but has a synergistic interaction with gnarley1 and rough sheath1, possibly correlated with changes in gibberellin and auxin signaling. In addition, double mutants between Xcl1 and crinkly4 had defects in shoot meristem maintenance. Thus, proper L1 development is essential for meristem function, and XCL1 may act to coordinate hormonal effects with KNOX gene function at the shoot apex.     

DEAD-BOX RNA HELICASE 27 regulates microRNA biogenesis,zygote division,and stem cell homeostasis

After double fertilization, zygotic embryogenesis initiates a new life cycle, and stem cell homeostasis in the shoot apical meristem (SAM) and root apical meristem (RAM) allows plants to produce new tissues and organs continuously. Here, we report that mutations in DEAD-BOX RNA HELICASE 27 (RH27) affect zygote division and stem cell homeostasis in Arabidopsis (Arabidopsis thaliana). The strong mutant allele rh27-1 caused a zygote-lethal phenotype, while the weak mutant allele rh27-2 led to minor defects in embryogenesis and severely compromised stem cell homeostasis in the SAM and RAM. RH27 is expressed in embryos from the zygote stage, and in both the SAM and RAM, and RH27 is a nucleus-localized protein. The expression levels of genes related to stem cell homeostasis were elevated in rh27-2 plants, alongside down-regulation of their regulatory microRNAs (miRNAs). Further analyses of rh27-2 plants revealed reduced levels of a large subset of miRNAs and their pri-miRNAs in shoot apices and root tips. In addition, biochemical studies showed that RH27 associates with pri-miRNAs and interacts with miRNA-biogenesis components, including DAWDLE, HYPONASTIC LEAVES 1, and SERRATE. Therefore, we propose that RH27 is a component of the microprocessor complex and is critical for zygote division and stem cell homeostasis.

As a new component of the microprocessor complex in Arabidopsis, DEAD-BOX RNA HELICASE 27 regulates the initiation of zygotic embryogenesis and stem cell homeostasis in the shoot and root meristems.     

Shoot meristem size is dependent on inbred background and presence of the maize homeobox gene, knotted1

The knotted1 (kn1) gene of maize is expressed in meristems and is absent from leaves, including the site of leaf initiation within the meristem. Recessive mutations of kn1 have been described that limit the capacity to make branches and result in extra carpels. Dominant mutations suggest that kn1 function plays a role in maintaining cells in an undifferentiated state. We took advantage of a Ds-induced dominant allele in order to screen for additional recessive alleles resulting from mobilization of the Ds element. Analysis of one such allele revealed a novel embryonic shoot phenotype in which the shoot initiated zero to few organs after the cotyledon was made, resulting in plants that arrested as seedlings. We refer to this phenotype as a limited shoot. The limited shoot phenotype reflected loss of kn1 function, but its penetrance was background dependent. We examined meristem size and found that plants lacking kn1 function had shorter meristems than non-mutant siblings. Furthermore, meristems of restrictive inbreds were significantly shorter than meristems of permissive inbreds, implying a correlation between meristem height and kn1 gene function in the embryo. Analysis of limited shoot plants during embryogenesis indicated a role for kn1 in shoot meristem maintenance. We discuss a model for kn1 in maintenance of the morphogenetic zone of the shoot apical meristem.     

Heterotrimeric G proteins control stem cell proliferation through CLAVATA signaling in Arabidopsis

Cell-to-cell communication is a fundamental mechanism for coordinating developmental and physiological events in multicellular organisms. Heterotrimeric G proteins are key molecules that transmit extracellular signals; similarly, CLAVATA signaling is a crucial regulator in plant development. Here, we show that Arabidopsis thaliana Gβ mutants exhibit an enlarged stem cell region, which is similar to that of clavata mutants. Our genetic and cell biological analyses suggest that the G protein beta-subunit1 AGB1 and RPK2, one of the major CLV3 peptide hormone receptors, work synergistically in stem cell homeostasis through their physical interactions. We propose that AGB1 and RPK2 compose a signaling module to facilitate meristem development.     

POL and related phosphatases are dosage-sensitive regulators of meristem and organ development in Arabidopsis

CLAVATA1 (CLV1) regulates stem cell accumulation at Arabidopsis shoot and flower meristems. CLV1 encodes a receptor-like kinase, but very little is known about downstream signaling components of receptor-kinase signaling in plants. poltergeist (pol) mutants suppress the accumulation of stem cells that occur in clv mutants, and POL has been hypothesized to modulate CLV1 signaling. The POL gene, which encodes a functional protein phosphatase type 2C, is a member of a six-gene family in Arabidopsis. We have isolated loss-of-function alleles for each of the five POL-like genes (PLL1-PLL5). All gene family members, with the exception of PLL3, are expressed broadly within the plant, albeit at differing levels. We show that PLL1 regulates meristem development in parallel with POL. We observe a strong dosage sensitivity at the meristem for POL and PLL1 function in both loss- and gain-of-function analyses, suggesting that these proteins are rate-limiting modulators of stem cell specification. PLL genes also function outside of the meristem: POL and PLL1 regulate pedicel length in interaction with ERECTA, while PLL4 and PLL5 regulate leaf development. We observed no developmental role for either PLL2 or PLL3 based on single and double mutant analysis.     

The indeterminate floral apex1 gene regulates meristem determinacy and identity in the maize inflorescence

Meristems may be determinate or indeterminate. In maize, the indeterminate inflorescence meristem produces three types of determinate meristems: spikelet pair, spikelet and floral meristems. These meristems are defined by their position and their products. We have discovered a gene in maize, indeterminate floral apex1 (ifa1) that regulates meristem determinacy. The defect found in ifa1 mutants is specific to meristems and does not affect lateral organs. In ifa1 mutants, the determinate meristems become less determinate. The spikelet pair meristem initiates more than a pair of spikelets and the spikelet meristem initiates more than the normal two flowers. The floral meristem initiates all organs correctly, but the ovule primordium, the terminal product of the floral meristem, enlarges and proliferates, expressing both meristem and ovule marker genes. A role for ifa1 in meristem identity in addition to meristem determinacy was revealed by double mutant analysis. In zea agamous1 (zag1) ifa1 double mutants, the female floral meristem converts to a branch meristem whereas the male floral meristem converts to a spikelet meristem. In indeterminate spikelet1 (ids1) ifa1 double mutants, female spikelet meristems convert to branch meristems and male spikelet meristems convert to spikelet pair meristems. The double mutant phenotypes suggest that the specification of meristems in the maize inflorescence involves distinct steps in an integrated process.