Inflorescence morphology, heterochrony, and phytogeny in the mimosoid tribes ingeae and acacieae (Leguminosae: Mimosoideae)

In earlier work (Grimes, 1992) on inflorescence morphology in the mimosoid tribes Ingeae and Acacieae I proposed that differences in inflorescence morphology result from three properties: the organization of components of the inflorescence and their relative positions; the hierarchical arrangement of the axes of the inflorescence and the position they assume in total tree architecture; and the heterochronic development of components of the inflorescence. Further work shows that the first two properties are better stated in terms of heterochrony; namely, that the organization of components of the inflorescence differs due to differences in timing of the development of organ systems and that the hierarchy of axes likewise differs due to heterochronic changes. Neither de novo origin of organs or organ systems nor suppression or loss of organs or organ systems accounts for the diversity in form. Observed heterochronic differences in the inflorescence structure may be divided into three types: spatial differences in the relationship between the unit inflorescence and the subtending leaf (hysteranthy); differences in the time of formation and/or the duration of whole axes; and changes in development pathways, leading to shoot dimorphism. These heterochronies are used as characters in a cladistic analysis, and it is shown that although some are homoplasious, many provide synapomorphies of clades of exemplars representing genera in the Ingeae and Acacieae.     

叶发育的遗传调控机理研究进展

叶是植物进行光合作用的主要器官。高等植物叶原基起始于顶端分生组织的周边区,在一系列基因精确调控下,叶原基建立近一远轴、基一顶轴和中．侧轴极性,引导原基细胞朝着特定的方向分裂和分化,最终发育戍一定形态和大小的叶片。近年来分子遗传学研究结果表明,数个转录因子家族基因、小分子RNA和细胞增殖相关因子组成一个复杂的遗传控制网络,调节叶片极性建成过程。此外,复叶的形态建成还受到另外一些转录因子的调控。本文对近年来叶发育遗传调控机理研究的新进展做简要介绍。     

Making leaves

Leaves are determinate organs that develop from the flanks of the shoot apical meristem through founder cell recruitment, establishment of proximodistal, dorsoventral and mediolateral axes, and subsequent growth, expansion and differentiation along these axes. Maintenance of the shoot apical meristem and production of leaves requires balanced partitioning of cells between pluripotent and differentiation fates. Hormones have a significant role in this balance but it is becoming apparent that additional intrinsic and extrinsic inputs influence hormone signalling to control meristem function and leaf initiation. As leaves develop, temporal and spatial regulation of growth and maturation determines leaf shape and complexity. Remarkably genes involved in leaf development in the context of the shoot apical meristem are also involved in elaboration of the leaf shape to generate subtle marginal serrations, more prominent lobes or a dissected compound leaf. Potentially these common regulatory modules represent a fundamental means of setting up boundaries separating discrete zones of growth. Defining gene networks involved in leaf shape variation and exploring interspecies differences between such networks is enabling exciting insight into changes that contribute to natural variation of leaf form.     

SHOOT GROWTH AND LEAF DIMORPHISM IN BOSTON IVY (PARTHENOCISSUS TRICUSPIDATA)

Boston ivy, a common ornamental vine in the grape family, successively produces two kinds of leaves during the growing season. The two “early leaves” at the base of each shoot are preformed in the winter bud, and their expansion in the spring is accompanied by little stem elongation. At maturity they have large three-lobed blades and long petioles. Most short shoots produce no more leaves, but “late leaves” develop on all long shoots at intervals of less than 2 days. All but the first few undergo their entire development during the growing season. They are much smaller than early leaves, and the lateral lobes of their blades are reduced or eliminated. They are separated from the early leaves and from each other by long internodes. The early and late leaves differ in the circumstances and continuity of ontogeny, and diverge in form at an early stage. This vine and its relatives are unique in their three-node cyclical pattern of organ occurrence and internode length along the shoot. Lateral shoots and buds are present at every third node, with tendrils at intervening nodes. The long shoots branch freely and repeatedly, and the production of late leaves and new shoot axes by vigorous compound shoots is limited only by the growing season. Despite its specialized organization, Boston ivy resembles several tree species in its association between a seasonal type of leaf dimorphism and a shoot system constructed of long and short shoots.     

Anatomy and development of the fern sporophyte

Recent research on the developmental anatomy and morphology of the fern sporophyte is reviewed. Detailed histological and experimental studies of the organization of the fern shoot apical meristem have reconfirmed the recently controversial role of the shoot apical cell as the single apical initial of the meristem. The shoot apical meristem is nevertheless an anatomically and functionally complex structure with a strongly zoned cytohistological organization. Fern shoot apex organization can be compared with that of seed plants. The control of leaf initiation and phyllotaxy remains poorly understood. Studies differ as to whether leaf initiation in ferns involves one leaf mother cell or a multicellular region of the shoot apex. The concept of non-appendicular fronds is refuted for living ferns. The later developmental changes in the determinate leaf apical and marginal meristems of the leaf primordium form an area that is still largely unexplored but could be investigated by methods similar to those used to study shoot and root apices. Branching in ferns is morphologiclaly and developmentally diverse. There is apparently more than one developmental mode of dichotomous branching, and several modes of lateral bud formation have been described, including the phyllogenous initiation of branches at the base of leaf primordia. Developmental changes in bud meristems related to apical dominance, inhibition, and bud activation is another major area for continued study. The traditional concept of the role of the root apical cell has been reestablished by studies similar to those made of the shoot apex. Detailed ultrastructural investigations of the root ofAzolla have given a sophisticated new picture of developmental processes in that organ. Fern roots show remarkably precise patterns of histogenesis in relation to apical segmentation. The formation of secondary vascular tissue inBotrychium suggests that the Ophioglossales may be related to the seed plants. The causal relationship of leaf (and branch and root) formation and the initiation of vascular tissue in the shoot needs more study. Although still poorly understood, protoxylem systems in ferns are variable and may have morphological and systematic significance. Recent investigations of hydraulic conductance in fern stems have found possible correlations of conductance levels with growth forms. The anatomical diversity of ferns makes comparative functional anatomy a promising field for future study.     

Phylloclade development in the Asparagaceae: an example of homoeosis

Phylloclades are traditionally defined as flattened, determinate, leaf-like stems primarily on the basis of their axillary position. However, because the literature is replete with controversy over the morphological interpretation of these organs, a study of phylloclade development in comparison with leaf and stem development was undertaken in four closely related species of the Asparagaceae: Ruscus aculeatus, Danae racemosa, Semele androgyna and Asparagus densiflorus. Results reveal a continuum in phylloclade development from very leaf-like forms, such as those of Danae , via the more intermediate types of Ruscus , to the gradually more shootlike forms of Semele and Asparagus. This continuum results from a differential expression of stem (or shoot) and leaf characteristics in an axillary position. When stem (or shoot) and leaf features are combined, as in the fertile phylloclade of Ruscus , an intermediate organ is formed. Phylloclades are a form of evolutionary novelty that exemplifies the phenomenon of homoeosis, which is the transference of features from one organ to another. Developmentally, this means that leaf features are expressed by the axillary meristem.     

Shoot organization genes regulate shoot apical meristem organization and the pattern of leaf primordium initiation in rice

The mechanism regulating the pattern of leaf initiation was analyzed by using shoot organization (sho) mutants derived from three loci (SHO1, SHO2, and SHO3). In the early vegetative phase, sho mutants show an increased rate of leaf production with random phyllotaxy. The resulting leaves are malformed, threadlike, or short and narrow. Their shoot apical meristems are relatively low and wide, that is, flat shaped, although their shape and size are highly variable among plants of the same genotype. Statistical analysis reveals that the shape of the shoot meristem rather than its size is closely correlated with the variations of plastochron and phyllotaxy. Rapid and random leaf production in sho mutants is correlated with the frequent and disorganized cell divisions in the shoot meristem and with a reduction of expression domain of a rice homeobox gene, OSH1. These changes in the organization and behavior of the shoot apical meristems suggest that sho mutants have fewer indeterminate cells and more determinate cells than wild type, with many cells acting as leaf founder cells. Thus, the SHO genes have an important role in maintaining the proper organization of the shoot apical meristem, which is essential for the normal initiation pattern of leaf primordia.     

Leaf and stem growth in the Lepidodendrales

Measurement of leaf length and stem diameter in three Upper Carboniferous l.epidodendron species shows an exponential relationship between these parameters. Larger axes bear longer leaves even in material which had apparently completed its primary' growth. It is suggested that this is a direct product of the determinate growth pattern of the ontogeny of arborescent lycopods. Measurements of Cyclostigma from the Irish Devonian are not explicable in these terms, and it is suggested that some specimens were immature at fossilization. It is recommended that the term leaf cushion be applied to the expanded leaf base in the Lepidodendrales at all growth stages, and not only after leaf abscission. Problems in the terminology of 'young' and 'old' growth stages in these determinate plants are discussed.     

CORKSCREW1 defines a novel mechanism of domain specification in the maize shoot

In higher plants, determinate leaf primordia arise in regular patterns on the flanks of the indeterminate shoot apical meristem (SAM). The acquisition of leaf form is then a gradual process, involving the specification and growth of distinct domains within the three leaf axes. The recessive corkscrew1 (cks1) mutation of maize (Zea mays) disrupts both leaf initiation patterns in the SAM and domain specification within the mediolateral and proximodistal leaf axes. Specifically, cks1 mutant leaves exhibit multiple midribs and leaf sheath tissue differentiates in the blade domain. Such perturbations are a common feature of maize mutants that ectopically accumulate KNOTTED1-like homeobox (KNOX) proteins in leaf tissue. Consistent with this observation, at least two knox genes are ectopically expressed in cks1 mutant leaves. However, ectopic KNOX proteins cannot be detected. We therefore propose that CKS1 primarily functions within the SAM to establish boundaries between meristematic and leaf zones. Loss of gene function disrupts boundary formation, impacts phyllotactic patterns, and leads to aspects of indeterminate growth within leaf primordia. Because these perturbations arise independently of ectopic KNOX activity, the cks1 mutation defines a novel component of the developmental machinery that facilitates leaf-versus-shoot development in maize.     

Influence of nitrogen availability on shoot development in young peach trees [Prunus persica (L.) Batsch]

It is commonly stated that nitrogen (N) influences biomass accumulation in plants. For trees, however, a precise characterisation of shoot response to N and its impact on architecture is lacking. We attempted to study on the phytomer scale the effects of N limitation on shoot growth components, i.e. leaf emergence rate, final internode length and branching on the main and secondary axes of 1-year-old peach trees [Prunus persica (L.) Batsch]. Trees were grown on recycled nutrient solutions in which N concentration was restored once a week. We used two hydroponic set-ups in which weekly N availability, i.e. amount of N per tree, differed being either low (N1) or high (N2). Net N availability was defined weekly as the relative amount of N remaining in each set-up before solution replenishment. It declined with time and three periods of contrasting net N availability were identified. During these periods, leaf emergence rate and final internode length were similar on the main axis of N1 and N2 trees, so too was the distribution of secondary axes along the main axis. Secondary axes responded to N limitation by decreasing their growth components according to their position along the main axis. Differences were most important for basal secondary axes. Leaf emergence rate and final internode length responded similarly to N availability depending on axis order and position in the tree. It was concluded that N availability, particularly during the period of maximum growth of axes, influenced the shoot growth components and thus tree architecture.     

Auxin Depletion from the Leaf Axil Conditions Competence for Axillary Meristem Formation in Arabidopsis and Tomato

The enormous variation in architecture of flowering plants is based to a large extent on their ability to form new axes of growth throughout their life span. Secondary growth is initiated from groups of pluripotent cells, called meristems, which are established in the axils of leaves. Such meristems form lateral organs and develop into a side shoot or a flower, depending on the developmental status of the plant and environmental conditions. The phytohormone auxin is well known to play an important role in inhibiting the outgrowth of axillary buds, a phenomenon known as apical dominance. However, the role of auxin in the process of axillary meristem formation is largely unknown. In this study, we show in the model species Arabidopsis thaliana and tomato (Solanum lycopersicum) that auxin is depleted from leaf axils during vegetative development. Disruption of polar auxin transport compromises auxin depletion from the leaf axil and axillary meristem initiation. Ectopic auxin biosynthesis in leaf axils interferes with axillary meristem formation, whereas repression of auxin signaling in polar auxin transport mutants can largely rescue their branching defects. These results strongly suggest that depletion of auxin from leaf axils is a prerequisite for axillary meristem formation during vegetative development.     

Phylloclade development in the Asparagaceae: an example of homoeosis

Phylloclades are traditionally defined as flattened, determinate, leaf-like stems primarily on the basis of their axillary position. However, because the literature is replete with controversy over the morphological interpretation of these organs, a study of phylloclade development in comparison with leaf and stem development was undertaken in four closely related species of the Asparagaceae: Ruscus aculeatus, Danae racemosa, Semele androgyna and Asparagus densiflorus. Results reveal a continuum in phylloclade development from very leaf-like forms, such as those of Danae, via the more intermediate types of Ruscus, to the gradually more shootlike forms of Semele and Asparagus. This continuum results from a differential expression of stem (or shoot) and leaf characteristics in an axillary position. When stem (or shoot) and leaf features are combined, as in the fertile phylloclade of Ruscus, an intermediate organ is formed. Phylloclades are a form of evolutionary novelty that exemplifies the phenomenon of homoeosis, which is the transference of features from one organ to another. Developmentally, this means that leaf features are expressed by the axillary meristem.     

Morphological factors of the central whorl leaf associated with leaf surface wetness and resistance in sorghum to shoot fly,Atherigona soccata*

Earlier studies showed that leaf surface water on the central whorl leaf of sorghum seedlings is associated with resistance to shoot fly. In this study, the results of an experiment to determine if leaf surface wetness (LSW) originates from atmospheric condensation or from the plant are described. Morphological structures: trichomes, stomata, leaf cuticle and quantity of surface wax of the central whorl leaf were also examined for their role in LSW production. The results suggest that LSW of the central whorl leaf originates from the plant and is not due to condensation of atmospheric moisture. The presence of trichomes was indirectly associated with LSW and resistance to shoot fly but stomatal density was not associated with LSW production. The amount of wax extracted per 100 mg of fresh weight varied significantly between genotypes and seedling age. It was more in susceptible than in resistant genotypes; however, cuticular thickness was not associated with resistance. It is suggested that LSW could be the result of some form of cuticular movement of water to the leaf surface.     

Initiation of axillary and floral meristems in Arabidopsis

Shoot development is reiterative: shoot apical meristems (SAMs) give rise to branches made of repeating leaf and stem units with new SAMs in turn formed in the axils of the leaves. Thus, new axes of growth are established on preexisting axes. Here we describe the formation of axillary meristems and floral meristems in Arabidopsis by monitoring the expression of the SHOOT MERISTEMLESS and AINTEGUMENTA genes. Expression of these genes is associated with SAMs and organ primordia, respectively. Four stages of axillary meristem development and previously undefined substages of floral meristem development are described. We find parallels between the development of axillary meristems and the development of floral meristems. Although Arabidopsis flowers develop in the apparent absence of a subtending leaf, the expression patterns of AINTEGUMENTA and SHOOT MERISTEMLESS RNAs during flower development suggest the presence of a highly reduced, "cryptic" leaf subtending the flower in Arabidopsis. We hypothesize that the STM-negative region that develops on the flanks of the inflorescence meristem is a bract primordium and that the floral meristem proper develops in the "axil" of this bract primordium. The bract primordium, although initially specified, becomes repressed in its growth.     

THE DEVELOPMENTAL BASIS OF ANISOPHYLLY IN SELAGINELLA MARTENSII. I. INITIATION AND MORPHOLOGY OF GROWTH

The dorsiventral shoot system of Selaginella martensii is characterized by opposite pairs of ventral and dorsal leaves that are dimorphic in size and form. This study was undertaken to determine if the smaller dorsal leaf can be appropriately regarded as an arrested form of the larger leaf. Although the pattern of cell divisions and cell enlargement associated with leaf initiation is similar for both leaf types, the extent of localized growth results in distinctly larger primordia on the ventral side of the shoot. Ventral leaf primordia are also distinguished by the early formation of more extensive mesophyll tissue. Regression analysis of quantitative data on leaf length vs. position and leaf width vs. length indicates that the growth pattern of ventral and dorsal leaves is significantly different. These observations indicate that the developmental pathways of the dimorphic leaves of Selaginella martensii do not diverge at a relatively late developmental stage, but rather can be distinguished from inception.     

Plant development controls leaf area expansion in alfalfa plants competing for light

Background and Aims

The growth of crops in a mixture is more variable and difficult to predict than that in pure stands. Light partitioning and crop leaf area expansion play prominent roles in explaining this variability. However, in many crops commonly grown in mixtures, including the forage species alfalfa, the sensitivity and relative importance of the physiological responses involved in the light modulation of leaf area expansion are still to be established. This study was designed to assess the relative sensitivity of primary shoot development, branching and individual leaf expansion in alfalfa in response to light availability.

Methods

Two experiments were carried out. The first studied isolated plants to assess the potential development of different shoot types and growth periods. The second consisted of manipulating the intensity of competition for light using a range of canopies in pure and mixed stands at two densities so as to evaluate the relative effects on shoot development, leaf growth, and plant and shoot demography.

Key Results

Shoot development in the absence of light competition was deterministic (constant phyllochrons of 32·5 °Cd and 48·2 °Cd for primary axes and branches, branching probability of 1, constant delay of 1·75 phyllochron before axillary bud burst) and identical irrespective of shoot type and growth/regrowth periods. During light competition experiments, changes in plant development explained most of the plant leaf area variations, with average leaf size contributing to a lesser extent. Branch development and the number of shoots per plant were the leaf area components most affected by light availability. Primary axis development and plant demography were only affected in situations of severe light competition.

Conclusions

Plant leaf area components differed with regard to their sensitivity to light competition. The potential shoot development model presented in this study could serve as a framework to integrate light responses in alfalfa crop models.     

SURVEY OF SHOOT ORGANIZATION IN THE ARACEAE

Shoot organization is examined in 87 species from 29 genera representing all six subfamilies of the Araceae and of Acorus, which has been placed in a separate family. Within each taxonomic group examined, the details of shoot organization are presented, including the types of segments and articles which make up the shoot, the degree of expansion of leaf blades, and the placement of buds along the shoots. Literature on shoot organization of the 29 genera is reviewed. The degree of correlation between shoot organization characteristics and systematic groupings is examined, and the utility of these characteristics for systematics is evaluated. It is found that within the taxa observed, the pattern of shoot organization provides a distinctive “fingerprint” at the generic or sectional level, sufficient for determination of the group. Some patterns which appear are pointed out: taxa with bisexual flowers usually produce a single inflorescence at the terminus of a vegetative article. A few taxa with bisexual flowers produce pairs of inflorescences at the ends of articles. Multiple inflorescences (more than two) at an article terminus occur only among taxa with unisexual flowers. Multiple inflorescences are associated with anisophyllous or homeophyllous sympodial growth, while single or paired inflorescences are associated with homeophyllous or intermittent homeophyllous sympodial growth. These patterns might be understood as the result of selection for flexibility of reproductive effort and of seasonal reproduction.     

Regulation of axis determinacy by the Arabidopsis PINHEAD gene

Plants produce proximal-distal growth axes with two types of growth potential: they can be indeterminate, in which case growth continues indefinitely, or they can be determinate, in which case growth is limited to the production of a single organ or a discrete set of organs. The indeterminate shoot axes of Arabidopsis pinhead/zwille mutants frequently are transformed to a determinate state. PINHEAD (PNH) is expressed in the central domain of the developing plant: the provascular tissue, the shoot apical meristem, and the adaxial (upper) sides of lateral organ primordia. Here, we show that ectopic expression of PNH on the abaxial (lower) sides of lateral organs results in upward curling of leaf blades. This phenotype correlates with a loss of cell number coordination between the two surfaces of the blade, indicating that ectopic PNH can cause changes in cell division rates. More strikingly, moving PNH expression from the central to the peripheral domain of the embryo causes transformation of the determinate cotyledon axis to an indeterminate state. We propose that growth axes are specified as determinate versus indeterminate in a PNH-mediated step. Our results add to a growing body of evidence that radial positional information is important in meristem formation. These results also indicate that genes regulating cell division and axis determinacy are likely to be among PNH targets.     

Weeds of change: Cardamine hirsuta as a new model system for studying dissected leaf development

Cardamine hirsuta, a small crucifer closely related to the model organism Arabidopsis thaliana, offers high genetic tractability and has emerged as a powerful system for studying the genetic basis for diversification of plant form. Contrary to A. thaliana, which has simple leaves, C. hirsuta produces dissected leaves divided into individual units called leaflets. Leaflet formation requires activity of Class I KNOTTED1-like homeodomain (KNOX) proteins, which also promote function of the shoot apical meristem (SAM). In C. hirsuta, KNOX genes are expressed in the leaves whereas in A. thaliana their expression is confined to the SAM, and differences in expression arise through cis-regulatory divergence of KNOX regulation. KNOX activity in C. hirsuta leaves delays the transition from proliferative growth to differentiation thus facilitating the generation of lateral growth axes that give rise to leaflets. These axes reflect the sequential generation of cell division foci across the leaf proximodistal axis in response to auxin activity maxima, which are generated by the PINFORMED1 (PIN1) auxin efflux carriers in a process that resembles organogenesis at the SAM. Delimitation of C. hirsuta leaflets also requires the activity of CUP SHAPED COTYLEDON (CUC) genes, which direct formation of organ boundaries at the SAM. These observations show how species-specific deployment of fundamental shoot development networks may have sculpted simple versus dissected leaf forms. These studies also illustrate how extending developmental genetic studies to morphologically divergent relatives of model organisms can greatly help elucidate the mechanisms underlying the evolution of form.