Floral development and evolution of capitulum structure in Anacyclus (Anthemideae, Asteraceae)

Abstract

Background and aims: Most of the diversity in the pseudanthia of Asteraceae is based on the differential symmetry and sexuality of its flowers. In Anacyclus, where there are (1) homogamous capitula, with bisexual, mainly actinomorphic and pentamerous flowers; and (2) heterogamous capitula, with peripheral zygomorphic, trimerous and long-/short-rayed female flowers, the floral ontogeny was investigated to infer their origin.

Methods: Floral morphology and ontogeny were studied using scanning electron microscope and light microscope techniques.

Key results: Disc flowers, subtended by paleae, initiate acropetally. Perianth and androecium initiation is unidirectional/simultaneous. Late zygomorphy occurs by enlargement of the adaxial perianth lobes. In contrast, ray flowers, subtended by involucral bracts, initiate after the proximal disc buds, breaking the inflorescence acropetal pattern. Early zygomorphy is manifested through the fusion of the lateral and abaxial perianth lobes and the arrest of the adaxials. We report atypical phenotypes with peripheral 'trumpet' flowers from natural populations. The peripheral 'trumpet' buds initiate after disc flowers, but maintain an actinomorphic perianth. All phenotypes are compared and interpreted in the context of alternative scenarios for the origin of the capitulum and the perianth identity.

Conclusions: Homogamous inflorescences display a uniform floral morphology and development, whereas the peripheral buds in heterogamous capitula display remarkable plasticity. Disc and ray flowers follow different floral developmental pathways. Peripheral zygomorphic flowers initiate after the proximal actinomorphic disc flowers, behaving as lateral independent units of the pseudanthial disc from inception. The perianth and the androecium are the most variable whorls across the different types of flowers, but their changes are not correlated. Lack of homology between hypanthial appendages and a calyx, and the perianth double-sided structure are discussed for Anacyclus together with potential causes of its ray flower plasticity.

Keywords: Anacyclus; Compositae; capitulum; disc flowers; evo-devo; inflorescence; pseudanthium; ray flowers.

Fig. 1.

Inflorescences of Anacyclus. Anacyclus homogamos (A, B); A. monanthos (C); A. clavatus (D); A. pyrethrum (E); A. alboranensis (F); A. valentinus (G, H, J); A. clavatus ‘trumpet’ (I). (A) Capitula. (B, C) Homogamous capitula. (D, E) Heterogamous capitula with peripheral ray flowers in anthesis. (F, G) Heterogamous capitula with reduced ray flowers giving a discoid aspect to the inflorescence. (H) Heterogamous capitulum with reduced and scarce ray flowers in anthesis. (I) Heterogamous capitulum with peripheral flowers with a ‘trumpet’ perianth. Taken from a field population of A. clavatus. (J) Heterogamous capitulum with peripheral flowers with a ‘trumpet’ perianth. Taken from a field population of A. valentinus. Scale bars: (A, D, E) = 5 mm; (B) = 1·6 mm; (C) = 2 mm; (F) = 1 cm; (G, H–J) = 2·5 cm.

Fig. 2.

Schematic drawing of the peripheral (A–F) and disc flowers (G). (A–C) Peripheral flowers found in A. valentinus, with relatively narrow (A), short (B) or null (C) perianth lamina. (D) Typical long and wide ray flower observed in heterogamous species such as A. clavatus. (E, F) ‘Trumpet’ flowers present in wild populations of A. clavatus (E) and A. valentinus (F). (G) Disc flower. The structure surrounding the ovaries corresponds to the wings, flat prolongations of the ovary wall.

Fig. 3.

SEM microphotographs. Adult floral tissues and organs of Anacyclus. Anacyclus homogamos (A, B, O, P), A. monanthos (C, F, G, L, M, N), A. valentinus (D, E, I), A. clavatus (H), A. clavatus ‘trumpet’ (J, Q), A. valentinus ‘trumpet’ (K). (A) Side view of the involucre. (B) Front view of disc flowers with subtending paleae. (C) Front view of the perianth hairs in disc flowers. (D) Side view of a lateral perianth lobe of a disc flower. Upper epidermal surface upwards. (E) Top view of the papillose cells on the upper epidermal surface of a disc flower perianth lobe. (F) Side view of the adaxial flank of a disc flower. The adaxial perianth lobes (pointing upwards) are taller than the other lobes. (G) Detail of the surface of an adaxial perianth lobe. (H) Front view of a ray flower with bifid style. (I) Side view of the lower (downwards) and upper perianth surface (upwards) of a ray flower. (J) Side view of a capitulum with ‘trumpet’ flowers sliced to expose the radial plane. Only disc flowers are detailed. (K) Side view of disc flowers present in a capitulum with ‘trumpet’ flowers prior to anthesis. (L) Side view of filaments and the proximal part of the anthers in a disc flower. The thick area of the filament closer to the anther is the collar. (M) Side view of a disc flower (removed perianth marked with an asterisk) displaying the stylopodium (nectary) ring surrounding the proximal part of the style. The irregular extensions of the ovary wall correspond to myxogenic cells. (N) Detail of a myxogenic cell from M. (O) Front view of a style branch from a disc flower touching the anthers. (P) Side view of a bifid style and its stigmatic lined surfaces, from a disc flower. (Q) Trifid style from a peripheral ‘trumpet’ flower. Abbreviations: a, anther; df, disc flower; f, filament; i, involucral bract; n, nectary; o, ovary; p, perianth; pa, palea; st, style; stg, stigmatic tissue. Scale bars: (A, B, H, J, K) = 0·2 mm; (C, N) = 10 µm; (D, F) = 40 µm; (E, G) = 6 µm; (I, O) = 20 µm; (L, M) = 100 µm; (P, Q) = 60 µm.

Fig. 4.

Pseudanthia with unusual phenotypes taken from natural populations of Anacyclus clavatus. (A) Individual with both homogamous and heterogamous capitula. (B) Capitulum with peripheral flowers with an intermediate morphology between a ‘trumpet’ and a ray flower perianth. (C) Capitulum with a unique ray flower (indicated by a black arrowhead) in the middle of the disc flowers. (D) Capitula with several ray flowers towards the periphery of the disc flower area. Scale bars: (A) = 15 mm; (B) = 5 mm; (C) = 7·5 mm; (D) = 6·5 mm.

Fig. 5.

Diagrams and formulas representing the floral morphologies in Anacyclus (for formula symbols, see Prenner et al., 2010). (A) Bisexual disc flower, present in all species. The black structure below the flower corresponds to the subtending palea. (B–D) Different types of peripheral flowers. (B) Female ray flower without adaxial perianth lobes. (C, D) Peripheral flowers with ‘trumpet’ perianths. (C) Bisexual peripheral ‘trumpet’ flower with almost equal perianth lobes. Present in populations of A. valentinus. (D) Female peripheral ‘trumpet’ flower with equal perianth lobes. Present in populations of A. clavatus. Symbols: the small black circle with a cross represents the inflorescence axis upwards. A dashed circle around the flower diagram in (A), (C) and (D) represents the gynoecial hypanthium. The ‘crest-like’ structure drawn at the adaxial side of these ovaries corresponds to the corona, which is an extension of the gynoecial hypanthium. Perianth lobes are white. Dashed lines represent the androecium and corolla adnation. Androecium in (A) and (C) displays grey lines between stamens, representing the post-genital stamen connation. Asterisks represent aborted stamens. A grey ring symbolizes the stylopodium. A central circle represents the gynoecium with two carpels: one adaxial with the basal seed (black dot) and the other abaxial reduced, representing a pseudomonomerous condition. Abbreviations: A, androecium; Ĝ, inferior ovary; P, perianth; r, reduced; Vb, basal ovule. Numbers indicate the number of organs per whorl. The superscript zero (‘0’) in (B) and (C) indicates that the stamens are lost in adult flowers. Symbols: ↓, zygomorphic whorl; *, actinomorphic whorl; ♀_plus, female flower' _{[ ]}, proximal fusion between organs of different whorls; (), connate organs; ⁽⁾, distal fusion of organs of the same whorl; _o, nectarial gland (stylopodium) surrounding the base of the style.

Fig. 6.

LM microphotographs. Floral anatomy of Anacyclus. Anacyclus clavatus (A–D, F, H, I, K); A. valentinus (G); and A. homogamos (E, J). (A) Transversal section of the penduncle. Asterisks indicate stomatic chambers. Arrowheads point to secretory ducts. (B) Detail of a capitate hair at the peduncle epidermis. (C) Longitudinal section of a young capitulum. The arrowhead points to one of the serial secretory ducts along the inflorescence below the floral buds. (D) Transversal section of two involucral bracts. (E) Transversal section of a mature involucral bract with a thick fibre layer. (F) Longitudinal section of a disc flower. (G) Transversal section of a disc flower at the level of the nectary (stylopodium) near the proximal part of the perianth. (H) Transversal section of a disc flower at the anther level. (I) Transversal section of a disc flower bud at the level of the union of perianth lobes. The lobes interlock their papillate surfaces to seal the top of the perianth. (J) Transversal section of a disc flower with a central style and five surrounding filaments. (K) Detail of the anther anatomy in transverse section. (L) Longitudinal section of two mature anthers full of pollen and the two style branches. The uniserial rows of red cells correspond to the stigmatic area of each branch. Abbreviations: a, anther; co, connective; df, disc flower; e, epidermis; en, endothecium; f, filament; m, middle layers; n, nectary; o, ovule; ov, ovary; p, perianth; pa, palea; r, receptacle; sp, sporangium; st, style; stg, stigmatic tissue; t, tapetum. Scale bars: (A, F) = 50 µm; (B, D, K, L) = 20 µm; (C, G) = 30 µm; (E) = 10 µm; (F) = 50 µm; (H) = 0·2 mm; (I) = 25 µm; (J) = 75 µm.

Fig. 7.

LM microphotographs. Floral transversal sections of Anacyclus. Anacyclus valentinus (A, B); and A. clavatus (C–O). (A–F) Disc and (G–L) ray flower tissues. (A) Hair at the ovary wall. (B) Ovary wall, with three myxogenic cells at the external epidermis. (C) Ovary of a disc flower with a young embryo. (D) Style at the level below the anthers with two main vascular bundles from each carpel. (E) Detail of (D), with the vascular bundles separated by the pollen transmitting tissue. (F) Style branch with the stigmatic areas towards the side. (G) Proximal part of the perianth. At the abaxial side (at the bottom) is a rib of the lamina filled by several layers of collenchyma. The upper half possesses parenchyma and is limited by a papillate epidermis. (H) Detail of the collenchymatic tissue with chloroplasts. (I) Distal portion of the perianth without traces of collenchyma. The lower epidermal surface is on the right and the upper epidermal surface is on the left. (J) Distal section of the ovary. The ovule tissue is at the centre. (K) Ovary wall with a layer of crystals parallel to the inner ovary epidermis. (L) Ovary wall with the inner ovary epidermis interspersed by small groups of cells similar to vascular bundles (asterisk). Abbreviations: c, collenchyma; e, epidermis; eb, embryo; ec, endocarp; io, inner ovary wall; mx, myxogenic cells; o, ovule; ow, outer ovary wall; pe, pericarp; pq, parenchyma; stg, stigmatic tissue; tt, transmitting pollen tissue. Scale bars: (A, D, F, K) = 25 µm; (B, I, J) = 50 µm; (C) = 0·1 mm; (E, L) = 12·5 µm; (G) = 80 µm; (H) = 35 µm.

Fig. 8.

SEM microphotographs. Inflorescence (A–D) and disc flower (E–P) development in Anacyclus. Anacyclus homogamos (A, B, D, I, P), A. clavatus (C, F, M, N), A. alboranensis (E), A. valentinus (G, J), A. monanthos (H, K, L) and A. pyrethrum (O). (A) Front view of a young reproductive branch. (B) Side view of a young capitulum with involucral bracts initiating helically. Disc flowers buds initiate at the proximal part. (C) Side view of a young heterogamous capitulum with developing parastichies. White arrowheads point to delayed floral meristems of ray flowers. (D) Side view of a homogamous inflorescence. Involucral bract partially removed without the opposite floral bud (black arrowhead). Surrounding disc floral buds are subtended by paleae. (E) Side view of the abaxial flank of developing disc flowers. Black diamonds point to the paleae emerging from a common meristem shared with the floral bud. The inflorescence axis is upwards. (F) Top view of a capitulum. The white asterisk points to the inflorescence meristem. (G) Side view of a developing inflorescence with flat receptacle; pre-anthetic proximal disc flowers flank the undeveloped central buds. The black arrowhead points to a disc flower with subtending paleae. (H) Disc flower bud before organ initiation. (I) Top view of a floral bud with incipient perianth primordia. The adaxial and lateral primordia initiate first, then the abaxial one (adaxial side upwards). (J) Side view of floral buds during stamen primordia initiation (adaxial side upwards). Black dots point to stamen primordia. (K) Top view of valvate perianth of a disc flower. The perianth lobes are thick with a papillose upper surface. Their lower epidermal surface possesses flat cells. (L) Side view of the adaxial flank of a developing disc flower. The two adaxial perianth lobes become taller in comparison with the rest of the lobes. Top of the bud populated by rounded cells and perianth hairs (white arrow). (M) Front view of a radial section of a young inflorescence with developing disc floral buds. Flowers show an actinomorphic perianth, without enlargement of the adaxial perianth lobes. White arrowheads indicate apical ovary appendages. Black arrows point to individual pedicels. (N) Front view of the adaxial side of a disc flower at mid development. Perianth hairs are conspicuous. (O) Elongated disc flowers with delayed adaxial perianth lobe enlargement. (P) Elongation of the adaxial perianth lobes following an acropetal direction. Abbreviations: cl, compound leaves; i, involucral bract; o, ovary; p, perianth; pa, palea. Scale bars: (A, E) = 20 µm; (B, C, N) = 40 µm; (D, M) = 100 µm; (F) = 90 µm; (G) = 0·2 µm; H–K) = 10 µm; (L)= 30 µm; (O, P) = 0·2 mm.

Fig. 9.

SEM microphotographs. Development of heterogamous inflorescences with ray (A–J) and ‘trumpet’ flowers (K–O). Anacyclus clavatus (A, D, E, G, I), A. pyrethrum (B), A. valentinus (C, J), A. radiatus (F), A. valentinus with ‘trumpet’ flowers (K, L, N, O) and A. clavatus with ‘trumpet’ flowers (M). (A) Side view of a young heterogamous capitulum with disc floral buds (white arrowheads) initiating and alternating with young involucral bracts; note the absence of a ray floral bud at this stage. (B) Side view of a heterogamous inflorescence with parastichies initiated by disc flower buds (white arrowsheads). (C) Top/side view of a heterogamous capitulum with young ray flower buds (white arrowhead) and differentiation of a disc floral bud/palea (black diamond). (D) Top view of a ray flower bud with the congenitally united perianth, with the adaxial side repressed and an enlarging abaxial side with a stamen remnant (white arrowhead). (E) Side view of the periphery of a heterogamous capitulum with two ray floral buds: one subtended by an involucral bract (centre, downwards), and the other (at the right) with a congenitally fused perianth. They are surrounded by disc flowers. (F) Top view of a ray flower bud with two carpel primordia. The black asterisk points to a stamen primordium. (G) Side view of a ray floral bud with fused lateral and abaxial perianth lobes. The adaxial perianth side remains repressed (white arrowhead). (H) Side view of the periphery of a heterogamous capitulum with two ray floral buds separated by a disc flower. Note the three fused perianth lobes of the ray flowers and the pentamery of the disc flower with conspicuous adaxial perianth lobes (adaxial side upwards). (I) Side view of the adaxial flank of a ray flower with the perianth rolled and covered by hairs. (J) Side view of a developing ray floral bud displaying enlarging style branches. (K) Side view of a heterogamous capitula with a peripheral ‘trumpet’ flower bud (black arrow) delayed in comparison with the surrounding disc flowers. Disc flowers have differentiated subtending paleae (black diamonds). (L) Detail of the ‘trumpet’ floral bud (black arrowhead) and disc floral buds with their paleae (black diamonds) shown in (F). (M) Side view of a heterogamous capitula with peripheral ‘trumpet’ flowers (white arrowheads). (N) Front view of a tetramerous ‘trumpet’ flower and two pentamerous disc flowers. (O) Side view of a heterogamous capitulum with ‘trumpet’ flowers (white arrowheads). Abbreviations: cl, compound leaf; df, disc flower; g, gynoecium; i, involucral bract; o, ovary; p, perianth; st, style. Scale bars: (A, B, E, L, N) = 20 µm; (D, G) = 10 µm; (F) = 6 µm; (I, K, M) = 60 µm; (C, H, J) = 40 µm; (O) = 0·2 mm.