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.     

Cladodes,leaf-like organs in Asparagus,show the significance of co-option of pre-existing genetic regulatory circuit for morphological diversity of plants

Plants in the genus Asparagus have determinate leaf-like organs called cladodes in the position of leaf axils. Because of their leaf-like morphology, axillary position, and morphological variation, it has been unclear how this unusual organ has evolved and diversified. In the previous study, we have shown that cladodes in the genus Asparagus are modified axillary shoots and proposed a model that cladodes have arisen by co-option and deployment of genetic regulatory circuit (GRC) involved in leaf development. Moreover, we proposed that the alteration of the expression pattern of genes involved in establishment of adaxial/abaxial polarity has led to the morphological diversification from leaf-like to rod-like form of cladodes in the genus. Thus, these results indicated that the co-option and alteration of pre-existing GRC play an important role in acquisition and subsequent morphological diversification.Here, we present data of further expression analysis of A. asparagoides. The results suggested that only a part of the GRC involved in leaf development appears to have been co-opted into cladode development. Based on our study and several examples of the morphological diversification, we briefly discuss the importance of co-option of pre-existing GRC and its genetic modularity in the morphological diversity of plants during evolution.     

Acquisition and diversification of cladodes: leaf-like organs in the genus Asparagus

The genus Asparagus is unusual in producing axillary, determinate organs called cladodes, which may take on either a flattened or cylindrical form. Here, we investigated the evolution of cladodes to elucidate the mechanisms at play in the diversification of shoot morphology. Our observations of Asparagus asparagoides, which has leaf-like cladodes, showed that its cladodes are anatomically and developmentally similar to leaves but differ in the adaxial/abaxial polarity of the vasculature. In addition to the expression of an ortholog of KNAT1, orthologous genes that are normally expressed in leaves, asymmetric leaves1 and HD-ZIPIII, were found to be expressed in cladode primordia in a leaf-like manner. The cylindrical cladodes of Asparagus officinalis showed largely similar expression patterns but showed evidence of being genetically abaxialized. These results provide evidence that cladodes are modified axillary shoots, suggest that the co-option of preexisting gene networks involved in leaf development transferred the leaf-like form to axillary shoots, and imply that altered expression of leaf polarity genes led to the evolution of cylindrical cladodes in the A. officinalis clade.     

A new conception of the shoot of higher plants

According to the classical model, the “shoot” consists only of the categories “caulome” (“stem” sensu lato) and “phyllome” (“leaf” sensu lato), (and “root” in cases of “adventitious” root formation). If lateral shoots are present, their position is axillary. Consequently, caulome as well as phyllome are inserted on the caulome and only on the caulome. This classical model of the shoot has two disadvantages of great consequence: (1) Intermediate organs cannot be accepted as such, but have to be interpreted (i.e. categorized) as either caulome or phyllome (or root) by distortion of the actual similarity. (2) Certain positional changes of organs cannot be accepted as such, but have to be “explained” by congenital fusion. The new conception of the shoot will have the advantages of the classical model but not its disadvantages. Hence, the shoot may consist of the following parts: (main and lateral) shoot, caulome, phyllome, root, emergence, and structures intermediate between (i.e. partially homologous to) any of the preceding. Thus, the five categories of the classical model, namely “shoot”, “caulome”, “phyllome”, “root” and “emergence” are no longer mutually exclusive; they may merge into each other due to an actual or potential continuum. Intermediate organs are therefore accepted as such; for example, an organ may be characterized as an intermediate form between a caulome and a phyllome. Besides intermediate forms, all changes in position are accepted as such. Hence, the following positional relations are possible: caulome and phyllome may be inserted on the caulome, caulome and phyllome may be inserted on the phyllome; roots may be inserted on caulome or phyllome; intermediate forms may be inserted on the caulome, phyllome, or other intermediate forms. Consequences of the new conception for morphological research are pointed out, especially for homologization, evolutionary considerations, and the direction in which research progresses.     

Cells within the nodal region of carnation shoots exhibit a high potential for adventitious shoot formation

Adventitious shoot formation was studied with leaf, stem and axillary bud explants of carnation (Dianthus caryophyllus L.). The shoot regeneration procedures were applicable for a wide range of cultivars and shoot regeneration percentages were high for all explant types. Using axillary bud explants, shoot regeneration efficiency was independent of the size of the bud and of its original position in the plant. In contrast, shoot regeneration from stem and leaf explants was strongly dependent on their original position on the plant. The most distal explants (just below the apex) showed the highest level of shoot regeneration. The adventitious shoot primordia developed at the periphery of the stem segment and at the base of leaf explants. In axillary bud, stem and leaf explants, shoot regeneration originated from node cells, located at the transition area between leaf and stem tissue. Moreover, a gradient in shoot regeneration response was observed, increasing towards the apical meristem.Abbreviations BA benzyladenine - NAA naphthaleneacetic acid     

Late Permian phylloclades of the new genus <Emphasis Type="Italic">Permophyllocladus</Emphasis> and problems of the evolutionary morphology of peltasperms

Phylloclades from the Upper Permian (Tatarian) deposits of the Sokovka locality, Vladimir Region, showing gradational transformation of a planate scale-leaved shoot into a foliar organ, are assigned to the new genus Permophyllocladus (Peltaspermales?). The phylloclades are distinctly dorsoventral: scaly leaves and their rudiments are developed on the lower side and are only marked by suture lines on the cuticle of the opposite side. In epidermal characteristics, the phylloclades are similar to the leaves of peltasperms from coeval deposits. It is supposed that peltasperm leaves are of phylloclade origin and were formed by cohesion of units of a coniferoid scale-leaved shoot that resembles shoots of the Mesozoic family Hirmerellaceae (Cheirolepidiaceae), which also tend to develop phylloclades.     

Regeneration from Phylloclade Explants and Callus Cultures of Schlumbergera and Rhipsalidopsis

Phylloclade explants of Schlumbergera and Rhipsalidopsis were cultured in vitro to produce axillary and adventitious shoots. The explants of both species, taken from greenhouse-grown plants, produced only axillary shoots. There was a pronounced improvement in adventitious shoot formation in phylloclade explants of cultivar CB4 of Rhipsalidopsis by increasing numbers of subcultures of axillary shoots used as donor plants. The axillary shoots generated from the explants were either subcultured to produce successive generations of axillary shoot cultures or made into phylloclade explants and tested for adventitious shoot formation at each subculture. The duration of each subculture varied from 6 to 12 weeks. After the first subculture, sporadic adventitious shoot formation began, and after the third subculture 87% explants of cultivar CB4 produced adventitious shoots at a frequency of about 12 shoots per explant. In contrast, there was no improvement in regenerative ability in explants of cultivar Thor-Olga of Schlumbergera up to third subculture. Adventitious shoots could be produced by callus culture too. Cultivar CB4 was highly regenerative, producing as many as 10 adventitious shoots per square cm of callus. In vitro grown plantlets, when transferred to pots continued to show prolific growth.     

Expression patterns of class I <Emphasis Type="Italic">KNOX</Emphasis> and <Emphasis Type="Italic">YABBY</Emphasis> genes in <Emphasis Type="Italic">Ruscus aculeatus</Emphasis> (Asparagaceae) with implications for phylloclade homology

STM (RaSTM) and YAB2 (RaYAB2) homologues were isolated from Ruscus aculeatus (Asparagaceae, monocots), and their expressions were analyzed by real-time polymerase chain reaction (PCR) to assess hypotheses on the evolutionary origin of the phylloclade in the Asparagaceae. In young shoot buds, RaSTM is expressed in the shoot apex, while RaYAB2 is expressed in the scale leaf subtending the shoot bud. This expression pattern is shared by other angiosperms, suggesting that the expression patterns of RaSTM and RaYAB2 are useful as molecular markers to identify the shoot and leaf, respectively. RaSTM and RaYAB2 are expressed concomitantly in phylloclade primordia. These results suggest that the phylloclade is not homologous to either the shoot or leaf, but that it has a double organ identity.     

Organ correlations and flowering in chenopodium rubrum L.

Correlations within a shoot ofChenopodium rubrum L. ecotype 374 grown under continuous light or photoperiodic flower induction were studied using surgical treatments. Removal of a single pair of shoot organs had a variety of effects depending on position: significant changes in the number of leaf pair on the main axis or in axillary buds and in the height of shoot apices; or no effect on the parameters scored. Flowering was not affected by any of the treatments carried out. Decapitation brought about a significant increase in the number of leaf pairs in axillary buds and flowering was inhibited in 8- and 9-d old plants. Flowering was not affected in 21-d old plants. The role of shoot organ correlations, especially that of apical dominance, in regulation of flowering inC.rubrum is discussed.     

Developmental shoot morphology in Phyllocladus (Podocarpaceae)

TOMLINSON, P. B., TAKASO, T. & RATTENBURY, J. A., 1989. Developmental shoot morphology in Phyllocladus (Podocarpaceae). Shoot architecture in the adult phase of Phyllocladus is established by a succession of units of extension that develop a system of permanent axes supporting photosynthetic units (phylloclades) each of which represents a branch complex with three branch orders. Seedlings have needle foliage leaves comparable to those of other conifers, but in adult plants all leaves are ephemeral, non-photosynthetic scales that for the most part subtend no axillary buds. Once rhythmic growth (usually seasonal) is established in the adult phase, each increment produces a whorl of phylloclades so that a regular tiered arrangement develops, with the tiers progressively reduced on outer units. In the resting terminal bud of permanent axes only scale primordia are present; with bud burst and beginning of extension of the unit the phylloclades are produced by syllepsis and complete the initiation and expansion of all axis orders in the short flushing cycle. Segments retain strict distichy throughout, but in a dorsiventral and not a lateral plane. Phylloclades may be either determinate, when the apex of the first-order axis develops as a terminal flattened segment, or indeterminate, when the apex retains radial symmetry and forms a resting bud that can continue axis extension as a permanent shoot in subsequent years. A phylloclade consequently only produces flattened lateral segments in its season of initiation. Reiteration from reserve buds is not possible, because none are produced in the adult phase, but is possible from detached meristems formed in the axils of needle leaves on juvenile shoots. Reiteration in the adult phase is thus possible only by axis dedifferentiation, that is, change from plagiotropy to orthoptropy. The distinctive massive vascular connection of the phylloclade is made possible by syllepsis. In this way the normal structural constraints of elaborate appendage development in conifers is fully overcome.     

THE TENDRIL OF PARTHENOCISSUS INSERTA: DETERMINATION AND DEVELOPMENT

Tendrils on long shoots of Parthenocissus inserta occur in a regular pattern opposite the alternate distichous leaves at two successive nodes of each three nodes. Ontogenetic study shows that the tendril is initiated at the flank of the shoot apex during the second plastochron in an essentially axillary position. It is carried upward with growth of the internode above the axillant leaf and ultimately is situated opposite the next younger leaf. In a rhythmic pattern a different group of appendages is produced by the shoot apex at each node in the sequence of three. In acropetal order these are: at the tendrilless node the leaf subtends an axillary bud complex which in turn subtends a tendril; the leaf at the lower tendril-bearing node directly subtends a tendril, and the leaf at the upper tendril-bearing node subtends an axillary bud. Tendril primordia were not induced to develop as foliaceous shoots when cultured in vitro or in decapitation experiments, indicating that the meristem which becomes a tendril is determined early in its inception. Although built on a shoot pattern, the tendril is regarded as an organ sui generis with a possible relationship to the inflorescence. The morphological nature of the tendril is discussed in the light of theories postulated in the literature.     

Quantitative analyses of shade-shoot architecture of conifers native to New Zealand

Shoot architecture was quantified by measuring the "maximum silhouette area ratio" (R_max). R_max was calculated from the maximum silhouette area (or projected area) of the intact shoot, divided by the silhouette area of the leaves or phylloclades (leaf-like flattened stems) when they are removed from the shoot and laid out flat. Like conifers of the Northern Hemisphere (NH) with non-appressed foliage, the R_max of shade-adapted shoots ranged from 0.5 to 1.0 in New Zealand (NZ) conifers with non-appressed foliage. Defining a "leaf" to mean either a true leaf or a phylloclade, the following was found: leaf area/leaf dry weight, leaf area/shoot dry weight, and leaf dry weight/shoot dry weight, were all similar in the shade-shoots of NZ and NH conifers. None of these variables were significantly correlated with R_max in the NZ conifers, unless species with leaves averaging less than 4 mm² in size were excluded from the analyses. Foliage dry weight/shoot projected area was strongly correlated with R_max. NZ conifers had both smaller and larger mean leaf sizes in comparison to NH conifers. The mean projected area per shade-adapted leaf of NZ conifers varied from 2.7 to 436 mm². In NH conifers, the mean projected area per shade leaf varied from 12 to 83 mm². Except for the strikingly larger range in leaf size in NZ conifers, the data support a hypothesis of strong convergent evolution of shade-shoot architecture in NZ and NH conifers. The results are discussed in relation to photosynthesis, stand production, and the ecological distribution of conifers.     

Influence of explant source, plant growth regulators and culture environment on culture initiation and establishment of Quercus robur L. in vitro

Suitable cytokinin supplements and culture environments havebeen determined for the initiation and establishment of shootcultures of Quercus robur seedling tissue. Initiation of axillaryshoot development from nodal explants required culture mediumsupplemented with BA (6-benzylamminopurine). The greatest numbersof stem segments for culture proliferation were obtained using1.0 mg I^-1 BA after 56 d culture. The frequency of shoot developmentand subsequent formation of multiple shoots at initiation wasinfluenced by the position of the nodal explant in the seedlingshoot, incubation temperature and daylength. Explants from basaland apical regions, which contained multiple axillary buds,produced the lowest frequencies of axillary shoot developmentand multiple shoot formation, many remained quiescent. Axillaryshoot development was greatest in single nodal explants excisedfrom the midstem positions, elongated regions of the shoot wherenodes were formerly associated with a leaf. Higher temperaturesstimulated shoot formation with greater numbers of stem segmentsfor culture multiplication being obtained from nodal explantsincubated at 25C. Axillary shoot development was promoted innodal explants maintained under daylengths of 16 h or more.Stem segments cut from axillary shoots which developed fromnodal explants were used to establish shoot multiplication cultureson medium supplemented with 0.4 mg I^-1 BA. Shoot formation fromstem segments was greater at higher incubation temperaturesof 25C and 30C. Multiplication coefficients for stem segmentsincreased after one subculture. Key words: Quercus robur, oak, micropropagation, cytokinin, temperature, daylength, rest, quiescence     

The developmental morphology ofIndotristicha ramosissima (Podostemaceae,Tristichoideae)

The developmental morphology ofIndotristicha ramosissima, a submerged rheophyte from South India, is described. Besides creeping organs (called roots) there are branched shoots with two kinds of short-lived photosynthetic appendages: scales and compound structures (called ramuli). These ramuli may be interpreted as leaf-stem intermediates because they combine typical leaf characters (extra-axillary position, determinate growth, subtending an axillary bud) and typical stem characters (nearly radial symmetry, acropetal development with apical meristem, arrangement of the scaly subunits helical or irregular). Floral shoots arise from axillary exogenous buds along the vegetative shoots, occasionally also from endogenous buds along the roots and vegetative shoots. The uppermost scales and ramuli of each floral shoot form a cup-like structure around the base of the terminal flower.Indotristicha is thought to be primitive within theTristichoideae (Podostemaceae). Some morphogenetic switches are postulated in order to deriveIndotristicha from a putative ancestor that still showed the classical root-shoot model typical of most angiosperms.     

SHOOT MERISTEMLESS trafficking controls axillary meristem formation,meristem size and organ boundaries in Arabidopsis

The shoot stem cell niche, contained within the shoot apical meristem (SAM) is maintained in Arabidopsis by the homeodomain protein SHOOT MERISTEMLESS (STM). STM is a mobile protein that traffics cell‐to‐cell, presumably through plasmodesmata. In maize, the STM homolog KNOTTED1 shows clear differences between mRNA and protein localization domains in the SAM. However, the STM mRNA and protein localization domains are not obviously different in Arabidopsis, and the functional relevance of STM mobility is unknown. Using a non‐mobile version of STM (2xNLS‐YFP‐STM), we show that STM mobility is required to suppress axillary meristem formation during embryogenesis, to maintain meristem size, and to precisely specify organ boundaries throughout development. STM and organ boundary genes CUP SHAPED COTYLEDON1 (CUC1), CUC2 and CUC3 regulate each other during embryogenesis to establish the embryonic SAM and to specify cotyledon boundaries, and STM controls CUC expression post‐embryonically at organ boundary domains. We show that organ boundary specification by correct spatial expression of CUC genes requires STM mobility in the meristem. Our data suggest that STM mobility is critical for its normal function in shoot stem cell control.     

DIVERSITY OF SHOOT MORPHOLOGY IN TYPHONIUM (ARACEAE)

The details of shoot organization, including number of leaves per shoot, position of foliage leaves and cataphylls, position of the lateral continuation shoot, nature of axillary buds and phyllotaxis, and the pattern of shoot extension were observed and compared in five species of Typhonium, Dracunculus vulgaris, Sauromatum venosum, Arum italicum, and Helicodiceros muscivorus, resulting in the recognition of four types of stems. Three of the four types were found in the genus Typhonium. One type was found in Typhonium giganteum and Sauromatum venosum and is presumably the same in Biarum. Another type, found in T. trilobatum, T. blumei, and T. flagelliforme, is distinct in the position of the lateral continuation shoot, which arises from the axil of the n-1 leaf and is adnate to the axis to above the n leaf. Based on the results, two groups, one of which is further subdivided into two subgroups, are recognized in subtribe Arinae (subfam. Aroideae tribe Areae).     

Development of Axillary and Leaf-opposed Buds in Rattan Palms

Axillary vegetative buds are present in Calamus, Ceratolobus,and Plectocomiopsis. Two species of Daemonorops Sect. Piptospathaalso have axillary vegetative buds. All species of Daemonoropshave only displaced adnate axillary inflorescence buds. A singlebud is initiated in the axil of the first or second leaf primordiumin a way similar to that for axillary inflorescence buds. Themeristem is displaced during development on to the internodeabove and sometimes on to the base of the leaf above. Leaf-opposedvegetative buds occur in five species of Daemonorops Sect. Cymbospathaand in one species of Daemonorops Sect. Piptospatha. This typeof bud is initiated 180° away from the axil of the firstor second leaf primordium. It is not a displaced axillary bud,but does become adnate to the internode above like the axillarybuds. One or more leaves, transitional between juvenile andadult, on a shoot often subtend both types of buds. Myrialepishas leaf-opposed vegetative buds, but their development wasnot observed. Korthalsia has buds that are displaced about 130°from the leaf axil and are intermediate between the axillaryand the leaf-opposed condition. Other forms of vegetative budsare described: multiple buds in Plectocomia, aerial forkingin Korthalsia, and suckering from inflorescences and from aerialstems in Calamus. bud development, rattan palms, palm taxonomy, branching     

Classical and dynamic morphology: toward a synthesis through the space of forms

In plant morphology, most structures of vascular plants can easily be assigned to pre-established organ categories. However, there are also intermediate structures that do not fit those categories associated with a classical approach to morphology. To integrate the diversity of forms in the same general framework, we constructed a theoretical morphospace based on a variety of modalities where it is possible to calculate the morphological distance between plant organs. This paper gives emphasis on shoot, leaf, leaflet and trichomes while ignoring the root. This will allow us to test the hypothesis that classical morphology (typology) and dynamic morphology occupy the same theoretical morphospace and the relationship between the two approaches remains a question of weighting of criteria. Our approach considers the shoot (i.e. leafy stem) as the basic morphological structural unit. A theoretical data table consisting of as many lines as there are possible combinations between different modalities of characters of a typical shoot was generated. By applying a principal components analysis (PCA) to these data it is possible to define a theoretical morphospace of shoots. Typical morphological elements (shoots, leaves, trichomes) and atypical structures (phylloclades, cladodes) including particular cases representing ‘exotic’ structures such as the epiphyllous appendages of Begonia and ‘water shoot’ and ‘leaf’ of aquatic Utricularia were placed in the morphospace. The more an organ differs from a typical shoot, the further away it will be from the barycentre of shoots. By giving a higher weight to variables used in classical typology, the different organ categories appear to be separate, as expected. If we do not make any particular arbitrary choice in terms of character weighting, as it is the case in the context of dynamic morphology, the clear separation between organs is replaced by a continuum. Contrary to typical structures, “intermediate” structures are only compatible with a dynamic morphology approach whether they are placed in the morphospace based on a ponderation compatible with typology or dynamic morphology. The difference in points of view between typology and continuum leads to a particular mode of weighting. By using an equal weighting of characters, contradictions due to the ponderation of characters are avoided, and the morphological concepts of continuum’ and ‘typology’ appear as sub-classes of ‘process’ or ‘dynamic morphology’.     

Ethylene Modulates the Developmental Plasticity and the Growth Balance Between Shoot and Root Systems in the In Vitro Grown Epiphytic Orchid Catasetum fimbriatum

The epiphytic habitat is potentially one of the most stressful environments for plants, making the effective developmental control in response to external cues critical for epiphyte survival. Because ethylene mediates several abiotic stresses in plants, here, we have examined the ethylene influence in both shoot and root systems of the epiphytic orchid Catasetum fimbriatum. Under controlled conditions, ethylene production was quantified during an entire growth cycle of C. fimbriatum development in vitro, while treatments modulating either ethylene concentration or perception were carried out over the early growth phase of these plants. After treatments, growth measurements and histological features were studied in both shoot and root tissues. Ethylene production showed a decreasing trend over the period of organ elongation; however, it increased considerably when leaves were shed, and a new axillary bud was initiating. The early exposure of young plants to higher concentrations of ethylene triggered morphogenic responses that included root hair formation instead of velamen, and a combination of inhibitory effects (decreases in both stem enlargement and cellular/organ elongation) and inductive effects (increases in leaf and root formation, bud initiation and cellular thickening) on plant growth, which favored biomass allocation to roots. Conversely, inhibition of ethylene perception over the plant growth phase generally resulted in the opposite morphogenic responses. Our data indicate that periodic variations in ethylene concentration and/or sensitivity seem to modulate several developmental features in shoot and root systems of C. fimbriatum which could have adaptive significance during the growing phase of this epiphytic orchid.