Heteroblasty and preformation in mayapple, Podophyllum Peltatum (Berberidaceae): developmental flexibility and morphological constraint

Developmental preformation can constrain growth responses of shoots to current conditions, but there is potential for flexibility in development preceding formation of the preformed organs. Mayapple (Podophyllum peltatum) is strongly heteroblastic, producing rhizome scales, bud scales, and either a single vegetative foliage leaf or two foliage leaves on a sexual shoot. To understand how and when preformation constrains growth responses, we compare (1) how leaf homologs of the renewal shoot differ in development, (2) whether there are differences in shoot development that occur in advance of morphological determination of shoot type, and (3) whether there are points of developmental flexibility in renewal shoot growth prior to preformation of the foliage and floral organs. We use scanning electron microscopy and histology to show that the three vegetative leaves (both types of scale leaves and the vegetative foliage leaf) are similar in the initial establishment of an encircling and overarching leaf base. Differences among them are found in the timing of differentiation of the leaf base and in the relative timing and degree of growth of the lamina and petiole. In contrast, foliage leaves on sexual shoots show less expression of the leaf base and precocious growth of the lamina and petiole. Prior to shoot type determination, there are no morphological differences in the sequence or position of leaf homologs that predict final shoot type. In this colony, leaves at positions 12 and 13, on average, appear to be identical in development until they are between 700 and 800 μm in length, when it becomes possible to distinguish leaves that will become vegetative foliage leaves from additional bud scale leaves on vegetative or sexual shoots. We suggest that late developmental determination of leaves at positions 12 and 13 reflects ontogenetic sensitivity to a transition to flowering. Thus, in mayapple, heteroblasty appears to facilitate developmental flexibility prior to the point where shoot growth becomes constrained by preformation of determined aerial structures.     

HETEROPHYLLIC DEVELOPMENT IN MUEHLENBECKIA (POLYGONACEAE)

Flowering shoots of Muehlenbeckia platyclados Meisn. bear only reduced scale leaves which resemble the membranous sheath portion (ochrea) of leaves of other members of the Polygonaceae. Shoots propagated from cuttings bear enlarged foliage leaves with distinct lamina, petiole, and ochrea zones. The developmental basis for this heterophylly is explored in order to determine whether scale leaves resemble foliage leaves in their pattern of ontogeny or are developmentally unique. SEM and histological analyses have shown that scale leaves and foliage leaves are distinctive from inception. The scale leaf arises as a collarlike growth and extends over the shoot apex as a hooded sheath without evidence of blade initiation. By contrast, the first stage of foliage-leaf ontogeny is the differentiation of the distal lamina from the future leaf base. As the foliage-leaf ochrea encircles the stem axis, the lamina grows erect and projects from the abaxial surface of the sheath. Lamina reduction coupled with ochrea elaboration in intermediate leaf types indicate a homology between the entire scale leaf and foliage-leaf ochrea. Despite this homology, the production of the bladeless scale leaf does not involve a mere suppression of the foliage-leaf lamina. Erect growth of the saccate ochrea of the foliage leaf contrasts with the hooded expansion of the scale. Early histological differences, including contrasting rates of cell differentiation, also distinguish the two organs. This disparity in modes of growth and differentiation from inception results from separate, predetermined courses of ontogeny. Unlike other plants studied, leaf size and degree of leaf elaboration decrease with shoot meristem enlargement in Muehlenbeckia. Leaf packing does increase with shoot development and may contribute to variations in leaf morphology. It is concluded that the peculiarities of the heterophyllic leaf sequence in Muehlenbeckia are a property of the shoot system as a whole.     

STRUCTURAL CHANGES IN POPULUS DELTOIDES TERMINAL BUDS AND IN THE VASCULAR TRANSITION ZONE OF THE STEMS DURING DORMANCY INDUCTION

Morphological and anatomical changes in shoots of vigorously growing cottonwood plants (Populus deltoides Bartr.) were studied during dormancy induction in 8-hr short days (SD) and in control plants grown in 18-hr long days (LD). Pronounced structural changes occurred in terminal buds after 4 wk and full dormancy was achieved in 7 wk of SD. Leaf expansion ceased after 5 wk of SD as foliage leaves matured to the terminal bud base at leaf plastochron index 0 (LPI 0). Within the bud, total leaf length (lamina + petiole) decreased and stipule length increased progressively each week; thus, the ratio total leaf length/stipule length decreased rapidly, especially at the position of incipient bud-scale leaves LPI - 1 and LPI - 2. These bud-scale leaves were fully developed by wk 6 and were derived from enlarged stipules and aborted laminae. The full complement of primordia within the bud at the start of SD eventually matured as foliage leaves and the first bud-scale leaf (LPI - 1) was initiated immediately following transfer to SD. Acropetal advance of the primary-secondary vascular transition zone (TZ) was associated with leaf maturation. However, it did not advance throughout the entire vascular cylinder as in LD, but only in those leaf traces serving mature leaves beneath the terminal bud. In both LD and SD treatments the same linear relationship was maintained between LPI of the TZ and LPI of the most recently matured leaf; both parameters simultaneously increased in LD and decreased in SD. Thus, the relationship between leaf maturation and advance of the TZ was maintained irrespective of environment.     

Development of leaves and shoot apex protection in Metrodorea and related species (Rutaceae)

Most members of Sapindales are characterized by compound leaves, but several genera also (or only) produce simple or unifoliolate leaves. A few genera may bear stipules or pseudostipules. Little is known about the morphological structure and morphogenesis of these types of leaves in Sapindales, but this information is required for comparative and evolutionary studies. Metrodorea is a Neotropical genus of Rutaceae, comprising species presenting compound and unifoliolate leaves, plus heterophylly, together with an intriguing bud‐protecting structure at the leaf base. The aims of the present study are: (1) to examine leaf morphogenesis in Metrodorea and in closely related species (four Esenbeckia spp., Helietta apiculata and Raulinoa echinata); and (2) to improve our understanding of the morphological evolution of leaves in Metrodorea and Rutaceae. Our data show that the hood‐shaped structure at the base of the leaf in Metrodorea, usually interpreted as a sheath, is, in fact, a pair of united stipules, a synapomorphy of the genus. In the species studied, it is possible to recognize two main types of unifoliolate leaf: early unifoliolate leaves and late unifoliolate leaves. We also found that the number of leaflets in the studied species is dependent on the late or early determination of the leaf primordium, and that loss of leaflets may have been favoured by the restriction of space available for development within the cavity formed by the pair of united stipules. © 2015 The Linnean Society of London, Botanical Journal of the Linnean Society, 2015, 178 , 267–282.     

Stipules inRhodoleia (Hamamelidaceae)

Rhodoleia has long been believed to be the only member of theHamamelidales lacking stipules, and its systematic position has been doubtful. The present investigation shows, in contrast, thatRhodoleia championi Hook. f. produces conspicuous stipules which are, however, restricted to a few leaves of the transition region between bud scales and foliage leaves. In the foliage leaves stipules are apparently reduced, except sometimes in the outermost leaf. The presence of stipules and other correspondences clearly shows thatRhodoleia belongs to theHamamelidaceae.     

Bud Content and its Relation to Shoot Size and Structure in Nothofagus pumilio(Poepp. et Endl.) Krasser (Nothofagaceae)

Buds of shoots from the trunk, main branches, secondary branchesand short branches of 10–21 year-old Nothofagus pumiliotrees were dissected and their contents recorded. The numberof differentiated nodes in buds was compared with the numberof nodes of sibling shoots developed at equivalent positionsduring the following growing season. Axillary buds generallyhad four cataphylls, irrespective of bud position in the tree,whereas terminal buds had up to two cataphylls. There were morenodes in terminal buds, and the most distal axillary buds, oftrunk shoots than in more proximal buds of trunk shoots, andin all buds of shoots at all other positions. The highest numberof nodes in the embryonic shoot of a bud varied between 15 and20. All shoots had proximal lateral buds containing an embryonicshoot with seven nodes, four with cataphylls and three withgreen leaf primordia. The largest trunk, and main branch, shootswere made up of a preformed portion and a neoformed portion;all other shoots were entirely preformed. In N. pumilio, theacropetally-increasing size of the sibling shoots derived froma particular parent shoot resulted from differences in: (1)the number of differentiated organs in the buds; (2) the probabilityof differentiation of additional organs during sibling shootextension; (3) sibling shoot length; (4) sibling shoot diameter;and (5) the death of the apex and the most distal leaves ofeach sibling shoot. Copyright 2000 Annals of Botany Company Axis differentiation, branching, bud structure, leaf primordia, neoformation, Nothofagus pumilio, preformation, size gradient     

LEAF DIMORPHISM IN POPULUS TRICHOCARPA

Critchfield , William B. (Pacific SW Forest & Range Expt. Sta., Berkeley, Calif.) Leaf dimorphism in Populus trichocarpa. Amer. Jour. Bot. 47 (8) : 699–711. Illus. 1960.—In Populus trichocarpa and other species of Populus, each tree bears 2 kinds of leaves, referred to here as “early” and “late” leaves. Both leaf types are present on all long shoots. They differ in many features of external morphology, including petiole length, size and occurrence of marginal glands, venation, and stomatal distribution. This type of foliar dimorphism has its origins in a pronounced difference in leaf ontogeny. The early leaves originate in the developing bud and overwinter as embryonic leaves. The first late leaves are also present in the winter bud, but as arrested primordia, and succeeding late leaves are initiated at the tip of the growing shoot and develop uninterruptedly to maturity during the growing season. A similar correlation between leaf form and the circumstances of leaf ontogeny appears to be a common feature of many other instances of heterophylly. The expansion of the pre-formed early leaves is almost completed by late spring, when the first late leaves begin to grow rapidly. The formation of late leaves may then continue until late in the season. The rapid elongation of the stem does not begin until the first late leaves expand. Elongation is restricted to shoots producing late leaves. Consequently, the early leaves are confined to short shoots and the base of long shoots; adventitious shoots and the upper part of long shoots bear only late leaves. Certain other woody plants with long and short shoots also exhibit a restriction of elongation to those shoots on which a second set of leaves is produced.     

Growth correlations inBryophyllum leaves and exogenous growth regulators

Growth correlations in leaves ofBryophyllum may be recognized by the development of marginal shoots varying in their particular lamina regions, the correlative inhibition increasing from the top to the base. Cytokinins extend their promoting action inB. crenatum leaves farther in the apical than in the basal direction. In the uppermost leaves ofB. daigremontianum they evoke the development of marginal shoots with flowers in the apical and of vegetative shoots in the basal region. Less suitable for this research are auxins, gibberellins, and triiodobenzoic acid which are unable to stimulate the development of marginal shoots on leaves grown out under short days if not supplemented by cytokinins. Only TIBA induces under long days formation of adventitious shoots directly from the lamina surface on leaves developed below the terminal ring fasciation exhibiting at free ends of connate leaves normal marginal shoots. Under short days a complete reduction of lateral teeth takes place inB. verticillatum both on the extremity of ring fasciation and on the uppermost leaves, the marginal shoots being formed under the subsequent long days only in the angles between the ring fasciation parts. Furthermore the correlative inhibition of the leaf causes anisophylly in marginal shoots in the same way as that of axillaries inBryophyllum.     

Endogenous Abscisic Acid Content Correlates with Photon Fluence Rate and Induced Leaf Morphology in Hippuris vulgaris

This research focused on studying how light and endogenous abscisic acid regulate leaf development in Hippuris vulgaris, a species of heterophyllic aquatic plant. Amounts of photosynthetically active radiation greater than 300 micromoles per square meter per second caused submerged H. vulgaris shoots to produce aerial-type leaves. Abscisic acid was not detected in shoots grown under noninducing light quantities (100 micromoles per square meter per second), but was present at 13.4 nanograms per gram fresh weight in shoot tips after plants were exposed to 1 photoperiod of inducing light (500 micromoles per square meter per second). This supports a role for abscisic acid in the high light-induced heterophylly in H. vulgaris, and provides additional support for the general hypothesis that abscisic acid regulates leaf development in heterophyllic aquatic plants. No relationship was observed here between postphotoperiodic light treatments of various red/far red ratios and heterophylly in H. vulgaris.     

Structural and hydraulic correlates of heterophylly in Ginkgo biloba

This study investigates the functional significance of heterophylly in Ginkgo biloba, where leaves borne on short shoots are ontogenetically distinct from those on long shoots. Short shoots are compact, with minimal internodal elongation; their leaves are supplied with water through mature branches. Long shoots extend the canopy and have significant internodal elongation; their expanding leaves receive water from a shoot that is itself maturing. Morphology, stomatal traits, hydraulic architecture, Huber values, water transport efficiency, in situ gas exchange and laboratory-based steady-state hydraulic conductance were examined for each leaf type. Both structure and physiology differed markedly between the two leaf types. Short-shoot leaves were thinner and had higher vein density, lower stomatal pore index, smaller bundle sheath extensions and lower hydraulic conductance than long-shoot leaves. Long shoots had lower xylem area:leaf area ratios than short shoots during leaf expansion, but this ratio was reversed at shoot maturity. Long-shoot leaves had higher rates of photosynthesis, stomatal conductance and transpiration than short-shoot leaves. We propose that structural differences between the two G. biloba leaf types reflect greater hydraulic limitation of long-shoot leaves during expansion. In turn, differences in physiological performance of short- and long-shoot leaves correspond to their distinct ontogeny and architecture.     

Leaves may function as temperature sensors in the heterophylly of Rorippa aquatica (Brassicaceae)

Many plants show heterophylly, which is variation in leaf form within a plant owing to environmental change. The molecular mechanisms underlying heterophylly have recently been investigated in several plant species. However, little is known about how plants exhibiting heterophylly sense environmental cues. Here, we used Rorippa aquatica (Brassicaceae), which shows heterophylly, to investigate whether a single leaf can sense and transit changes in ambient temperature. The morphology of newly developed leaves after single-leaf warming treatment was significantly different from that of mock-treated control leaves, suggesting that leaves are sensing organs that mediate the responses to changes in ambient temperature in R. aquatica.     

HETEROPHYLLY AND NEOFORMATION OF LEAVES IN SUGAR MAPLE (ACER SACCHARUM)

Variation in leaf form and timing of leaf initiation were investigated in vigorous leader shoots of open-grown saplings and larger forest trees of sugar maple (Acer saccharum Marsh.). Winter buds of leader shoots usually contained 6 or 8 leaf primordia and embryonic leaves, whereas 12 to 18 leaves typically expanded along the shoots each year. Preformed (early) leaves differ in form from neoformed (late) leaves. As in some other Acer species, the first-formed late leaves have large angles of secondary lobe divergence and deeply indented sinuses. This pattern of heterophylly contributes to the multilayered nature of open-grown saplings and leader shoots of forest trees of sugar maple.     

LEAF TURNOVER RATES OF ADENOSTOMA FASCICULATUM (ROSACEAE)

The age structure of the foliage of a 26-yr-old stand of Adenostoma fasciculatum H. & A. (chamise) was analyzed. The mean number of standing leaves and the yearly increase in leaf scars on the leaf-producing short shoots allowed an estimate of annual leaf production. The average chamise leaf persists for two seasons. Short shoots produce 4–6 leaves per yr; however after 4–5 yr their productivity declines. About 72% of the standing leaves were produced during the current and 28% during the foregoing season. Nearly one-half of all the leaves produced was found on current-year short shoots (i.e., on long shoots that had developed during the spring of the same year). Thus, earlier estimates of leaf production in chamise based only on current-year long shoot growth were too low.     

EARLY LEAF ONTOGENY AND SHOOT DEVELOPMENT IN BROWNEA ARIZA (LEGUMINOSAE)

Brownea ariza Benth. (Leguminosae: Caesalpinioideae) shows early shoot tip abortion and subsequent renewal growth from the pseudoterminal bud. This species is unusual in that the entire shoot system is formed before flushing from the bud occurs, shoot tip abortion occurs during flushing, and the aborting portion contains three to six leaves as well as primordial structures varying from hood to peg shape. This study focused on the morphological changes from initiation of scale and foliage leaf primordia in the “resting” renewal bud through bud elongation to flushing and bud abortion. Scanning electron microscopy revealed that embryonic scale leaves are hood-shaped while foliage leaf primordia show early segmentation into leaflets and stipules. No transitional stages were observed. Bud scales and foliage leaves show opposite developmental trends. In bud scales, length at maturity increases from first to last formed, while length decreases in sequentially formed foliage leaves. Early in leaf development the stipules keep pace with the elongation of the rachis. When the bud reaches about one half of its final length the leaf rachis begins to exceed the lengths of its stipules. This young rachis terminates in a distinct mucro that persists until maturity at which time it abscises. Growth patterns indicate that mucro and rachis are a single developmental unit. The early abortion of a shoot tip containing several leaves cannot be easily rationalized. Previous suggestions have involved maintenance of form and ecological adaptation. We add the possibility of elimination of cell progeny encumbered by mutations. From this and other studies of this group, it is clear that at maturity leaves of different species may look alike, e.g., Hymenaea and Colophospermum are bifoliolate; Brownea, Saraca, and others are multifoliolate. However, early stages of leaf ontogeny are quite diverse and may be of systematic value, since these early differences are lost or masked by later development.     

Spine production is induced by fire: a natural experiment with three Berberis species

Earlier studies indicate that some plant species allocate more mass to produce longer spines in shoots resprouting after browsing. Here we present, for the first time, evidence that fire induces a similar response. Many terrestrial herbivores may benefit from fire through the enhanced availability of fast growing species colonizing or re-sprouting in burned areas. It is less clear whether post-fire plant growth responds to the enhanced risk of herbivory by an increased investment in defensive traits. In this study, we tested whether the production of spines is influenced by the set of environmental conditions that result from fire events. We compared the resource allocation pattern of resprouting shoots from three Berberis species growing in two areas that burned 1999 with samples collected from unburned areas within the same plant communities. We divided the shoot into three main components: supporting tissue (twigs), assimilating tissue (leaves) and defensive structures (spines). We found that plants resprouting after fire allocated more mass to spines and leaves but not twigs. This resulted in a higher density of both spines and leaves. Spines were significantly longer in plants resprouting after fire. Leaves were shorter at the apical end of the shoot, but did not show any significant change in size following fire. We suggest that this type of post-fire response may be a general adaptation to pruning and leaf picking by browsing herbivores in arid and semi-arid regions. Changes in the browsing pressure following fire will determine the fitness value of this response.     

Leaf Production and Morphology in the Artichoke Gall of Yew (Taxus baccata L.)

Comparative leaf production rates and leaf morphology studiesfor galled and normal shoots of yew trees have been obtainedthroughout the life cycle of the causative agent, the gall midge,Taxomyia taxi. Normal and galled shoot leaf numbers have beenrelated to those of their parent shoots. It was found that whereasthe annual leaf production of normal shoots was positively relatedto that of the parent shoots, galled shoot leaf production remainedconstant regardless of parent shoot vigour showing leaf stimulationby the midge to be a special case. The midge larva appears tobe determining the rate of leaf production in galled shoots.In galls leaf production continues throughout the winter monthswith no dormant period. From morphological evidence, alternationof leaves and cataphylls is continued in galled buds.     

Heteroblasty in Arabidopsis thaliana (L.) Heynh

 Heteroblasty in Arabidopsis thaliana was analyzed in a variety of plants with mutations in leaf morphology using a tissue-specific β-glucuronidase gene marker. Some mutants exhibited their mutant phenotypes specifically in foliage leaves. The phenotypes associated with the foliage-leaf-specific mutations were also found to be induced ectopically in cotyledons in the presence of the lec1 mutation. Moreover, the features of an emf1lec1 double mutant showed that cotyledons can be partially converted into carpelloids. When heteroblastic traits were examined in foliage leaves in the presence of certain mutations or natural deviations by histochemical analysis of the expression of the tissue-specific marker gene, it was found that ectopic expression of the developmental program for the first foliage leaves in lec1 cotyledons seemed to affect the heteroblastic features of the first set of foliage leaves, while foliage leaves beyond the third position appeared normal. Similarly, in wild-type plants, discrepancies in heteroblastic features, relative to standard features, of foliage leaves at early positions seemed to be eliminated in foliage leaves at later positions. These results suggest that heteroblasty in foliage leaves might be affected in part by the heteroblastic stage of the preceding foliage leaves but is finally controlled autonomously at each leaf position. Received: 9 July 1999 / Accepted: 17 August 1999     

Phyllotaxis, phenology and architecture in Cephalotaxus, Torreya and c(Coniferales)

In Amentotaxus, Cephalotaxus and Torreya there is a regular seasonal alternation of foliage leaves and bud-scales, with foliage leaves largely preformed, i.e. initiated in the season before they expand. On most plagiotropic shoots phyllotaxis in the production of foliage leaves may be either bijugate ( Cephulotaxus, Torreya ) or decussate ( Amentotaxus ). In bijugate phyllotaxis successive leaf pairs originate at an angle of about 68° to each other, i.e. approximately one-half of the 'ideal' or Fibonacci angle of 137.5°. Secondary leaf orientation in Cephulotaxus and Torreya , by twisting of the leaf base, produces the dorsiventrality of plagiotropic shoots, whereas in Amentotaxus secondary orientation involves a twisting of the stemc as well as the leaf base. In Cephalotaxus cc condition is constant in the production of the numerous but imprecise number of bud-scales and in the production of foliage leaves. However, in Torreya the phyllotaxis changes from bijugate in the production of foliage leaves to decussate in the production of bud-scales, which are constant in number (about eight pairs). This allows a precise analysis of the biphasic production of leaf primordia in the seasonal cycle. The phyllotactic change in Torreya may not be the result of reported changes in shoot apex dimensions since Cephalotaxus , with its constant phyllotaxis, has a comparable seasonal change in apex dimensions. Information on architecture, chirality and cone morphology is also included.     

Integrative regulation of leaf morphogenesis by gibberellic and abscisic acids in the aquatic angiosperm proserpinaca palustris L

A two-hormone system regulating leaf development in the heterophyllous amphibious angiosperm Proserpinaca palustris L. is described. Aerial shoots develop expanded, lanceolate, serrate leaves under long-day photoperiods (LD, 16 h light: 8 h dark), whereas growth under short days (SD, 10 h light: 14 h dark) induces dissected leaf formation. The photoperiodic effect on leaf development of aerial shoots involves changes in endogenous gibberellins (GAs) since plants grown under SD in the presence of GA₃ develop expanded lanceolate serrate leaves. However, when submerged, shoots develop highly dissectedaquatic leaves regardless of photoperiod or GA₃ treatment. In the present study, submerged plants exposed to 1.0 or 5.0 μM abscisic acid (ABA) developed aerial-type leaves typical of the photoperiod under which they were cultured. Both exogenous ABA (5.0 μM) and GA₃ (10 μM) treatments were required for laminar expansion to occur on submerged shoots under SD. It is suggested that (1) leaf development in Proserpinaca is regulated by both endogenous GAs and ABA, and (2) the endogenous status of these phytohormones is modulated by different environmental stimuli of photoperiod and water stress, respectively. The adaptive significance of this mechanism is discussed.     

New Sphenophyllum plant from the Upper Devonian of Zhejiang Province,China

Sphenophyllum was an important and long-surviving sphenopsid genus in the Paleozoic floras, with a worldwide distribution. A new species, Sphenophyllum changxingense sp. nov., is described from the Upper Devonian Wutong Formation of Changxing County, Zhejiang Province, China. This plant is characterized by two orders of slender axes and wedge-shaped leaves borne in whorls. The axes bear short spines and show longitudinal ridges and furrows on surface. Three to eight isophyllous leaves, with one, two, or no second-order axes, are attached at each node of first-order axes. Leaves bear spines and show a bilobate morphology; the two leaf lobes divide distally to form several marginal segments, each segment with a leaf vein. Sphenophyllum changxingense represents an early and primitive species within the genus, in light of the absence of heterophylly and specialized hook-like leaves. Like some Carboniferous and Permian species, it appears to have formed dense mats with mutually supportive axes. This plant adds to the known diversity of early sphenopsids in the Late Devonian.