Meristem Fate Research Articles

A regulatory network controlling developmental boundaries and meristem fates contributed to maize domestication.

During domestication, early farmers selected different vegetative and reproductive traits, but identifying the causative loci has been hampered by their epistasis and functional redundancy. Using chromatin immunoprecipitation sequencing combined with genome-wide association analysis, we uncovered a developmental regulator that controls both types of trait while acting upstream of multiple domestication loci. tasselsheath4 (tsh4) is a new maize domestication gene that establishes developmental boundaries and specifies meristem fates despite not being expressed within them. TSH4 accomplishes this by using a double-negative feedback loop that targets and represses the very same microRNAs that negatively regulate it. TSH4 functions redundantly with a pair of homologs to positively regulate a suite of domestication loci while specifying the meristem that doubled seed yield in modern maize. TSH4 has a critical role in yield gain and helped generate ideal crop plant architecture, thus explaining why it was a major domestication target.

ELONGATED HYPOCOTYL5-mediated light signaling promotes shoot regeneration in Arabidopsis thaliana.

Injured plant somatic tissues regenerate themselves by establishing shoot or root meristems. In Arabidopsis (Arabidopsis thaliana), a two-step culture system ensures regeneration by first promoting the acquisition of pluripotency and subsequently specifying the fate of new meristems. Although previous studies have reported the importance of phytohormones auxin and cytokinin in determining the fate of new meristems, whether and how environmental factors influence this process remains elusive. In this study, we investigated the impact of light signals on shoot regeneration using Arabidopsis hypocotyls as explants. We found that light signals promote shoot regeneration while inhibiting root formation. ELONGATED HYPOCOTYL 5 (HY5), the pivotal transcriptional factor in light signaling, plays a central role in this process by mediating the expression of key genes controlling the fate of new meristems. Specifically, HY5 directly represses root development genes and activates shoot meristem genes, leading to the establishment of shoot progenitor from pluripotent callus. We further demonstrated that the early activation of photosynthesis is critical for shoot initiation, and this is transcriptionally regulated downstream of HY5-dependent pathways. In conclusion, we uncovered the intricate molecular mechanisms by which light signals control the establishment of new meristems through the regulatory network governed by HY5, thus highlighting the influence of light signals on plant developmental plasticity.

BdRCN4, a Brachypodium distachyon TFL1 homologue, is involved in regulation of apical meristem fate.

In higher plants, the shift from vegetative to reproductive development is governed by complex interplay of internal and external signals. TERMINALFLOWER1 (TFL1) plays a crucial role in the regulation of flowering time and inflorescence architecture in Arabidopsis thaliana. This study aimed to explore the function of BdRCN4, a homolog of TFL1 in Brachypodium distachyon, through functional analyses in mutant and transgenic plants. The results revealed that overexpression of BdRCN4 in B. distachyon leads to an extended vegetative phase and reduced production of spikelets. Similar results were found in A. thaliana, where constitutive expression of BdRCN4 promoted a delay in flowering time, followed by the development of hypervegetative shoots, with no flowers or siliques produced. Our results suggest that BdRCN4 acts as a flowering repressor analogous to TFL1, negatively regulating AP1, but no LFY expression. To further validate this hypothesis, a 35S::LFY-GR co-transformation approach on 35::BdRCN4 lines was performed. Remarkably, AP1 expression levels and flower formation were restored to normal in co-transformed plants when treated with dexamethasone. Although further molecular studies will be necessary, the evidence in B. distachyon support the idea that a balance between LFY and BdRCN4/TFL1 seems to be essential for activating AP1 expression and initiating floral organ identity gene expression. This study also demonstrates interesting conservation through the molecular pathways that regulate flowering meristem transition and identity across the evolution of monocot and dicot plants.

Molecular Evolution of RAMOSA1 (RA1) in Land Plants.

RAMOSA1 (RA1) is a Cys2-His2-type (C2H2) zinc finger transcription factor that controls plant meristem fate and identity and has played an important role in maize domestication. Despite its importance, the origin of RA1 is unknown, and the evolution in plants is only partially understood. In this paper, we present a well-resolved phylogeny based on 73 amino acid sequences from 48 embryophyte species. The recovered tree topology indicates that, during grass evolution, RA1 arose from two consecutive SUPERMAN duplications, resulting in three distinct grass sequence lineages: RA1-like A, RA1-like B, and RA1; however, most of these copies have unknown functions. Our findings indicate that RA1 and RA1-like play roles in the nucleus despite lacking a traditional nuclear localization signal. Here, we report that copies diversified their coding region and, with it, their protein structure, suggesting different patterns of DNA binding and protein-protein interaction. In addition, each of the retained copies diversified regulatory elements along their promoter regions, indicating differences in their upstream regulation. Taken together, the evidence indicates that the RA1 and RA1-like gene families in grasses underwent subfunctionalization and neofunctionalization enabled by gene duplication.

STAMENLESS1 activates SUPERWOMAN1 and FLORAL ORGAN NUMBER1 to control floral organ identities and meristem fate in rice.

Floral patterns are unique to rice and contribute significantly to its reproductive success. SL1 encodes a C2H2 transcription factor that plays a critical role in flower development in rice, but the molecular mechanism regulated by it remains poorly understood. Here, we describe interactions of the SL1 with floral homeotic genes, SPW1, and DL in specifying floral organ identities and floral meristem fate. First, the sl1 spw1 double mutant exhibited a stamen-to-pistil transition similar to that of sl1, spw1, suggesting that SL1 and SPW1 may located in the same pathway regulating stamen development. Expression analysis revealed that SL1 is located upstream of SPW1 to maintain its high level of expression and that SPW1, in turn, activates the B-class genes OsMADS2 and OsMADS4 to suppress DL expression indirectly. Secondly, sl1 dl displayed a severe loss of floral meristem determinacy and produced amorphous tissues in the third/fourth whorl. Expression analysis revealed that the meristem identity gene OSH1 was ectopically expressed in sl1 dl in the fourth whorl, suggesting that SL1 and DL synergistically terminate the floral meristem fate. Another meristem identity gene, FON1, was significantly decreased in expression in sl1 background mutants, suggesting that SL1 may directly activate its expression to regulate floral meristem fate. Finally, molecular evidence supported the direct genomic binding of SL1 to SPW1 and FON1 and the subsequent activation of their expression. In conclusion, we present a model to illustrate the roles of SL1, SPW1, and DL in floral organ specification and regulation of floral meristem fate in rice.

Molecular Insights into the Accelerated Sprouting of and Apical Dominance Release in Potato Tubers Subjected to Post-Harvest Heat Stress.

Climate change-induced heat stress (HS) increasingly threatens potato (Solanum tuberosum L.) production by impacting tuberization and causing the premature sprouting of tubers grown during the hot season. However, the effects of post-harvest HS on tuber sprouting have yet to be explored. This study aims to investigate the effects of post-harvest HS on tuber sprouting and to explore the underlying transcriptomic changes in apical bud meristems. The results show that post-harvest HS facilitates potato tuber sprouting and negates apical dominance. A meticulous transcriptomic profiling of apical bud meristems unearthed a spectrum of differentially expressed genes (DEGs) activated in response to HS. During the heightened sprouting activity that occurred at 15-18 days of HS, the pathways associated with starch metabolism, photomorphogenesis, and circadian rhythm were predominantly suppressed, while those governing chromosome organization, steroid biosynthesis, and transcription factors were markedly enhanced. The critical DEGs encompassed the enzymes pivotal for starch metabolism, the genes central to gibberellin and brassinosteroid biosynthesis, and influential developmental transcription factors, such as SHORT VEGETATIVE PHASE, ASYMMETRIC LEAVES 1, SHOOT MERISTEMLESS, and MONOPTEROS. These findings suggest that HS orchestrates tuber sprouting through nuanced alterations in gene expression within the meristematic tissues, specifically influencing chromatin organization, hormonal biosynthesis pathways, and the transcription factors presiding over meristem fate determination. The present study provides novel insights into the intricate molecular mechanisms whereby post-harvest HS influences tuber sprouting. The findings have important implications for developing strategies to mitigate HS-induced tuber sprouting in the context of climate change.

Cotton Meristem Transcriptomes: Constructing an RNA-Seq Pipeline to Explore Crop Architecture Regulation.

Plants stem cells, known as meristems, specify all patterns of growth and organ size. Differences in meristem activities contribute to diverse shoot architectures. As many architectural traits, such as branching patterns, flowering time, and fruit size, are yield determinants, meristem regulation is of fundamental importance to crop productivity. Cotton (Gossypium spp.) produces our most prevalent natural fiber that finds its way into products ranging from industrial cellulose, medical supplies, and paper currency, to a broad diversity of textiles, not least of which is our clothing. However, the cotton plant has growth habits that challenge management practices and limit harvest yield and quality. Unraveling and leveraging the genetic networks regulating meristem activities offers the potential to overcome these limitations. We use virus-based technologies in cotton to perturb signals regulating meristem fate and size. In this chapter, we describe our pipeline for altering cotton meristem dynamics and preparing, analyzing, and exploring the transcriptomes from isolated meristems.

Genome-wide association study and transcriptome analysis reveal candidate genes for off-season flowering in blueberry

Off-season flowering in daylength-sensitive plants is an intriguing characteristic that represents an opportunity to expand crop's production timing and regions, and potentially speed up breeding. Southern Highbush Blueberry (SHB) is classified as a short-day plant, with a blooming period in the northern hemisphere ranging from late winter through spring. In Florida, some blueberry genotypes have consistently bloomed during the fall season, suggesting that flower bud initiation occurred during the summer. Such a characteristic indicates a facultative response to daylength or day-neutrality capacity, leading to the off-season flowering observed. To understand the genetic basis of off-season flowering in SHB, we performed a genome-wide association study (GWAS), followed by transcriptomic analysis of contrasting genotypes. Among the 536 genotypes evaluated, 14 % bloomed during the fall, of which seven presented consistently high scores for off-season flowering capacity. The GWAS revealed 12 single nucleotide polymorphisms (SNPs) significantly associated with the off-season flowering trait, which together accounted for 17 % of the phenotypic variance. A gene homologous to an RNA helicase and reported to modulate florescence formation and flowering time in other plant species, was identified within a genomic region associated with the off-season flowering. This gene was up-regulated in a fall-flowering blueberry genotype. Additionally, we detected down-regulation of flowering repressors and up-regulation of MADS-box transcription factors known to be involved in the fate of floral meristems. Our findings provide insights into the genetic and molecular basis of this complex trait in blueberry. These results can be useful for marker-assisted selection and further functional gene validation to accelerate the development of blueberry varieties suitable for off-season production.

Architectural traits underlie growth form diversity and polycarpic versus monocarpic life histories in Cerberiopsis (Apocynaceae)

Abstract Plant architecture strongly influences plant growth habits, as it determines the arrangement, function and fate of meristems. How architecture could be involved in the monocarpic life history, i.e. dying after flowering, remains poorly investigated. Monocarpy is evident in some species since they are annual or because their single stem flowers apically. However, monocarpy in long-lived branched trees is rare and remains poorly understood. We aim to highlight the architectural features involved in the monocarpic strategy of Cerberiopsis candelabra, a rainforest tree endemic to New Caledonia. We conducted a comparative analysis of the genus, which comprises three species with different growth habits. Twenty plants of each species were studied at different ontogenic stages. We compared their developmental sequence and analysed their processes of growth, branching, flowering and reiteration. We identified a combination of traits that distinguish the species, and we found a syndrome of two architectural features that support the monocarpic strategy in C. candelabra: the synchronous flowering of all terminal meristems and the absence of delayed branching. Flowering in C. candelabra preferentially occurs when the complete architectural sequence is developed, but the plant never shows signs of senescence, suggesting that environmental stresses, such as wind disturbance, could be the main trigger for flowering. The architecture of C. candelabra is suggested to be the most derived in the genus.

Spatio-temporal analysis of strawberry architecture: insights into the control of branching and inflorescence complexity.

Plant architecture plays a major role in flowering and therefore in crop yield. Attempts to visualize and analyse strawberry plant architecture have been few to date. Here, we developed open-source software combining two- and three-dimensional representations of plant development over time along with statistical methods to explore the variability in spatio-temporal development of plant architecture in cultivated strawberry. We applied this software to six seasonal strawberry varieties whose plants were exhaustively described monthly at the node scale. Results showed that the architectural pattern of the strawberry plant is characterized by a decrease of the module complexity between the zeroth-order module (primary crown) and higher-order modules (lateral branch crowns and extension crowns). Furthermore, for each variety, we could identify traits with a central role in determining yield, such as date of appearance and number of branches. By modeling the spatial organization of axillary meristem fate on the zeroth-order module using a hidden hybrid Markov/semi-Markov mathematical model, we further identified three zones with different probabilities of production of branch crowns, dormant buds, or stolons. This open-source software will be of value to the scientific community and breeders in studying the influence of environmental and genetic cues on strawberry architecture and yield.

Restructuring plant types for developing tailor-made crops.

Plants have adapted to different environmental niches by fine-tuning the developmental factors working together to regulate traits. Variations in the developmental factors result in a wide range of quantitative variations in these traits that helped plants survive better. The major developmental pathways affecting plant architecture are also under the control of such pathways. Most notable are the CLAVATA-WUSCHEL pathway regulating shoot apical meristem fate, GID1-DELLA module influencing plant height and tillering, LAZY1-TAC1 module controlling branch/tiller angle and the TFL1-FT determining the floral fate in plants. Allelic variants of these key regulators selected during domestication shaped the crops the way we know them today. There is immense yield potential in the 'ideal plant architecture' of a crop. With the available genome-editing techniques, possibilities are not restricted to naturally occurring variations. Using a transient reprogramming system, one can screen the effect of several developmental gene expressions in novel ecosystems to identify the best targets. We can use the plant's fine-tuning mechanism for customizing crops to specific environments. The process of crop domestication can be accelerated with a proper understanding of these developmental pathways. It is time to step forward towards the next-generation molecular breeding for restructuring plant types in crops ensuring yield stability.

A genotype-specific architectural and physiological profile is involved in the flowering regularity of apple trees.

In polycarpic plants, meristem fate varies within individuals in a given year. In perennials, the proportion of floral induction (FI) in meristems also varies between consecutive years and among genotypes of a given species. Previous studies have suggested that FI of meristems could be determined by the within-plant competition for carbohydrates and by hormone signaling as key components of the flowering pathway. At the genotypic level, variability in FI was also associated with variability in architectural traits. However, the part of genotype-dependent variability in FI that can be explained by either tree architecture or tree physiology is still not fully understood. This study aimed at deciphering the respective effect of architectural and physiological traits on FI variability within apple trees by comparing six genotypes with contrasted architectures. Shoot type demography as well as the flowering and fruit production patterns were followed over 6 years and characterized by different indexes. Architectural morphotypes were then defined based on architectural traits using a clustering approach. For two successive years, non-structural starch content in leaf, stem and meristems, and hormonal contents (gibberellins, cytokinins, auxin and abscisic acid) in meristems were quantified and correlated to FI within-tree proportions. Based on a multi-step regression analysis, cytokinins and gibberellins content in meristem, starch content in leaves and the proportion of long shoots in tree annual growth were shown to contribute to FI. Although the predictive linear model of FI was common to all genotypes, each of the explicative variables had a different weight in FI determination, depending on the genotype. Our results therefore suggest both a common determination model and a genotype-specific architectural and physiological profile linked to its flowering behavior.

Over-Expression of Larch DAL1 Accelerates Life-Cycle Progression in Arabidopsis

Homologs of Larix kaempferiDEFICIENS-AGAMOUS-LIKE 1 (LaDAL1) promote flowering in Arabidopsis. However, their functional role in the whole life-cycle is limited. Here, we analyzed the phenotypes and transcriptomes of Arabidopsis plants over-expressing LaDAL1. With respect to the defined life-cycle stage of Arabidopsis based on the meristem state, the results showed that LaDAL1 promoted seed germination, bolting, flower initiation, and global proliferative arrest, indicating that LaDAL1 accelerates the meristem reactivation, the transitions of vegetative meristem to inflorescence and flower meristem, and meristem arrest. As a marker gene of meristem, TERMINAL FLOWER 1 was down-regulated after LaDAL1 over-expression. These results reveal that LaDAL1 accelerates the life-cycle progression in Arabidopsis by promoting the transition of meristem fate, providing more and novel functional information about the conifer age-related gene DAL1.

GIF1 controls ear inflorescence architecture and floral development by regulating key genes in hormone biosynthesis and meristem determinacy in maize

BackgroundInflorescence architecture and floral development in flowering plants are determined by genetic control of meristem identity, determinacy, and maintenance. The ear inflorescence meristem in maize (Zea mays) initiates short branch meristems called spikelet pair meristems, thus unlike the tassel inflorescence, the ears lack long branches. Maize growth-regulating factor (GRF)-interacting factor1 (GIF1) regulates branching and size of meristems in the tassel inflorescence by binding to Unbranched3. However, the regulatory pathway of gif1 in ear meristems is relatively unknown.ResultIn this study, we found that loss-of-function gif1 mutants had highly branched ears, and these extra branches repeatedly produce more branches and florets with unfused carpels and an indeterminate floral apex. In addition, GIF1 interacted in vivo with nine GRFs, subunits of the SWI/SNF chromatin-remodeling complex, and hormone biosynthesis-related proteins. Furthermore, key meristem-determinacy gene RAMOSA2 (RA2) and CLAVATA signaling-related gene CLV3/ENDOSPERM SURROUNDING REGION (ESR) 4a (CLE4a) were directly bound and regulated by GIF1 in the ear inflorescence.ConclusionsOur findings suggest that GIF1 working together with GRFs recruits SWI/SNF chromatin-remodeling ATPases to influence DNA accessibility in the regions that contain genes involved in hormone biosynthesis, meristem identity and determinacy, thus driving the fate of axillary meristems and floral organ primordia in the ear-inflorescence of maize.

Reflections on the Triptych of Meristems That Build Flowering Branches in Tomato.

Branching is an important component determining crop yield. In tomato, the sympodial pattern of shoot and inflorescence branching is initiated at floral transition and involves the precise regulation of three very close meristems: (i) the shoot apical meristem (SAM) that undergoes the first transition to flower meristem (FM) fate, (ii) the inflorescence sympodial meristem (SIM) that emerges on its flank and remains transiently indeterminate to continue flower initiation, and (iii) the shoot sympodial meristem (SYM), which is initiated at the axil of the youngest leaf primordium and takes over shoot growth before forming itself the next inflorescence. The proper fate of each type of meristems involves the spatiotemporal regulation of FM genes, since they all eventually terminate in a flower, but also the transient repression of other fates since conversions are observed in different mutants. In this paper, we summarize the current knowledge about the genetic determinants of meristem fate in tomato and share the reflections that led us to identify sepal and flower abscission zone initiation as a critical stage of FM development that affects the branching of the inflorescence.

Axillary Bud Fate Shapes Plant Architecture in Horticultural Crops

Above-ground plant architecture is dictated to a large extent by the fates and growth rates of aerial plant meristems. Shoot apical meristem gives rise to the fundamental plant form by generating new leaves. However, the fates of axillary meristems located in leaf axils have a great influence on plant architecture and affect the harvest index, yield potential and cultural practices. Improving plant architecture by breeding facilitates denser plantations, better resource use efficiency and even mechanical harvesting. Knowledge of the genetic mechanisms regulating plant architecture is needed for precision breeding, especially for determining feasible breeding targets. Fortunately, research in many crop species has demonstrated that a relatively small number of genes has a large effect on axillary meristem fates. In this review, we select a number of important horticultural and agricultural plant species as examples of how changes in plant architecture affect the cultivation practices of the species. We focus specifically on the determination of the axillary meristem fate and review how plant architecture may change even drastically because of altered axillary meristem fate. We also explain what is known about the genetic and environmental control of plant architecture in these species, and how further changes in plant architectural traits could benefit the horticultural sector.

The FveFT2 florigen/FveTFL1 antiflorigen balance is critical for the control of seasonal flowering in strawberry while FveFT3 modulates axillary meristem fate and yield.

Summary Plant architecture is central in determining crop yield. In the short‐day species strawberry, a crop vegetatively propagated by daughter‐plants produced by stolons, fruit yield is further dependent on the trade‐off between sexual reproduction (fruits) and asexual reproduction (daughter‐plants). Both are largely dependent on meristem identity, which establishes the development of branches, stolons and inflorescences.Floral initiation and plant architecture are modulated by the balance between two related proteins, FLOWERING LOCUS T (FT) and TERMINAL FLOWER 1 (TFL1). We explored in woodland strawberry the role of the uncharacterised FveFT2 and FveFT3 genes and of the floral repressor FveTFL1 through gene expression analyses, grafting and genetic transformation (overexpression and gene editing).We demonstrate the unusual properties of these genes. FveFT2 is a nonphotoperiodic florigen permitting short‐day (SD) flowering and FveTFL1 is the long‐hypothesised long‐day systemic antiflorigen that contributes, together with FveFT2, to the photoperiodic regulation of flowering. We additionally show that FveFT3 is not a florigen but promotes plant branching when overexpressed, that is likely to be through changing axillary meristem fate, therefore resulting in a 3.5‐fold increase in fruit yield at the expense of stolons.We show that our findings can be translated into improvement of cultivated strawberry in which FveFT2 overexpression significantly accelerates flowering.

Functional Diversification of euANT/PLT Genes in Oryza sativa Panicle Architecture Determination.

Grain yield, which is one of the most important traits in rice breeding, is controlled in part by panicle branching patterns. Numerous genes involved in the control of panicle architecture have been identified through mutant and QTL characterization. Previous studies suggested the importance of several AP2/ERF transcription factor-encoding genes in the control of panicle development, including the AINTEGUMENTA/PLETHORA-like (euANT/PLT) genes. The ANT gene was specifically considered to be a key regulator of shoot and floral development in Arabidopsis thaliana. However, the likely importance of paralogous euANT/PLT genes in the regulation of meristem identities and activities during panicle architecture development has not to date been fully addressed in rice. In this study, we observed that the rice euANT/PLT genes displayed divergent temporal expression patterns during the branching stages of early panicle development, with spatial localization of expression in meristems for two of these genes. Moreover, a functional analysis of rice ANT-related genes using genome editing revealed their importance in the control of panicle architecture, through the regulation of axillary meristem (AM) establishment and meristem fate transition. Our study suggests that the paralogous euANT/PLT genes have become partially diversified in their functions, with certain opposing effects, since they arose from ancestral gene duplication events, and that they act in regulating the branching of the rice panicle.

SB1 Encoding RING-Like Zinc-Finger Protein Regulates Branch Development as a Transcription Repressor

Inflorescence structure of rice, including the number and length of branches, and the density of the spikelet, can greatly affect the number of grains per panicle, which is one of the key factors in yield compositions. Here we identified five allelic mutants sb1-1/2/3/4/5 that related to branch development of rice. In these mutants, the branch meristem fate was prolonged sharply, resulting in delay of transition from branches to spikelets, and then increased the numbers of branches and spikelets per panicle. SB1 encodes a nuclear RING-like domain protein of SHI/LRP/SRS family and strongly expressed in branch meristems. The results of protein interaction and chromatin immunoprecipitation further suggested that SB1 directly repressed the expression of DEP1, TAW1, MOC1 and IPA1 by interacting with a co-repressor complex to affect acetylation level of histone H3 on target regions. Thus, we proposed that SB1 is a transcription repressor of branch meristem activity by widely and negatively regulating a series of genes that maintain branch meristem fate.

A Comparative Study on the Branching Pattern of Monocyclic and Bicyclic Shoots of Apple cv. "Fuji".

The development of tree architecture results from shoot growth and branching, but their relationship is still not fully understood. The goal of this study was to determine the effect of parent shoot growth characteristics on branching patterns in terms of polycyclism, growth duration (GD), and growth period (GP), considering apple tree as a case study. Weekly shoot growth records were collected from 227 shoots during their second year of growth and the resulting branching patterns from the following year. The branching patterns were compared between the different shoot categories, using hidden semi-Markov models. Our results showed that the branching pattern was similar in bicyclic and monocyclic shoots with a long GD. The number of floral laterals, and the frequency and length of the floral zones, increased with GD. Moreover, a long GD led to strong acrotony, due to the high occurrence of a vegetative zone with long laterals in the distal position of the shoot. In bicyclic shoots, an early GP of the second GU led to more frequent and longer floral zones than a late GP. Therefore, the GD was the strongest driver of the branching pattern, and GP modulated the flowering capacity. The main similarities among shoot categories resulted from the existence of latent buds and floral zones associated with growth cessation periods. Even though flowering was more abundant during the early GP, the positions of floral zones indicated that induction in axillary meristems can also occur late in the season. This study provides new knowledge regarding the relationships between the dynamics of parent shoot growth and axillary meristem fates, with key consequences on flowering abundance and positions.