Strategy for shoot meristem proliferation in plants

Shoot apical meristem (SAM) of plants harbors stem cells capable of generating the aerial tissues including reproductive organs. Therefore, it is very important for plants to control SAM proliferation and its density as a survival strategy. The SAM is regulated by the dynamics of a specific gene network, such as the WUS-CLV interaction of A. thaliana. By using a mathematical model, we previously proposed six possible SAM patterns in terms of the manner and frequency of stem cell proliferation. Two of these SAM patterns are predicted to generate either dichotomous or axillary shoot branch. Dichotomous shoot branches caused by this mechanism are characteristic of the earliest vascular plants, such as Cooksonia and Rhynia, but are observed in only a small minority of plant species of the present day. On the other hand, axillary branches are observed in the majority of plant species and are induced by a different dynamics of the feedback regulation between auxin and the asymmetric distribution of PIN auxin efflux carriers. During evolution, some plants may have adopted this auxin-PIN system to more strictly control SAM proliferation.     

Embryonic shoot apical meristem formation in higher plants

The shoot apical meristem (SAM) is essential for organ formation in higher plants. How the SAM is formed during plant development is poorly understood, however. In this review, we focus on several recent studies that provide new insights into the mechanism of SAM formation during embryogenesis. Recently, positive and negative regulators of the class I KNOX genes, which are thought to be necessary for SAM formation, have been identified; the Arabidopsis CUP-SHAPED COTYLEDON (CUC) genes are required for the expression of a class I KNOX gene, SHOOT MERISSTEMLES (STM) during embryogenesis, and the Arabidopsis ASYMMETRIC LEAVES1 (AS1), AS2, and several other genes negatively regulate KNOX gene expression in cotyledon primordia. Also, several genes that are involved in the formation of the adaxial–abaxial axis of cotyledons seem to regulate embryonic SAM formation. Electronic Publication     

Reaction-diffusion pattern in shoot apical meristem of plants

A fundamental question in developmental biology is how spatial patterns are self-organized from homogeneous structures. In 1952, Turing proposed the reaction-diffusion model in order to explain this issue. Experimental evidence of reaction-diffusion patterns in living organisms was first provided by the pigmentation pattern on the skin of fishes in 1995. However, whether or not this mechanism plays an essential role in developmental events of living organisms remains elusive. Here we show that a reaction-diffusion model can successfully explain the shoot apical meristem (SAM) development of plants. SAM of plants resides in the top of each shoot and consists of a central zone (CZ) and a surrounding peripheral zone (PZ). SAM contains stem cells and continuously produces new organs throughout the lifespan. Molecular genetic studies using Arabidopsis thaliana revealed that the formation and maintenance of the SAM are essentially regulated by the feedback interaction between WUSHCEL (WUS) and CLAVATA (CLV). We developed a mathematical model of the SAM based on a reaction-diffusion dynamics of the WUS-CLV interaction, incorporating cell division and the spatial restriction of the dynamics. Our model explains the various SAM patterns observed in plants, for example, homeostatic control of SAM size in the wild type, enlarged or fasciated SAM in clv mutants, and initiation of ectopic secondary meristems from an initial flattened SAM in wus mutant. In addition, the model is supported by comparing its prediction with the expression pattern of WUS in the wus mutant. Furthermore, the model can account for many experimental results including reorganization processes caused by the CZ ablation and by incision through the meristem center. We thus conclude that the reaction-diffusion dynamics is probably indispensable for the SAM development of plants.     

Axillary meristem development in Arabidopsis thaliana

Axillary shoot apical meristems initiate post-embryonically in the axils of leaves. Their developmental fate is a main determinant of the final plant body plan. In Arabidopsis, usually a single axillary meristem initiates in the leaf axil even though there is developmental potential for formation of multiple branches. While the wild-type plants rarely form multiple branches in the leaf axil, tfl1-2 plants regularly develop two or more branches in the axils of the rosette leaves. Axillary meristem formation in Arabidopsis occurs in two waves: an acropetal wave forms during plant vegetative development, and a basipetal wave forms during plant reproductive development. We report here the morphological and anatomical changes, and the STM expression pattern associated with the formation of axillary and accessory meristems during Arabidopsis vegetative development.     

Modelling the development and arrangement of the primary vascular structure in plants

Background and Aims

The process of vascular development in plants results in the formation of a specific array of bundles that run throughout the plant in a characteristic spatial arrangement. Although much is known about the genes involved in the specification of procambium, phloem and xylem, the dynamic processes and interactions that define the development of the radial arrangement of such tissues remain elusive.

Methods

This study presents a spatially explicit reaction–diffusion model defining a set of logical and functional rules to simulate the differentiation of procambium, phloem and xylem and their spatial patterns, starting from a homogeneous group of undifferentiated cells.

Key Results

Simulation results showed that the model is capable of reproducing most vascular patterns observed in plants, from primitive and simple structures made up of a single strand of vascular bundles (protostele), to more complex and evolved structures, with separated vascular bundles arranged in an ordered pattern within the plant section (e.g. eustele).

Conclusions

The results presented demonstrate, as a proof of concept, that a common genetic–molecular machinery can be the basis of different spatial patterns of plant vascular development. Moreover, the model has the potential to become a useful tool to test different hypotheses of genetic and molecular interactions involved in the specification of vascular tissues.     

Allometry and development in herbaceous plants: functional responses of meristem allocation to light and nutrient availability

We examined the relationship between meristem allocation and plant size for four annual plant species: Arabidopsis thaliana, Arenaria serphyllifolia, Brassica rapa, and Chaenorrhinum minus. Gradients of light and nutrient availability were used to obtain a range of plant sizes for each of these species. Relative allocation to reproductive, inactive, and growth meristems were used to measure reproductive effort, apical dominance, and branching intensity, respectively. We measured allocation to each of these three meristem fates at weekly intervals throughout development and at final developmental stage. At all developmental stages reproductive effort and branching intensity tended to increase with increasing plant size (i.e., due to increasing resource availability) and apical dominance tended to decrease with increasing plant size. We interpret these responses as a strategy for plants to maximize fitness across a range of environments. In addition, significant differences in meristem response among species may be important in defining the range of habitats in which a species can exist and may help explain patterns of species competition and coexistence in habitats with variable resource availability.     

Lilium candidum bulblet and meristem development

Lilium candidum L., commonly known as the Madonna lily, is a wild Lilium species with medicinal properties and excellent potential as an ornamental crop, but one that has been scarcely investigated. The aim of this research was to study (1) tissue culture propagation of L. candidum bulblets, (2) early bulblet development, and (3) the effect of temperature and bulblet weight on bulblet and plant growth and meristem development. An investigation of the effect of explant type and temperature on in vitro bulblet propagation showed that scales were the most efficient explants for in vitro propagation and that exposing the regenerating bulblets to 15°C for 4 wk increased bulblet weight but reduced the number of bulblets produced. For bulblets planted in soil after 12 wk of exposure to 15°C or 25°C, the fastest growth was observed in the bulblets that had been exposed to 15°C and that had a larger initial size. Histological examination showed that young in vitro-grown bulblets had a rudimentary meristem comprising few cells with no layer organization. After 12 wk of growth, all bulblets showed a layered meristem, regardless of bulblet size or exposure to 15°C. However, an increased amount of leaf primordia was detected in larger bulblets. Furthermore, the histological examination revealed that in L. candidum, as opposed to other lily species, there had been no real "phase change" in the meristem and that the phase change from juvenile to vegetative adult occurred at a much later stage in L. candidum than in other species.     

Abnormal development and altered hormone profile and sensitivity in Arabidopsis plants ectopically expressing Brassica shoot apical meristem genes

The previously isolated Brassica genes homologous to the Arabidopsis SHOOT MERISTEMLESS (STM), CLAVATA 1 (CLV1), and ZWILLE (ZLL) were characterized during embryonic and postembryonic development in vivo. Ectopic expression of the Brassica genes in Arabidopsis caused profound phenotypic deviations from the WT. While the over-expression of BnCLV1 produced smaller embryonic shoot apical meristems (SAMs) with delayed activation at germination, the introduction of Brassica STM enhanced the structure of the SAM and accelerated meristem reactivation. These opposite behaviors were related to differential levels of endogenous cytokinins and abscisic acid (ABA), as well as the expression of genes regulating meristem activity. Low levels of ABA and increased accumulation of the cytokinins trans-zeatin-O-glucoside (t-ZOG), cis-zeatin-O-glucoside (c-ZOG), trans-zeatin riboside (t-ZR), and isopentenyladenosine (iPA) were measured in seedlings of Arabidopsis plants over-expressing the Brassica STM. This was in contrast to BnCLV1 over-expressors which had very low levels of cytokinins. During the early phases of meristem reactivation the expression of the Arabidopsis AtKNAT6, AtWUSCHEL, and AtCUPSHAPED COTYLEDON-1 was induced by the introduction of the Brassica STM whereas that of AtCLAVATA 3 was inhibited. An opposite expression profile was measured in lines ectopically expressing BnCLV1. Other phenotypic abnormalities observed in Arabidopsis plants over-expressing the Brassica STM included lobed leaves, ectopic meristems, and increased number of reproductive organs, i.e. flowers and siliques. The introduction of BnZLL-1 and -2 did not cause major developmental abnormalities.     

Photoperiod regulates flower meristem development in Arabidopsis thaliana

Photoperiod has been known to regulate flowering time in many plant species. In Arabidopsis, genes in the long day (LD) pathway detect photoperiod and promote flowering under LD. It was previously reported that clavata2 (clv2) mutants grown under short day (SD) conditions showed suppression of the flower meristem defects, namely the accumulation of stem cells and the resulting production of extra floral organs. Detailed analysis of this phenomenon presented here demonstrates that the suppression is a true photoperiodic response mediated by the inactivation of the LD pathway under SD. Inactivation of the LD pathway was sufficient to suppress the clv2 defects under LD, and activation of the LD pathway under SD conditions restored clv2 phenotypes. These results reveal a novel role of photoperiod in flower meristem development in Arabidopsis. Flower meristem defects of clv1 and clv3 mutants are also suppressed under SD, and 35S:CO enhanced the defects of clv3, indicating that the LD pathway works independently from the CLV genes. A model is proposed to explain the interactions between photoperiod and the CLV genes.     

Identifying novel regulators of shoot meristem development

New organs are initiated throughout the life span of higher plants. This process occurs at the shoot meristem, which is initiated during embryogenesis and is later responsible for generating the above-ground portion of the plant. The shoot meristem can be thought of as having two zones, a central zone containing meristematic cells in an undifferentiated state, and a surrounding peripheral zone where cells enter a specific developmental pathway toward a differentiated state. Recent advances have revealed several genes that specifically regulate meristem development inArabidopsis. However, extensive mutagenesis by several labs have identified only a handful, of loci that appear to specifically regulate shoot meristem development. We have undertaken an enhancer/suppressor mutagenesis of an existing meristem mutant (clv1) and have identified novel regulators of meristem development. The extended abstract of a paper presented at the 13th International Symposium in Conjugation with Award of the International Prize for Biology “Frontier of Plant Biology”     

Common regulatory themes in meristem development and whole-plant homeostasis

The maintenance of meristems throughout plant ontogeny allows the development of a diversity of structural forms from the same genetic base. Examination of the common and contrasting features of these meristems leads to the outline of common regulatory themes in meristem development. In particular, by including comparisons with embryogenesis research, we see that hormones and factors that are generally attributed roles in stress response, such as redox potential, carotenoids, flavonoids, brassinosteroids, jasmonic acid and ethylene, are emerging as major candidates for long-distance or short-distance signalling molecules in meristem development. In each case, hormone response appears to be influenced greatly by the developmental window or transition stage at which the meristem resides.     

Plant development: light exposure directs meristem fate

Leaf initiation was previously thought to be self-regulated and not reliant on environmental cues. However, a recent study has revealed that light redirects meristem fate from maintenance to lateral organ initiation, through the regulation of the plant hormones auxin and cytokinin.     

Regulation of potato meristem development by jasmonic acid in vitro

The influence of jasmonic acid (JA) on differentiation of meristems of the potato,Solanum tuberosum cv. Vesna, was investigated in vitro. Meristems were grown on Murashige and Skoog (MS) medium supplemented with indole-3-acetic acid (IAA) (10 μM), kinetin (10 μM), gibberellic acid (3 μM), as modified by Bang. Addition of JA in concentrations of 0.5–10 μM increased the number of meristems that developed into buds, particularly in meristems isolated from shoots grown from tubers in the dark. JA had no noticeable effect on meristems from germs grown in light. All added concentrations of JA retarded callus and root formation. The inhibitory effect on rhizogenesis disappeared immediately after transfer of the developed buds to medium without JA.     

Benzylaminopurine induces phenocopies of floral meristem and organ identity mutants in wild-typeArabidopsis plants

Arabidopsis thaliana (L.) Heynh. has been used as a model system to investigate the regulatory genes that control and coordinate the determination, differentiation and morphogenesis of the floral meristem and floral organs. We show here that benzylaminopurine (BAP), a cytokinin, influences flower development inArabidopsis and induces partial phenocopies of known floral homeotic mutants. Application of BAP to wild-type inflorescences at three developmental stages results in: (i) increase in floral organ number; (ii) formation of abnormal floral organs and (iii) induction of secondary floral buds in the axils of sepals. These abnormalities resemble the phenotypes of mutants,clv1 (increase in organ number),ap1,ap2,ap3 (abnormal floral organs) andap1 (secondary floral buds in the axils of first-whorl organs). In addition, BAP induces secondary floral buds in the axils of perianth members ofapt2-6, ap3-1 andag mutants, and accentuates the phenotype of theapt2-1 mutant to resemble theapt2-6 mutant. These observations suggest that exogenous BAP suppresses the normal functioning of the genes for floral meristem identity and thereby affects flower development and the later stages of floral organ differentiation.Abbreviations BAP N6-benzylaminopurine - CK cytokinin     

Regulation of potato meristem development by jasmonic acid in vitro

The influence of jasmonic acid (JA) on differentiation of meristems of the potato,Solanum tuberosum cv. Vesna, was investigated in vitro. Meristems were grown on Murashige and Skoog (MS) medium supplemented with indole-3-acetic acid (IAA) (10 M), kinetin (10 M), gibberellic acid (3 M), as modified by Bang. Addition of JA in concentrations of 0.5–10 M increased the number of meristems that developed into buds, particularly in meristems isolated from shoots grown from tubers in the dark. JA had no noticeable effect on meristems from germs grown in light. All added concentrations of JA retarded callus and root formation. The inhibitory effect on rhizogenesis disappeared immediately after transfer of the developed buds to medium without JA.