Disentangling confusions in inflorescence morphology:Patterns and diversity of reproductive shoot ramification in angiosperms

Terminology of inflorescence diversity has often been used in a confusing way in the literature,partly because it was based on uncritical and outdated definitions.In particular,the terms cyme,thyrse,and panicle have been misused.Although a more critical classification worked out by several authors is available,it is unfortunately not in general use because most of the relevant publications are written in German.In addition,some terms have not been used in the same way by morphologists and developmental geneticists.The present review attempts to remedy the situation with a simple outline of a classification based on:(i)different branching patterns;(ii)differential elongation of axes of different orders;and(iii)repetition of basic ramification patterns in different ways.Racemose and cymose branching are two extreme patterns;the former with limitation of axial orders to two,the second with limitation of lateral axes of each order to two.In a branching system,a sequence of racemose→cymose and,within the cyme,of dichasial→monochasial is common,but the reverse sequence generally does not occur.Systematic and evolutionary aspects of inflorescences are briefly discussed.Branching patterns are often stable in larger clades.Inflorescences of mutants studied in developmental genetic studies are mainly altered in flower or branch numbers or relative branch length,but not in branching patterns.This is also a contribution towards the goal of a unified terminology for the different fields of biology dealing with inflorescences.     

SPIRAL DEVELOPMENTAL PATTERNS IN THE STEM AND INFLORESCENCE OF LILIUM TIGRINUM

Extensive correlations in spirality were observed among vegetative and floral organs in Lilium tigrinum Ker. Organs involved were vegetative leaves, bracts, and bracteoles. These correlations varied in their degree of constancy depending upon the organs involved. The mature inflorescences of L. tigrinum appeared to fit the common definition of a raceme. In 67.3% of the flowers at node 3 on the raceme, the bract-bracteole spirals reversed the spiral of vegetative leaves on the stem. These reversals resembled those observed on essentially cymose inflorescences of certain members of the Caryophyllaceae. Cymose branching was found to be an invariable feature of the inflorescence of L. tigrinum when secondary flowers appear. The apparently indeterminate tips of inflorescence main axes were interpreted as exhibiting stages in progression from a basically determinate (cymose) inflorescence. It was concluded that the ancestors of L. tigrinum had well-developed cymose branching patterns in the inflorescence. Reversal of stem spirals by the bract-bracteole spirals at the apices of many inflorescences was considered to be the result of complete utilization of the inflorescence meristem. Explanations for those reversals were provided by the field theory and by the theory of the first available space.     

Evolutionary origin of the Asteraceae capitulum: Insights from Calyceraceae

? Premise of the study: Phylogenies based on molecular data are revealing that generalizations about complex morphological structures often obscure variation and developmental patterns important for understanding the evolution of forms, as is the case for inflorescence morphology within the well-supported MGCA clade (Menyanthaceae + Goodeniaceae + Calyceraceae + Asteraceae). While the basal families share a basic thyrsic/thyrsoid structure of their inflorescences, Asteraceae possesses a capitulum that is widely interpreted as a racemose, condensed inflorescence. Elucidating the poorly known inflorescence structure of Calyceraceae, sister to Asteraceae, should help clarify how the Asteraceae capitulum evolved from thyrsic/thyrsoid inflorescences. ? Methods: The early development and structure of the inflorescence of eight species (five genera) of Calyceraceae were studied by SEM, and patterns of evolutionary change were interpreted via phylogenetic character mapping. ? Key results: The basic inflorescence structure of Calyceraceae is a cephalioid (a very condensed botryoid/thyrsoid). Optimization of inflorescence characters on a DNA sequence-derived tree suggests that the Asteraceae capitulum derives from a simple cephalioid through two morphological changes: loss of the terminal flower and suppression of the cymose branching pattern in the peripheral branches. ? Conclusions: Widely understood as a condensed raceme, the Asteraceae capitulum is the evolutionary result of a very reduced, condensed thyrsoid. Starting from that point, evolution worked separately only on the racemose developmental control/pattern within Asteraceae and mainly on the cymose developmental control/pattern within Calyceraceae, producing head-like inflorescences in both groups but with very different diversification potential. We also discuss possible remnants of the ancestral cephalioid structure in some Asteraceae.     

The questionable affinities of Lactoris: evidence from branching pattern, inflorescence morphology, and stipule development

The phylogenetically ambivalent monotypic genus Lactoris presents sympodial (determinate) branching, as a terminal flower is present on each main branch. The synflorescence is thyrsoid. Partial inflorescences are rhipidia with up to three flowers. The ochrealike stipule is formed by the fusion of two lateral stipules, which forms an adaxial ligule-like structure and a two-flanked leaf sheath that encircles the parental axis. The leaf sheath elongates with the growth of the preceding internode. Although sympodial growth and a sheathing leaf base are present in all Piperales (Aristolochiaceae, Lactoridaceae, Piperaceae, and Saururaceae), the presence of stipules is confined to Lactoris, Saururaceae, and some Piperaceae. These characters are consistent with the placement of Lactoris within Piperales, although its phylogenetic position within the order remains equivocal, except for the possible sister group relationship suggested by the presence of cymose inflorescences in both Lactoris and Aristolochiaceae.     

Ontogeny and structure of the acervulate partial inflorescence in Hyophorbe lagenicaulis (Arecaceae; Arecoideae)

Background and Aims

The palm tribe Chamaedoreeae displays flowers arranged in a complex partial inflorescence called an acervulus. This type of partial inflorescence has so far not been reported elsewhere in the largest palm subfamily Arecoideae, which is traditionally characterized by flowers predominantly arranged in triads of one central female and two lateral male flowers. The ontogenetic basis of the acervulus is as yet unknown and its structural diversity throughout the genera of the Chamaedoreeae poorly recorded. This study aims to provide critical information on these aspects.

Methods

Developmental series and mature inflorescences were sampled from plants cultivated in international botanical gardens and wild populations. The main techniques employed included scanning electronic microscopy and serial anatomical sectioning of resin-embedded fragments of rachillae.

Key Results

Inflorescence ontogeny in Hyophorbe lagenicaulis demonstrates that the acervulus and the inflorescence rachilla form a condensed and cymose branching system resembling a coenosome. Syndesmy results from a combined process of rapid development and adnation, without or with reduced axis elongation. Acervulus diversity in the ten taxa of the Chamaedoreeae studied is displayed at the level of their positioning within the inflorescence, their arrangement, the number of floral buds and their sexual expression.

Conclusions

The results show that a more general definition of the type of partial inflorescence observed within the large subfamily Arecoideae would correspond to a cyme rather than to a floral triad. In spite of their common cymose architecture, the floral triad and the acervulus present differences with respect to the number and arrangement of floral buds, the superficial pattern of development and sexual expression.     

The ramification of Apinagia riedelii: A key to the understanding of the plant architecture of Podostemaceae,subfamily Podostemoideae

The study of the ramification pattern of Apinagia riedelii results in a new concept of the architecture of this species, with general implications to members of subfamily Podostemoideae with dithecous leaves. The presence of a subtending leaf below the floriferous shoot proves axillary branching also for species with dithecous leaves. Previous opinions of an unusual ramification mode by subfoliar or non-axillary branching or stem bifurcation in combination with dithecous leaves hitherto pleaded for Podostemoideae is refuted. Moreover, the view of the so-called dithecous leaves with one sheath (theca) at the ventral and one at the dorsal side of the leaf, previously regarded as initially connected with branching, has to be changed. The dithecous leaf arises from the branch and not from the mother shoot axis – as previously believed – and represents the addorsed hypsophyll, i.e., the first leaf (prophyll) of the floriferous branch. This finding leads to the conclusion that the lower sheath of the dithecous leaf is the ventral (not dorsal) sheath pointing to the branch and surrounding its flower bud with a ligule or an ochrea and a hood upon the bud. In this way, the branch and its flower bud become seemingly sunk in the leaf base. At the fusion of leaf basis and shoot results this enigmatic common tissue. The wings of the dorsal (upper) sheath of the dithecous leaf point to the mother shoot axis of the branch. Successive floriferous branches along the main stem disclose the shoot axis of A. riedelii as a monopodium (not sympodium) that develops an anthocladial (foliated) inflorescence in the form of a botrys or a compound botrys, respectively. Since it is generally difficult to define cymose or racemose inflorescences if subtending leaves are absent – which occur in most other species of subfamily Podostemoideae with dithecous leaves – the nature of these inflorescences is discussed anew. The findings on A. riedelii have consequences on our comprehension of the shoot architecture of Podostemoideae.     

宽叶兔儿风花序侧生分枝的变异式样以及分枝兔儿风的分类地位问题

宽叶兔儿风Ainsliaealatifolia花序主轴上的侧生分枝通常被描述为由单个或2–4个头状花序聚集而组成的簇生花序。作者在野外和标本馆中仔细研究了该种居群内侧生分枝花序形态的变异,依据其简化和集中的程度在居群内区分出3种花序类型:简单的复合聚伞花序、复杂的复合聚伞花序以及两者之间的过渡类型,具有后面两种类型的个体在居群内少见。这一发现不仅为探讨兔儿风属内各种花序的演化提供了新的线索,而且为理清宽叶兔儿风这一地理广布种的分类学问题提供了新的视野。居群内有些侧生分枝为复杂的复合聚伞花序类型的个体整个花序的主轴折断了,这是由于整个主轴顶端部分被昆虫蛀食或者其他外力造成的。值得注意的是分枝兔儿风Ainsliaealatifoliavar.ramifera的主模式就属于这种情况。分枝兔儿风和宽叶兔儿风原变种之间在分布区、生境以及物候上并没有明显的分化,因此分枝兔儿风被处理成宽叶兔儿风的异名。     

Towards an ontogenetic understanding of inflorescence diversity

Backgrounds and Aims

Conceptual and terminological conflicts in inflorescence morphology indicate a lack of understanding of the phenotypic diversity of inflorescences. In this study, an ontogeny-based inflorescence concept is presented considering different meristem types and developmental pathways. By going back to the ontogenetic origin, diversity is reduced to a limited number of types and terms.

Methods

Species from 105 genera in 52 angiosperm families are investigated to identify their specific reproductive meristems and developmental pathways. Based on these studies, long-term experience with inflorescences and literature research, a conceptual framework for the understanding of inflorescences is presented.

Key Results

Ontogeny reveals that reproductive systems traditionally called inflorescences fall into three groups, i.e. ‘flowering shoot systems’ (FSS), ‘inflorescences’ sensu stricto and ‘floral units’ (FUs). Our concept is, first, based on the identification of reproductive meristem position and developmental potential. The FSS, defined as a seasonal growth unit, is used as a reference framework. As the FSS is a leafy shoot system bearing reproductive units, foliage and flowering sequence play an important role. Second, the identification of two different flower-producing meristems is essential. While ‘inflorescence meristems’ (IMs) share acropetal primordia production with vegetative meristems, ‘floral unit meristems’ (FUMs) resemble flower meristems in being indeterminate. IMs produce the basic inflorescence types, i.e. compound and simple racemes, panicles and botryoids. FUMs give rise to dense, often flower-like units (e.g. heads). They occur solitarily at the FSS or occupy flower positions in inflorescences, rendering the latter thyrses in the case of cymose branching.

Conclusions

The ontogenetic concept differs from all existing inflorescence concepts in being based on meristems and developmental processes. It includes clear terms and allows homology statements. Transitional forms are an explicit part of the concept, illustrating the ontogenetic potential for character transformation in evolution.     

Inflorescence structure and control of flowering time and duration by light in buckwheat (Fagopyrum esculentum Moench)

Morphogenesis of the reproductive structure of buckwheat and the impact of light conditions on flowering time and duration have been investigated using the variety 'La Harpe'. Inflorescences were initiated acropetally, in leaf axils, by the shoot apical meristem until its arrest of functioning which was accompanied by the abortion of the last inflorescence produced. The buckwheat inflorescence is a compound raceme that produces laterally flowered cymose clusters, the number of which was affected by the position of the inflorescence along the main stem. Similarly, the number of flowers in a lateral cluster was dependent on the inflorescence's position on the stem. The development of each inflorescence was stopped as its meristem stopped functioning and, in a situation reminiscent of the shoot apical meristem, the latest initiated cyme aborted. The development of each cyme was also terminated with the abortion of a few young flowers. The variety 'La Harpe' is a facultative short-day plant: the number of nodes generated before the initiation of the first inflorescence and the number of days from sowing to macroscopic appearance of this inflorescence were reduced in 8 h days as compared with 16 h days. The number of inflorescences, and thus flowering duration, was also strongly reduced by short days. It was unaffected by light irradiance in 8 h days while, in 16 h days, it was prolonged when light intensity was increased, suggesting the interaction of two different mechanisms for its regulation. Buckwheat is a distylous species, but inflorescence structure and flowering behaviour were not affected by floral morph.     

Inflorescence morphology of some South American Anacardiaceae and the possible phylogenetic trends

Barfod, A. 1988. Inflorescence morphology of some South American Anacardiaceae and the possible phylogenetic trends. - Nord. J. Bot. 8: 3–11. Copenhagen. ISSN 0107–055X.
The inflorescences of 15 native and one introduced species of South American Anacardiaceae belonging to the genera Anacardium, Loxopterygium, Mangifera, Mauria, Mosquitoxylon, Schinus, Spondias, Tapirira and Toxicodendron are described according to the terminology of Troll and coworkers. The tribal divisions in the Anacardiaceae are supported by the inflorescence morphology. Tribe Spondia-deae has paniculate inflorescences whereas tribe Anacardieae and tribe Rhoeae both have thyrsoids. Toxicodendron is exceptional for the tribe Rhoeae having axillary panicles. Thyrosids are hypothesized derived from panicles by a two step process including neoteny and enriching by cymose branching.     

Synchronization of growth, branching and flowering processes in the South American tropical tree Cecropia obtusa (Cecropiaceae)

Cecropia obtusa Trécul (Cecropiaceae) is a pioneer species associated with the initial phases of regeneration of tropical South American forests. A comparison of the succession of morphological events associated with each node (inflorescences or branches developed or aborted and underlying internode length) making up the axes of 30 trees helped to establish a link between their architecture and the regularity and synchronicity of their expression of growth, flowering, and branching processes over time on an individual and stand level. For a given individual, new nodes are emitted at the same rate on all the axes, irrespective of their branching order. Flowering and branching alternate, and these processes occur in all the axes of the tree synchronously. On a stand level, flowering and branching occur regularly every 35 nodes or so, which apparently corresponds to an annual rhythm. Under nonlimiting conditions, a single branch tier would be emitted each year, and it is thus possible to determine a posteriori the age of a crown accurately. The merits of the method, the possibility of estimating the age of natural Cecropia obtusa regrowth by observing tree architecture, and the possible applications in the field of ecology are discussed.     

Reinvestigation of Nystroemia pectiniformis Halle, an enigmatic seed plant from the Upper Permian of China

Reinvestigation of Nystroemia pectiniformis Halle from the Upper Shihhotze Formation of Shanxi Province, China, has led to the identification of new and important features of this enigmatic Late Permian seed plant, permitting its typification and diagnosis. After reassembling several of the previously studied specimens to form a single articulated branching system comprising at least four orders of branching, previously unknown features of its branching pattern and morphology have been characterized. First–order axes are wide and branch to one side only, bearing second–order branches either singly or in pairs and of two kinds: one fertile and bearing characteristic ovulate branching systems and the other presumably vegetative. Ovulate second–order axes are narrow and branch to one side only, producing numerous, closely spaced lateral branches in two alternate to sub–opposite rows. Lateral branches are slender and produce numerous ovulate branching systems to one side of the axis only. Ovulate branching systems divide unequally to produce 3–15 ultimate axes of different lengths that are planated. Each ultimate axis bears a single terminal ovule with 180 degree rotational symmetry and two horn–like integumentary projections distally. The other kind of second–order axes are distinct from those bearing ovules; they are wider and longer and branches occur on both sides of the secondary axis, lacking divisions in close proximity to the first–order axis. These have only been observed incomplete although their distinct morphology indicates they are unlikely to be ovulate branches from which ovules/seeds have been shed. Additional organs of the Nystroemia plant are considered, including pollen organs previously assigned by Halle to the same species (displaying its characteristic branching style), and also leaves of Chiropteris reniformis Halle that were probably borne on the larger kind of second–order branches. Implications of Nystroemia on seed plant evolution and distribution are discussed, and it is concluded that this most likely represents a late stratigraphic occurrence of a plesiomorphic hydrasperman–type seed plant with affinities closely allied to members of the Lyginopteridales.     

Inflorescence and floral development in Streptocarpus and Saintpaulia (Gesneriaceae) with particular reference to the impact of bracteole suppression

Floral development and inflorescence structure within Streptocarpus and Saintpaulia were investigated using Scanning Electron Microscopy (SEM). We discuss the structure and development of the pair-flowered cyme and the floral ontogeny found in the Gesneriaceae in a phylogenetic context with particular reference to an East African clade of Streptocarpus and Saintpaulia. Current phylogenetic hypotheses divide the caulescent East African Streptocarpus species into two distinct clades, in relation to which the position of Saintpaulia is not yet clear. Variation in the branching of the inflorescence showed phylogenetic significance and included dichasial, monochasial and unbranched patterns. In four of the East African Streptocarpus species sampled a single lateral bracteole was present on the first to third axes, after which the inflorescence was ebracteolate. Our results indicate that there may be some link between bracteole suppression and an alteration in the order of sepal initiation. The loss or suppression of lateral bracteoles also appears to result in the precocious development of the lateral cyme meristem.     

Ephemeral root modules in Fraxinus mandshurica

Historically, ephemeral roots have been equated with 'fine roots' (i.e. all roots of less than an arbitrary diameter, such as 2 mm), but evidence shows that 'fine roots' in woody species are complex branching systems with both rapid-cycling and slow-cycling components. A precise definition of ephemeral roots is therefore needed. Using a branch-order classification, a rhizotron method and sequential sampling of a root cohort, we tested the hypothesis that ephemeral root modules exist within the branching Fraxinus mandshurica (Manchurian ash) root system as distal nonwoody lateral branches, which show anatomical, nutritional and physiological patterns distinct from their woody mother roots. Our results showed that in F. mandshurica, distal nonwoody root branch orders die rapidly as intact lateral branches (or modules). These nonwoody branch orders exhibited highly synchronous changes in tissue nitrogen concentrations and respiration, dominated root turnover, nutrient flux and root respiration, and never underwent secondary development. The ephemeral root modules proposed here may provide a functional basis for differentiating and sampling short-lived absorptive roots in woody plants, and represent a conceptual leap over the traditional coarse-fine root dichotomies based on arbitrary size classes.     

PHILLIPOPTERIS GEN. NOV.—ANATOMICALLY PRESERVED SPORANGIAL FRUCTIFICATIONS FROM THE UPPER PENNSYLVANIAN OF THE APPALACHIAN BASIN

The discovery of a new type of sporangial fructification in coal balls from the Upper Pennsylvanian of Ohio provides the basis for describing Phillipopteris globiformis gen. et sp. nov. Sporangia are borne terminally on up to two orders of branching axes. Penultimate axes branch pinnately to produce irregularly branched ultimate axes. Sporangial wall cells are of a single type and show no specialization for dehiscence. Spores are radial and trilete, and reminiscent of the sporae dispersae genus Dictyotriletes. Phillipopteris increases our knowledge of diversity among fernlike plants from the late Paleozoic, and shares several features with Sclerocelyphus Mamay.     

外来物种黄顶菊花器官分化的初步研究

利用扫描电镜(SEM)观察了黄顶菊(Flaveria bidentis(L.)Kuntz)花序发育过程中蝎尾状聚伞花序、头状花序和小花的形成.黄顶菊的花序由主轴及一至三级分枝组成,各级分枝交互对生,形成方式相同.植株主轴和侧枝顶端的每个花序由3～6个蝎尾状聚伞花序密集而成;每一蝎尾状聚伞花序由5～15个头状花序组成;每一头状花序中有4～11枚小花.小花分化顺序为5个花冠原基、5个雄蕊原基和2个心皮原基.2007年,天津地区黄顶菊的花期是7月下旬到9月下旬.7月中旬,花序和花器官原基不断形成并分化,至花器官成熟经历的时间约15 d.     

玉兰属的研究

介绍了玉兰属Yulania Spach分类简史,分析了玉兰属与木兰属Magnolia L.的主要分类性状及其区别,阐述了药室纵裂方向、开花时期、花蕾顶生与腋生等性状的演化关系,提出玉兰属与木兰属是趋同演化的两个分类群,花先叶开放等性状是玉兰属的重要标志,中国暖温带是该属树种的起源中心、分布中心和多样性中心等新观点。确立玉兰属的系统位置,对解决现有木兰属乃至木兰科分类系统的争论具有重要的意义。     

STRUCTURALLY PRESERVED PLANTS FROM SOUTHEASTERN KENTUCKY: STAUROPTERIS BISERIATA SP. NOV.

Several axes of the coenopterid fern Stauropteris are described from permineralized peat associated with Lower-Middle Pennsylvanian coal deposits of southeastern Kentucky. This represents the first documented report of the genus in North America. The specimens are regarded as representatives of a new species—S. biseriata—based on the distinctive branching habit. Three branch orders are described, and in each case, branches are singular and distichous, arranged in a two-ranked pattern. This is in contrast to other species of Stauropteris in which the branches are paired and form a quadriseriate pattern. A pair of vascularized aphlebiae subtend each branch through all branching orders. Aphlebiae associated with first- and second-order branches are three-parted at the point of insertion; those that subtend third-order branches are singular. Stauropteris and a number of Devonian fern-like plants are compared on the basis of certain morphological similarities.     

Studies on the cupulate seed genus Hydrasperma Long from Berwickshire and East Lothian in Scotland and County Kerry in Ireland

Twelve petrified cupules containing seeds of Hydrasperma tenuis Long from the Upper-Devonian/ Lower Carboniferous Transition Series from Ballyheigue, Kerry Head, Ireland have been studied. The cupules containing 2–6 seeds are borne in pairs. Each cupule is campanulate and composed of up to 24 oval to terete units. The axis of the cupule is forked, each resultant branch dividing in an alternate monopodial fashion producing six major axes. These divide repeatedly, each terminating in a narrow rounded tip. A reconstruction of a four-seeded cupule is presented. Hydrasperma longii sp. nov. is proposed for the first 'named' Scottish cupulate seeds named by Long as Hydrasperma cf. tenuis. Hydrasperma longii differs from H. tenuis: comparison of H. tenuis with other cupulate Lower Carboniferous seeds indicates that two major branching patterns of the cupule occur in early seed plants. Following an initial dichotomy, branching may either be entirely dichotomous, or alternately monopodial. The Aneurophytales appears to have the branching patterns consistent with its position as the ancestral group.