Axillary Meristem Development Research Articles

Unraveling the molecular mechanisms governing axillary meristem initiation in plants.

Axillary meristems (AMs) located in the leaf axils determine the number of shoots or tillers eventually formed, thus contributing significantly to the plant architecture and crop yields. The study of AM initiation is unavoidable and beneficial for crop productivity. Shoot branching is an undoubted determinant of plant architecture and thus greatly impacts crop yield due to the panicle-bearing traits of tillers. The emergence of the AM is essential for the incipient bud formation, and then the bud is dormant or outgrowth immediately to form a branch or tiller. While numerous reviews have focused on plant branching and tillering development networks, fewer specifically address AM initiation and its regulatory mechanisms. This review synthesizes the significant advancements in the genetic and hormonal factors governing AM initiation, with a primary focus on studies conducted in Arabidopsis (Arabidopsis thaliana L.) and rice (Oryza sativa L.). In particular, by elaborating on critical genes like LATERAL SUPPRESSOR (LAS), which specifically regulates AM initiation and the networks in which they are involved, we attempt to unify the cascades through which they are positioned. We concentrate on clarifying the precise mutual regulation between shoot apical meristem (SAM) and AM-related factors. Additionally, we examine challenges in elucidating AM formation mechanisms alongside opportunities provided by emerging omics approaches to identify AM-specific genes. By expanding our comprehension of the genetic and hormonal regulation of AM development, we can develop strategies to optimize crop production and address global food challenges effectively.

Detection of Transcription Factors Related to Axillary Bud Development after Exposure to Cold Conditions in Hexaploid Chrysanthemum morifolium Using Arabidopsis Information.

Chrysanthemum is one of the most commercially used ornamental flowering plants in the world. As chrysanthemum is self-incompatible, the propagation of identical varieties is carried out through cuttings rather than through seed. Axillary bud development can be controlled by changing the temperature; for instance, axillary bud development in some varieties is suppressed at high temperatures. In this study, we focused on the simultaneous axillary bud growth from multiple lines of chrysanthemum upon changing conditions from low to normal temperature. Transcriptome analysis was conducted on the Chrysanthemum morifolium cultivar 'Jinba' to identify the important genes for axillary bud development seen when moved from low-temperature treatment to normal cultivation temperature. We performed RNA-Seq analysis on plants after cold conditions in two-day time-course experiments. Under these settings, we constructed a transcriptome of 415,923 C. morifolium and extracted 7357 differentially expressed genes. Our understanding of Arabidopsis axillary meristem development and growth showed that at least 101 genes in our dataset were homologous to transcription factors involved in the biological process. In addition, six genes exhibited statistically significant variations in expression throughout conditions. We hypothesized that these genes were involved in the formation of axillary buds in C. morifolium after cold conditions.

Characterization of the Molecular Events Underlying the Establishment of Axillary Meristem Region in Pepper.

Plant architecture is a major motif of plant diversity, and shoot branching patterns primarily determine the aerial architecture of plants. In this study, we identified an inbred pepper line with fewer lateral branches, 20C1734, which was free of lateral branches at the middle and upper nodes of the main stem with smooth and flat leaf axils. Successive leaf axil sections confirmed that in normal pepper plants, for either node n, Pn (Primordium n) < 1 cm and Pn+1 < 1 cm were the critical periods between the identification of axillary meristems and the establishment of the region, whereas Pn+3 < 1 cm was fully developed and formed a completely new organ. In 20C1734, the normal axillary meristematic tissue region establishment and meristematic cell identity confirmation could not be performed on the axils without axillary buds. Comparative transcriptome analysis revealed that "auxin-activated signaling pathway", "response to auxin", "response to abscisic acid", "auxin biosynthetic process", and the biosynthesis of the terms/pathways, such as "secondary metabolites", were differentially enriched in different types of leaf axils at critical periods of axillary meristem development. The accuracy of RNA-seq was verified using RT-PCR for some genes in the pathway. Several differentially expressed genes (DEGs) related to endogenous phytohormones were targeted, including several genes of the PINs family. The endogenous hormone assay showed extremely high levels of IAA and ABA in leaf axils without axillary buds. ABA content in particular was unusually high. At the same time, there is no regular change in IAA level in this type of leaf axils (normal leaf axils will be accompanied by AM formation and IAA content will be low). Based on this, we speculated that the contents of endogenous hormones IAA and ABA in 20C1734 plant increased sharply, which led to the abnormal expression of genes in related pathways, which affected the formation of Ams in leaf axils in the middle and late vegetative growth period, and finally, nodes without axillary buds and side branches appeared.

OsbHLH067, OsbHLH068, and OsbHLH069 redundantly regulate inflorescence axillary meristem formation in rice.

Rice axillary meristems (AMs) are essential to the formation of tillers and panicle branches in rice, and therefore play a determining role in rice yield. However, the regulation of inflorescence AM development in rice remains elusive. In this study, we identified no spikelet 1-Dominant (nsp1-D), a sparse spikelet mutant, with obvious reduction of panicle branches and spikelets. Inflorescence AM deficiency in nsp1-D could be ascribed to the overexpression of OsbHLH069. OsbHLH069 functions redundantly with OsbHLH067 and OsbHLH068 in panicle AM formation. The Osbhlh067 Osbhlh068 Osbhlh069 triple mutant had smaller panicles and fewer branches and spikelets. OsbHLH067, OsbHLH068, and OsbHLH069 were preferentially expressed in the developing inflorescence AMs and their proteins could physically interact with LAX1. Both nsp1-D and lax1 showed sparse panicles. Transcriptomic data indicated that OsbHLH067/068/069 may be involved in the metabolic pathway during panicle AM formation. Quantitative RT-PCR results demonstrated that the expression of genes involved in meristem development and starch/sucrose metabolism was down-regulated in the triple mutant. Collectively, our study demonstrates that OsbHLH067, OsbHLH068, and OsbHLH069 have redundant functions in regulating the formation of inflorescence AMs during panicle development in rice.

Axillary Meristem Development in Plants

Abstract: The shoot apical meristem of seed plants gives rise to the above-ground parts of the plants during development, including leaves, stems, and lateral meristems. Among them, two types of meristems, axillary meristem and vascular cambium, support the main lateral growth. In this review, we will discuss the regulatory network of lateral growth, focusing on recent progress made mainly in Arabidopsis thaliana, tomato and maize, including the identification of genes and their roles in controlling lateral meristems. In addition, we will summarize the latest evidence about how meristem affects yield-related traits, and discuss the strategies for modulating meristem regulatory genes so as to increase crop yield in agriculture.

MiR156-independent repression of the ageing pathway by longevity-promoting AHL proteins in Arabidopsis.

Summary Plants age by developmental phase changes. In Arabidopsis, the juvenile to adult vegetative phase change (VPC) is marked by clear heteroblastic changes in leaves. VPC and the subsequent vegetative to reproductive phase change are promoted by SQUAMOSA PROMOTOR BINDING PROTEIN‐LIKE (SPL) transcription factors and repressed by miR156/157 targeting SPL transcripts.By genetic, phenotypic, and gene expression analyses, we studied the role of the longevity‐promoting AT‐HOOK MOTIF NUCLEAR LOCALIZED 15 (AHL15) and family members in SPL‐driven plant ageing.Arabidopsis ahl loss‐of‐function mutants showed accelerated VPC and flowering, whereas AHL15 overexpression delayed these phase changes. Expression analysis and tissue‐specific AHL15 overexpression revealed that AHL15 affects VPC and flowering time directly through its expression in the shoot apical meristem and young leaves, and that AHL15 represses SPL2/9/13/15 gene expression in a miR156/157‐independent manner. The juvenile traits of spl loss‐of‐function mutants appeared to depend on enhanced expression of the AHL15 gene, whereas SPL activity prevented vegetative growth from axillary meristem by repressing AHL15 expression.Our results place AHL15 and close family members together with SPLs in a reciprocal regulatory feedback loop that modulates VPC, flowering time, and axillary meristem development in response to both internal and external signals.

Flower meristem maintenance by TILLERS ABSENT 1 is essential for ovule development in rice.

Plant development depends on the activity of pluripotent stem cells in meristems, such as the shoot apical meristem and the flower meristem. In Arabidopsis thaliana, WUSCHEL (WUS) is essential for stem cell homeostasis in meristems and integument differentiation in ovule development. In rice (Oryza sativa), the WUS ortholog TILLERS ABSENT 1 (TAB1) promotes stem cell fate in axillary meristem development, but its function is unrelated to shoot apical meristem maintenance in vegetative development. In this study, we examined the role of TAB1 in flower development. The ovule, which originates directly from the flower meristem, failed to differentiate in tab1 mutants, suggesting that TAB1 is required for ovule formation. Expression of a stem cell marker was completely absent in the flower meristem at the ovule initiation stage, indicating that TAB1 is essential for stem cell maintenance in the 'final' flower meristem. The ovule defect in tab1 was partially rescued by floral organ number 2 mutation, which causes overproliferation of stem cells. Collectively, it is likely that TAB1 promotes ovule formation by maintaining stem cells at a later stage of flower development.

Gymnosperm Resprouting—A Review

Gymnosperms are generally regarded as poor resprouters, especially when compared to angiosperms and particularly following major disturbance. However, is it this clear-cut? This review investigates two main aspects of gymnosperm resprouting: (i) various papers have provided exceptions to the above generalization—how frequent are these exceptions and are there any taxonomic trends?; and (ii) assuming gymnosperms are poor resprouters are there any anatomical or physiological reasons why this is the case? Five of six non-coniferous gymnosperm genera and 24 of 80 conifer genera had at least one species with a well-developed resprouting capability. This was a wider range than would be expected from the usual observation ‘gymnosperms are poor resprouters’. All conifer families had at least three resprouting genera, except the monospecific Sciadopityaceae. Apart from the aboveground stem, buds were also recorded arising from more specialised structures (e.g., lignotubers, tubers, burls and underground stems). In some larger genera it appeared that only a relatively small proportion of species were resprouters and often only when young. The poor resprouting performance of mature plants may stem from a high proportion of apparently ‘blank’ leaf axils. Axillary meristems have been recorded in a wide range of conifer species, but they often did not form an apical dome, leaf primordia or vascular connections. Buds or meristems that did form often abscised at an early stage. While this review has confirmed that conifers do not resprout to the same degree as angiosperms, it was found that a wide diversity of gymnosperm genera can recover vegetatively after substantial disturbance. Further structural studies are needed, especially of: (i) apparently blank leaf axils and the initial development of axillary meristems; (ii) specialised regeneration structures; and (iii) why high variability can occur in the resprouting capacity within species of a single genus and within genera of the same family.

Genome-Wide Identification and Characterization of KNOTTED-Like Homeobox (KNOX) Homologs in Garlic (Allium sativum L.) and Their Expression Profilings Responding to Exogenous Cytokinin and Gibberellin.

Garlic (Allium sativum L.) is an important vegetable and is cultivated and consumed worldwide for its economic and medicinal values. Garlic cloves, the major reproductive and edible organs, are derived from the axillary meristems. KNOTTED-like homeobox (KNOX) proteins, such as SHOOT MERISTEM-LESS (STM), play important roles in axillary meristem formation and development. However, the KNOX proteins in garlic are still poorly known. Here, 10 AsKNOX genes, scattered on 5 of the 8 chromosomes, were genome-wide identified and characterized based on the newly released garlic genome. The typical conserved domains of KNOX proteins were owned by all these 10 AsKNOX homologs, which were divided into two Classes (Class I and Class II) based on the phylogenetic analysis. Prediction and verification of the subcellular localizations revealed the diverse subcellular localization of these 10 AsKNOX proteins. Cis-element prediction, tissue expression analysis, and expression profilings in responding to exogenous GA3 and 6-BA showed the potential involvement of AsKNOX genes in the gibberellin and cytokinin signaling pathways. Overall, the results of this work provided a better understanding of AsKNOX genes in garlic and laid an important foundation for their further functional studies.

Regulation of ARGONAUTE10 Expression Enables Temporal and Spatial Precision in Axillary Meristem Initiation in Arabidopsis.

Axillary meristems (AMs) give rise to lateral shoots and are critical to plant architecture. Understanding howdevelopmental cues and environmental signals impact AM development will enable the improvement of plant architecture in agriculture. Here, we show that ARGONAUTE10 (AGO10), which sequesters miR165/166, promotes AM development through the miR165/166 target gene REVOLUTA. We reveal that AGO10 expression is precisely controlled temporally and spatially by auxin, brassinosteroids, and light to result in AM initiation only in the axils of leaves at a certain age. AUXIN RESPONSE FACTOR 5 (ARF5) activates while BRASSINAZOLE-RESISTANT 1 (BZR1) and PHYTOCHROME-INTERACTING FACTOR 4 (PIF4) repress AGO10 transcription directly. In axils of young leaves, BZR1 and PIF4 repress AGO10 expression to prevent AM initiation. In axils of older leaves, ARF5 upregulates AGO10 expression to promote AM initiation. Our results uncover the spatiotemporal control of AM development through the cooperation of hormones and light converging on a regulator of microRNA.

Prolonged cold exposure to Arabidopsis juvenile seedlings extends vegetative growth and increases the number of shoot branches

ABSTRACT Environmental factors such as photoperiod, temperature, phytohormones, sugars, and soil nutrients can affect the development of axillary meristems and emergence of shoot branches in plants. We investigated how an extended period of cold exposure to Arabidopsis plants before and after inflorescence meristem differentiation would affect plant growth and shoot branching. The number of rosette leaves and shoot branches increased when wild type (WT) juvenile seedlings, but not adult plants, were subjected to a prolonged cold exposure (10/7°C day/night cycle). As the duration of cold exposure to WT juvenile seedlings increased, so too did the rosette area, number of leaves, and rosette branches revealing an extended period of vegetative growth. The prolonged cold treatment also increased the primary inflorescence stem height and number of cauline branches in WT plants revealing a delay in reproductive development that could be altered by early (set domain group 8; sdg8) and late (methyltransferase 1; met1) flowering mutants. The axillary buds/leaf and rosette branches/leaf ratios declined significantly in WT, yet were enhanced in the loss-of-function of carotenoid cleavage dioxygenase 7 (ccd7) and teosinte branched 1 (brc1) hyper-branched mutants. This indicated that axillary meristem differentiation continued during the cold exposure, which did not directly impact axillary bud formation or shoot branching. We conclude that a prolonged cold exposure to juvenile seedlings prior to inflorescence meristem development extended vegetative growth and delayed the reproductive phase to allow additional leaf primordia and axillary meristems to differentiate that enhanced the number of shoot branches in Arabidopsis.

Regulation of plant architecture by a new histone acetyltransferase targeting gene bodies.

Axillary meristem development determines both plant architecture and crop yield; this critical process is regulated by the PROLIFERATING CELL FACTORS (TCP) family of transcription factors. Although TCP proteins bind primarily to promoter regions, some also target gene bodies for expression activation. However, the underlying regulatory mechanism remains unknown. Here we show that TEN, a TCP from cucumber (Cucumis sativus L.), controls the identity and mobility of tendrils. Through its C terminus, TEN binds at intragenic enhancers of target genes; its N-terminal domain functions as a non-canonical histone acetyltransferase (HAT) to preferentially act on lysine 56 and 122 of the histone H3 globular domain. This HAT activity is responsible for chromatin loosening and host-gene activation. The N termini of all tested CYCLOIDEA and TEOSINTE BRANCHED 1-like TCP proteins contain an intrinsically disordered region; despite their sequence divergence, they have conserved HAT activity. This study identifies a non-canonical class of HATs and provides a mechanism by which modification at the H3 globular domain is integrated with the transcription process.

A Novel Variation in the FRIZZLE PANICLE (FZP) Gene Promoter Improves Grain Number and Yield in Rice.

Secondary branch number per panicle plays a crucial role in regulating grain number and yield in rice. Here, we report the positional cloning and functional characterization for SECONDARY BRANCH NUMBER7 (qSBN7), a quantitative trait locus affecting secondary branch per panicle and grain number. Our research revealed that the causative variants of qSBN7 are located in the distal promoter region of FRIZZLE PANICLE (FZP), a gene previously associated with the repression of axillary meristem development in rice spikelets. qSBN7 is a novel allele of FZP that causes an ∼56% decrease in its transcriptional level, leading to increased secondary branch and grain number, and reduced grain length. Field evaluations showed that qSBN7 increased grain yield by 10.9% in a temperate japonica variety, TN13, likely due to its positive effect on sink capacity. Our findings suggest that incorporation of qSBN7 can increase yield potential and improve the breeding of elite rice varieties.

Regulation of Shoot Apical Meristem and Axillary Meristem Development in Plants

Plants retain the ability to produce new organs throughout their life cycles. Continuous aboveground organogenesis is achieved by meristems, which are mainly organized, established, and maintained in the shoot apex and leaf axils. This paper will focus on reviewing the recent progress in understanding the regulation of shoot apical meristem and axillary meristem development. We discuss the genetics of plant meristems, the role of plant hormones and environmental factors in meristem development, and the impact of epigenetic factors on meristem organization and function.

Stem Cell Maintenance in the Shoot Apical Meristems and during Axillary Meristem Development

Stem Cell Maintenance in the Shoot Apical Meristems and during Axillary Meristem Development

Class I KNOX Gene &lt;i&gt;OSH1&lt;/i&gt; is Indispensable for Axillary Meristem Development in Rice

Class I KNOX Gene &lt;i&gt;OSH1&lt;/i&gt; is Indispensable for Axillary Meristem Development in Rice

Antagonistic action of TILLERS ABSENT1 and FLORAL ORGAN NUMBER2 regulates stem cell maintenance during axillary meristem development in rice.

Shoot branches are formed from the axillary meristem and their formation is a key process in plant development. Although our understanding of the mechanisms underlying stem cell maintenance in the shoot apical meristem (SAM) is progressing, our knowledge of these mechanisms during the process of axillary meristem development is insufficient. To elucidate the genetic mechanisms underlying axillary meristem development in rice (Oryza sativa), we undertook a molecular genetic analysis focusing on TILLERS ABSENT1 (TAB1) and FLORAL ORGAN NUMBER2 (FON2), respective orthologs of the WUSCHEL and CLAVATA3 genes involved in SAM maintenance in Arabidopsis (Arabidopsis thaliana). We revealed that stem cells were established at an early stage of axillary meristem development in the wild-type, but were not maintained in tab1. By contrast, the stem cell region and TAB1 expression domain were expanded in fon2, and FON2 overexpression inhibited axillary meristem formation. These results indicate that TAB1 is required to maintain stem cells during axillary meristem development, whereas FON2 negatively regulates stem cell fate by restricting TAB1 expression. Thus, the genetic pathway regulating SAM maintenance in Arabidopsis seems to have been recruited to play a specific role within a narrow developmental window - namely, axillary meristem establishment - in rice.

TILLERS ABSENT1, the WUSCHEL ortholog, is not involved in stem cell maintenance in the shoot apical meristem in rice

ABSTRACTStem cell maintenance in the shoot apical meristem (SAM) is very important for plant development and is regulated by the WUSCHEL–CLAVATA (WUS–CLV) feedback loop in Arabidopsis (Arabidopsis thaliana). WUS promotes stem cell identity, whereas CLV negatively regulates stem cell proliferation by repressing WUS expression. We previously showed that, in rice (Oryza sativa), the WUS ortholog TILLERS ABSENT1 (TAB1, also known as OsWUS) has no function in SAM maintenance, whereas it plays a crucial role in axillary meristem development. Recently, we showed that a double mutant of FLORAL ORGAN NUMBER2 (FON2) and ABERRANT SPIKELET AND PANICLE1 (ASP1) led to a marked enlargement of the inflorescence meristem, and that the TAB1 function is not associated with massive stem cells in this meristem. In this paper, we confirmed that TAB1 is also unrelated to the enlargement of the SAM in the vegetative phase of the fon2 and fon2 asp1 mutants. In addition, misexpression of TAB1 under the promoter of FON1 led to a slight reduction of the SAM size in wild type, suggesting that TAB1 is not a positive regulator of stem cells. Taking together, TAB1 seems not to be involved in meristem maintenance, irrespective of the meristem type.

The Ha‐ROXL gene is required for initiation of axillary and floral meristems in sunflower

Axillary meristems (AMs) contribute to the growth of a plant, determining adult architecture and reproductive success in response to environmental stimuli. The missing flowers (mf) mutant of sunflower (Helianthus annuus) is defective in AM development. mf lacks shoot branching and ray flowers, occasionally producing few disk flowers. Here we demonstrated that a point mutation in the REGULATOR OF AXILLARY MERISTEM FORMATION-LIKE (Ha-ROXL) gene of mf generates a premature stop codon and therefore a nonfunctional bHLH transcription factor, no longer localized in the nucleus, where it should exert its function. Virus-induced gene silencing of Ha-ROXL also causes defects in disk and ray flower development. Ha-ROXL mRNA accumulates at the adaxial boundaries of leaves and AMs. During inflorescence development, Ha-ROXL is expressed in small arcs of cells before a clear separation between abaxial bracts and disk flower primordia. No Ha-ROXL mRNA accumulates in mf inflorescences. Several genes known to play roles in plant architecture, auxin transport, and flower development are differentially expressed in mf and Ha-ROXL-silenced plants. These results highlight the predominant role of Ha-ROXL in regulating AMs in sunflower. In dicot, mf is the first mutant for which the ROXL gene is also required for initiation of flower meristems.

Decreased Spikelets 4 Encoding a Novel Tetratricopeptide Repeat Domain-Containing Protein Is Involved in DNA Repair and Spikelet Number Determination in Rice.

Spikelet number per panicle is a determinative factor of rice yield. DNA repair epigenetically alters the DNA accessibility, which can eventually regulate the transcription of the target genes. However, what and how DNA repair genes are related to rice spikelet development remains unknown. Here, we report the map-based cloning of a novel spikelet number gene DES4 encoding a tetratricopeptide domain-containing protein. DES4 is a close ortholog of Arabidopsis BRU1, which is functionally related to axillary meristem development. A single base pair deletion in the last exon of DES4 caused a premature stop of the resulting protein. The des4 mutant exhibited dwarf, reduced tiller, and spikelet numbers phenotypes, as well as hypersensitivity to genotoxic stresses, suggesting its essential role in DNA repair. DES4 is predominantly expressed in young panicles and axillary meristems, and DES4 protein is localized in nucleus. A set of DNA repair genes such as cyclins, KUs (KD subunits) and recombinases were differentially regulated in des4. Meanwhile, rice spikelet number genes LAX1, LAX2, and MOC1 were significantly down-regulated in des4. In morphology, des4 showed more severe reduction of spikelet numbers than lax1, lax2, and moc1, suggesting that DES4 may work upstream of the three genes.