Angiosperm ovules: diversity, development, evolution

Abstract

Background: Ovules as developmental precursors of seeds are organs of central importance in angiosperm flowers and can be traced back in evolution to the earliest seed plants. Angiosperm ovules are diverse in their position in the ovary, nucellus thickness, number and thickness of integuments, degree and direction of curvature, and histological differentiations. There is a large body of literature on this diversity, and various views on its evolution have been proposed over the course of time. Most recently evo-devo studies have been concentrated on molecular developmental genetics in ovules of model plants.

Scope: The present review provides a synthetic treatment of several aspects of the sporophytic part of ovule diversity, development and evolution, based on extensive research on the vast original literature and on experience from my own comparative studies in a broad range of angiosperm clades.

Conclusions: In angiosperms the presence of an outer integument appears to be instrumental for ovule curvature, as indicated from studies on ovule diversity through the major clades of angiosperms, molecular developmental genetics in model species, abnormal ovules in a broad range of angiosperms, and comparison with gymnosperms with curved ovules. Lobation of integuments is not an atavism indicating evolution from telomes, but simply a morphogenetic constraint from the necessity of closure of the micropyle. Ovule shape is partly dependent on locule architecture, which is especially indicated by the occurrence of orthotropous ovules. Some ovule features are even more conservative than earlier assumed and thus of special interest in angiosperm macrosystematics.

Fig. 1.

Anatropous ovules in Tasmannia piperita (Winteraceae). SEM micrographs. (A) Young ovules in one series on a placenta, showing the nucellar apex and initiation of the inner integument (arrow). (B) Ovule before anthesis, antiraphal side, micropyle curved toward the pollen tube transmitting tissue on the placenta, inner integument lobed (arrow). (C) Ovules at anthesis, in two series, curved away from each other, micropylar area partly covered with secretion from micropyle. (D) Three ovules at anthesis, seen from raphal side, the funiculus surrounded by papillate pollen tube transmitting tissue (arrow). Scale bars: (A, B, C) = 0·1 mm; (D) = 0·3 mm.

Fig. 2.

Development of an anatropous bitegmic angiosperm ovule. Median longitudinal sections (schematized and augmented from Bouman, 1984a). (A–E) Straight thin line drawn through the middle of the nucellus. Arrowhead indicating successive ovule curvature from 0 to 180 °. (E, E′) Two possible ways of designation of sides of a mature ovule are shown with colours. In (E′) the thin line is not straight but follows the curvature of the ovule. (A) Ovule before integument initiation. (B) Ovule at initiation of inner integument. (C) Slightly older ovule. (D) Ovule with both integuments formed. (E) Mature ovule. Raphal side blue, antiraphal side red. (E′) Mature ovule. Concave side blue, convex side red.

Fig. 3.

Diversity in ovule curvature. Median longitudinal microtome sections. (A) Orthotropous ovule (Barclaya rotundifolia). (B) Anatropous ovule (Asimina triloba). (C) Campylotropous ovule (Hypecoum pendulum). In the zig-zag micropyle (C) the part formed by the outer integument is marked with a green arrow, the part formed by the inner integument with a red arrow. Scale bars: (A) = 0·2 mm; (B, C) = 0·1 mm.

Fig. 4.

Abnormal orthotropous ovules on a multiovulate placenta (asterisks). (A) Takhtajania perrieri. (B) Butomus umbellatus. (C) Podophyllum emodi. Abnormal hemitropous ovule with short outer integument marked with an arrow. Scale bars: (A) = 0·15 mm; (B) = 0·1 mm; (C) = 0·5 mm.

Fig. 5.

Orthotropous ovules and ovary locule architecture (arrows point to micropyles). (A) Houttuynia cordata. (B) Xiphidium coeruleum. (C) Akebia quinata (with secretory hairs and secretions between the ovules). Scale bars: (A) = 0·2 mm; (B) = 0·3 mm; (C) = 0·1 mm.

Fig. 6.

Orthotropous ovules and conditions of ovary locule architectures under which they occur (schematic, only one integument is drawn in each ovule for simplicity; augmented and modified from Endress, 1994a). (A–C) Ovary or locules not filled with secretion. (A) Single ovule with basal placenta (LS gynoecium) (e.g. Piperaceae, Juglandaceae, Urticaceae). (B) Ovules on parietal placentae with the micropyle directed toward another placenta (TS ovary) (e.g. Casearia, Salicaceae; Mayaca, Mayacaceae). (C) Ovules with long funiculi curved to their own placenta (LS gynoecium) (e.g. Helianthemum, Cistaceae). (D–F) Ovary or locules filled with secretion (secretion shaded blue). (D) Basal diffuse placenta (LS gynoecium) (e.g. Pistia, Araceae). (E) Laminar-diffuse placenta (TS carpel/ovary) (e.g. Barclaya, Nymphaeaceae; Hydrocharis, Hydrocharitaceae; Akebia, Lardizabalaceae, shown, in the latter ovules slightly curved at anthesis). (F) Axile placenta (TS ovary) (e.g. Acorus, Acoraceae; Xiphidium, Haemodoraceae).

Fig. 7.

Different patterns of contact between the ovule and pollen tube transmitting tissue of the stylar canal in gynoecia with a single orthotropous ovule on a basal placenta (schematic, only one integument drawn in each ovule for simplicity). (A) Integument(s) protruding into the stylar canal (i, e.g. Didymeles, Didymelaceae, schematized after von Balthazar et al., 2003; Elatostema, Urticaceae, schematized after Fagerlind, 1944). (B) Nucellus (nucellar beak, n) protruding into the stylar canal (e.g. Polygonum, Polygonaceae, schematized after Edman, 1929). (C) Carpel forming an obturator (o, e.g. Elatostema, Urticaceae, schematized after Fagerlind, 1944).

Fig. 8.

Different orientations of curved ovules with respect to carpel curvature (denoted by a red line). (A) Syntropous. Curvature of the ovule in the same direction as the curvature of the carpel. (B) Antitropous. Curvature of the ovule in the opposite direction to that of the carpel.

Fig. 9.

Gradients in ovule development on multiovulate placentae. (A–C) Acropetal and basipetal development of ovules on the placenta (and reduction of last formed ovules in some cases). (A) Basipetal. Solanum sisymbrifolium. (B) Acropetal, upper ovules reduced. Liquidambar orientalis. (C) Acropetal, upper ovules greatly reduced. Corylopsis willmottiae. (D–F) Peripheral delay in development. (D) Passiflora holosericea. After ovule initiation. (E) Passiflora holosericea. After integument initiation. (F) Nymphaea tetragona. Scale bars: (A, D, E) = 0·05 mm; (B, F) = 0·2 mm; (C) = 0·1 mm.

Fig. 10.

Diversity of nucellus thickness and integument number and thickness (thick lines, morphological surfaces; thin lines, boundaries between cell layers; epidermal layer drawn in full, other layers only partially drawn; modified from Endress, 2011). (A–F) Different nucellus shapes. Meiocytes are shaded grey. (A) Crassinucellar. (B) Weakly crassinucellar. (C) Pseudocrassinucellar. (D) Incompletely tenuinucellar. (E) Tenuinucellar. (F) Reduced tenuinucellar. (G–K) Different integument differentiation. In bitegmic ovules, the inner integument is shaded red, the outer blue. (G) The outer integument is thicker than the inner. (H) The inner integument is thicker than the outer. (I) Both integuments are equally thick. (J) Unitegmic. (K) Ategmic.

Fig. 11.

Two possibilities for morphological closure of a tubular structure through differential directional growth: irregular thickening or lobation. (A, B) End of a tube seen from above. (A) Tube open. (B) Tube partially closed by irregular thickening (arrows). (C, D) End of the tube seen from the side. (C) Tube open. (D) Tube partially closed by lobe formation (arrows). (E) Micropyle with lobed inner (i) and outer (o) integuments. Illicium floridanum (from Igersheim and Endress, 1997, Fig. 75). Scale bar: (E) = 0·1 mm.