<Emphasis Type="Italic">OsREL2</Emphasis>, a rice TOPLESS homolog functions in axillary meristem development in rice inflorescence

The morphology of the rice inflorescence, called the panicle, is determined mainly by the activities of axillary meristems including primary, secondary, and spikelet meristems. Recently, in maize, the RAMOSA1 ENHANCER LOCUS2 (REL2) gene, orthologous to the Arabidopsis shoot apical meristem fate-determining TOPLESS, was shown to be involved in the regulation of axillary meristem determinacy. In order to investigate the function of the rice REL2 homolog, we identified and characterized the rice REL2 gene (OsREL2). Compared to other rice TPL homologs, OsREL2 gene expression stayed relatively low throughout panicle development. We characterized a T-DNA insertion osrel2 mutant that showed pleiotropic phenotypic defects, such as defects in panicle heading, sterile lemma elongation, and panicle development, suggesting the OsREL2 functions in multiple developmental processes. In particular, osrel2 developed shorter axillary branches and reduced numbers of lateral organs on axillary branches in comparison to the wild-type, indicating that OsREL2 is important in axillary meristem maintenance. Interestingly, osrel2 produced more primary branches and fewer secondary branches than the wild-type. These results suggest that OsREL2 is involved in branch formation regulation, presumably by suppressing primary branch formation and promoting secondary branch formation.     

barren inflorescence2 regulates axillary meristem development in the maize inflorescence

Organogenesis in plants is controlled by meristems. Shoot apical meristems form at the apex of the plant and produce leaf primordia on their flanks. Axillary meristems, which form in the axils of leaf primordia, give rise to branches and flowers and therefore play a critical role in plant architecture and reproduction. To understand how axillary meristems are initiated and maintained, we characterized the barren inflorescence2 mutant, which affects axillary meristems in the maize inflorescence. Scanning electron microscopy, histology and RNA in situ hybridization using knotted1 as a marker for meristematic tissue show that barren inflorescence2 mutants make fewer branches owing to a defect in branch meristem initiation. The construction of the double mutant between barren inflorescence2 and tasselsheath reveals that the function of barren inflorescence2 is specific to the formation of branch meristems rather than bract leaf primordia. Normal maize inflorescences sequentially produce three types of axillary meristem: branch meristem, spikelet meristem and floral meristem. Introgression of the barren inflorescence2 mutant into genetic backgrounds in which the phenotype was weaker illustrates additional roles of barren inflorescence2 in these axillary meristems. Branch, spikelet and floral meristems that form in these lines are defective, resulting in the production of fewer floral structures. Because the defects involve the number of organs produced at each stage of development, we conclude that barren inflorescence2 is required for maintenance of all types of axillary meristem in the inflorescence. This defect allows us to infer the sequence of events that takes place during maize inflorescence development. Furthermore, the defect in branch meristem formation provides insight into the role of knotted1 and barren inflorescence2 in axillary meristem initiation.     

Development and structure of trichotomous branching in Edgeworthia chrysantha (Thymelaeaceae)

We studied the development and structure of the unusual trichotomous branching of Edgeworthia chrysantha. Three "branch primordia" are formed sequentially on the shoot apex of a main axis and develop into trichotomous branching. The branch primordia are clearly distinguishable from the typical axillary buds of other angiosperms; they develop much more rapidly than axillary buds, and the borders between the branch primordia and shoot apex of the main axis are anatomically unclear. Furthermore, at a later stage, leaves subtending the branch primordia produce typical axillary buds. These results suggest that the trichotomous branching in this species involves the division of the shoot apical meristem. Expression analysis of genes involved in branching or maintenance of the shoot apical meristem in this species should clarify the control mechanism of this novel branching pattern in angiosperms. We also observed the phyllotactic patterns in trichotomous branching and have related these patterns to the shoot system as a whole.     

Genetic control of branching patterns in grass inflorescences

Inflorescence branching in the grasses controls the number of florets and hence the number of seeds. Recent data on the underlying genetics come primarily from rice and maize, although new data are accumulating in other systems as well. This review focuses on a window in developmental time from the production of primary branches by the inflorescence meristem through to the production of glumes, which indicate the transition to producing a spikelet. Several major developmental regulatory modules appear to be conserved among most or all grasses. Placement and development of primary branches are controlled by conserved auxin regulatory genes. Subtending bracts are repressed by a network including TASSELSHEATH4, and axillary branch meristems are regulated largely by signaling centers that are adjacent to but not within the meristems themselves. Gradients of SQUAMOSA-PROMOTER BINDING-like and APETALA2-like proteins and their microRNA regulators extend along the inflorescence axis and the branches, governing the transition from production of branches to production of spikelets. The relative speed of this transition determines the extent of secondary and higher order branching. This inflorescence regulatory network is modified within individual species, particularly as regards formation of secondary branches. Differences between species are caused both by modifications of gene expression and regulators and by presence or absence of critical genes. The unified networks described here may provide tools for investigating orphan crops and grasses other than the well-studied maize and rice.

Recent work on grass inflorescence branching identifies extensive conserved regulation, but also divergence particularly in formation of secondary branches and spikelets.     

孟仁草的花序发育研究

在光学显微镜和扫描电镜下观察了禾本科(Poaceae)虎尾草属(Chloris Sw.)孟仁草(Chloris barbata Sw.)的花序发育过程,以寻找适于虎尾草群(Chloris group)分支分析的发育性状.结果发现了未见于成熟花序的23个发育性状.阐明盂仁草花序的本质是二级长侧枝包围平截的主轴构成指形花序.该类型花序仅见于单子叶植物和少数高度特化的双子叶植物.涉及花序分枝的分子遗传机制研究亟待开展.     

Repression of floral meristem fate is crucial in shaping tomato inflorescence

Tomato is an important crop and hence there is a great interest in understanding the genetic basis of its flowering. Several genes have been identified by mutations and we constructed a set of novel double mutants to understand how these genes interact to shape the inflorescence. It was previously suggested that the branching of the tomato inflorescence depends on the gradual transition from inflorescence meristem (IM) to flower meristem (FM): the extension of this time window allows IM to branch, as seen in the compound inflorescence (s) and falsiflora (fa) mutants that are impaired in FM maturation. We report here that Jointless (J), which encodes a MADS-box protein of the same clade than Short Vegetative Phase (SVP) and Agamous Like 24 (AGL24) in Arabidopsis, interferes with this timing and delays FM maturation, therefore promoting IM fate. This was inferred from the fact that j mutation suppresses the high branching inflorescence phenotype of s and fa mutants and was further supported by the expression pattern of J, which is expressed more strongly in IM than in FM. Most interestingly, FA--the orthologue of the Arabidopsis LEAFY (LFY) gene--shows the complementary expression pattern and is more active in FM than in IM. Loss of J function causes premature termination of flower formation in the inflorescence and its reversion to a vegetative program. This phenotype is enhanced in the absence of systemic florigenic protein, encoded by the Single Flower Truss (SFT) gene, the tomato orthologue of Flowering Locus T (FT). These results suggest that the formation of an inflorescence in tomato requires the interaction of J and a target of SFT in the meristem, for repressing FA activity and FM fate in the IM.     

Suppression of sorghum axillary bud outgrowth by shade, phyB and defoliation signalling pathways

In recent years, several genetic components of vegetative axillary bud development have been defined in both monocots and eudicots, but our understanding of environmental inputs on branching remains limited. Recent work in sorghum ( Sorghum bicolor ) has revealed a role for phytochrome B (phyB) in the control of axillary bud outgrowth through the regulation of Teosinte Branched1 ( TB1 ) gene. In maize ( Zea mays ), TB1 is a dosage-dependent inhibitor of axillary meristem progression, and the expression level of TB1 is a sensitive measure of axillary branch development. To further explore the mechanistic basis of branching, the expression of branching and cell cycle-related genes were examined in phyB-1 and wild-type sorghum axillary buds following treatment with low-red : far-red light and defoliation. Although defoliation inhibited bud outgrowth, it did not influence the expression of sorghum TB1 ( SbTB1 ), whereas changes in SbMAX2 expression, a homolog of the Arabidopsis ( Arabidopsis thaliana ) branching inhibitor MAX2 , were associated with the regulation of bud outgrowth by both light and defoliation. The expression of several cell cycle-related genes was also decreased dramatically in buds repressed by defoliation, but not by phyB deficiency. The data suggest that there are at least two distinct molecular pathways that respond to light and endogenous signals to regulate axillary bud outgrowth.     

The interaction of two homeobox genes,BREVIPEDICELLUS and PENNYWISE,regulates internode patterning in the Arabidopsis inflorescence

Plant architecture results from the activity of the shoot apical meristem, which initiates leaves, internodes, and axillary meristems. KNOTTED1-like homeobox (KNOX) genes are expressed in specific patterns in the shoot apical meristem and play important roles in plant architecture. KNOX proteins interact with BEL1-like (BELL) homeodomain proteins and together bind a target sequence with high affinity. We have obtained a mutation in one of the Arabidopsis BELL genes, PENNYWISE (PNY), that appears phenotypically similar to the KNOX mutant brevipedicellus (bp). Both bp and pny have randomly shorter internodes and display a slight increase in the number of axillary branches. The double mutant shows a synergistic phenotype of extremely short internodes interspersed with long internodes and increased branching. PNY is expressed in inflorescence and floral meristems and overlaps with BP in a discrete domain of the inflorescence meristem where we propose the internode is patterned. The physical association of the PNY and BP proteins suggests that they participate in a complex that regulates early patterning events in the inflorescence meristem.     

Genetic and morphological characterization of the barley <Emphasis Type="Italic">uniculm2</Emphasis> (<Emphasis Type="Italic">cul2</Emphasis>) mutant

Axillary meristem growth and development help define plant architecture in barley (Hordeum vulgare L). Plants carrying the recessive uniculm2 (cul2) mutation initiate vegetative axillary meristem development but fail to develop tillers. In addition, inflorescence axillary meristems develop into spikelets, but the spikelets at the distal end of the inflorescence have an altered phyllotaxy and are sometimes absent. Double mutant combinations of cul2 and nine other recessive mutations that exhibit low to high tiller number phenotypes resulted in a uniculm vegetative phenotype. One exception was the occasional multiple shoots produced in combination with granum-a; a high tillering mutant that occasionally produces two shoot apical meristems. These results show that the CUL2 gene product plays a role in the development of axillary meristems into tillers but does not regulate the development of vegetative apical meristems. Moreover, novel double-mutant inflorescence phenotypes were observed with cul2 in combination with the other mutants. These data show that the wild-type CUL2 gene product is involved in controlling proper inflorescence development and that it functions in combination with some of the other genes that affect branching. Our genetic analysis indicates that there are genetically separate but not distinct regulatory controls on vegetative and inflorescence axillary development. Finally, to facilitate future positionally cloning of cul2, we positioned cul2 on chromosome 6(6H) of the barley RFLP map.     

The Relationship between auxin transport and maize branching

Maize (Zea mays) plants make different types of vegetative or reproductive branches during development. Branches develop from axillary meristems produced on the flanks of the vegetative or inflorescence shoot apical meristem. Among these branches are the spikelets, short grass-specific structures, produced by determinate axillary spikelet-pair and spikelet meristems. We investigated the mechanism of branching in maize by making transgenic plants expressing a native expressed endogenous auxin efflux transporter (ZmPIN1a) fused to yellow fluorescent protein and a synthetic auxin-responsive promoter (DR5rev) driving red fluorescent protein. By imaging these plants, we found that all maize branching events during vegetative and reproductive development appear to be regulated by the creation of auxin response maxima through the activity of polar auxin transporters. We also found that the auxin transporter ZmPIN1a is functional, as it can rescue the polar auxin transport defects of the Arabidopsis (Arabidopsis thaliana) pin1-3 mutant. Based on this and on the groundbreaking analysis in Arabidopsis and other species, we conclude that branching mechanisms are conserved and can, in addition, explain the formation of axillary meristems (spikelet-pair and spikelet meristems) that are unique to grasses. We also found that BARREN STALK1 is required for the creation of auxin response maxima at the flanks of the inflorescence meristem, suggesting a role in the initiation of polar auxin transport for axillary meristem formation. Based on our results, we propose a general model for branching during maize inflorescence development.     

The role of auxin transport during inflorescence development in maize (Zea mays, Poaceae)

Axillary meristems play a fundamental role in inflorescence architecture. Maize (Zea mays) inflorescences are highly branched panicles because of the production of multiple types of axillary meristems. We used auxin transport inhibitors to show that auxin transport is required for axillary meristem initiation in the maize inflorescence. The phenotype of plants treated with auxin transport inhibitors is very similar to that of barren inflorescence2 (bif2) and barren stalk1 (ba1) mutants, suggesting that these genes function in the same auxin transport pathway. To dissect this pathway, we performed RNA in situ hybridization on plants treated with auxin transport inhibitors. We determined that bif2 is expressed upstream and that ba1 is expressed downstream of auxin transport, enabling us to integrate the genetic and hormonal control of axillary meristem initiation. In addition, treatment of maize inflorescences with auxin transport inhibitors later in development results in the production of single instead of paired spikelets. Paired spikelets are a key feature of the Andropogoneae, a group of over 1000 grasses that includes maize, sorghum, and sugarcane. Because all other grasses bear spikelets singly, these results implicate auxin transport in the evolution of inflorescence architecture. Furthermore, our results provide insight into mechanisms of inflorescence branching that are relevant to all plants.     

Class II tassel seed mutations provide evidence for multiple types of inflorescence meristems in maize (Poaceae)

The tassel seed mutations ts4 and Ts6 of maize cause irregular branching in its inflorescences, tassels, and ears, in addition to feminization of the tassel due to the failure to abort pistils. A comparison of the development of mutant and wild-type tassels and ears using scanning electron microscopy reveals that at least four reproductive meristem types can be identified in maize: the inflorescence meristem, the spikelet pair meristem, the spikelet meristem, and the floret meristem. ts4 and Ts6 mutations affect the fate of specific reproductive meristems in both tassels and ears. ts4 mutants fail to form spikelet meristems from spikelet pair meristems. Ts6 mutants are delayed in the conversion of certain spikelet meristems into floret meristems. Once floret meristems are established in both of these mutants, they form florets that appear normal but fail to undergo pistil abortion in the tassel. The abnormal branching associated with each mutant is suppressed at the base of ears, permitting the formation of normal, fertile spikelets. The classification of the different types of reproductive meristems will be useful in interpretation of gene expression patterns in maize. It also provides a framework for understanding meristem functions that can be varied to diversify inflorescence architectures in the Gramineae.     

Floral displays: genetic control of grass inflorescences

Inflorescences in angiosperms are complex structures that have many different types of meristems. Among complex inflorescences, the best studied are in the grass family. Multiple inflorescence genes have been cloned from grasses over the past few years, many of them by positional cloning using the rice genome as a source of positional information. Several genes affect the apical meristem of the inflorescence differently from the lateral branch meristems, allowing morphological differentiation that permits diversification. ramosa1 (ra1), ra2, and ra3 have been cloned from maize and form part of a network of genes that control the production of lateral branching. Curiously, only ra2 is widely conserved; to date, ra1 and ra3 have been found only in Andropogoneae. Additional domestication genes that affect the inflorescence have also been cloned from maize, rice, and wheat.     

barren inflorescence2 Encodes a co-ortholog of the PINOID serine/threonine kinase and is required for organogenesis during inflorescence and vegetative development in maize

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.