Female germ unit in Genlisea and Utricularia, with remarks about the evolution of the extra-ovular female gametophyte in members of Lentibulariaceae

Abstract

Lentibulariaceae is the largest family among carnivorous plants which displays not only an unusual morphology and anatomy but also the special evolution of its embryological characteristics. It has previously been reported by authors that Utricularia species lack a filiform apparatus in the synergids. The main purposes of this study were to determine whether a filiform apparatus occurs in the synergids of Utricularia and its sister genus Genlisea, and to compare the female germ unit in these genera. The present studies clearly show that synergids in both genera possess a filiform apparatus; however, it seems that Utricularia quelchii synergids have a simpler structure compared to Genlisea aurea and other typical angiosperms. The synergids are located at the terminal position in the embryo sacs of Pinguicula, Genlisea and were probably also located in that position in common Utricularia ancestor. This ancestral characteristic still occurs in some species from the Bivalvaria subgenus. An embryo sac, which grows out beyond the limit of the integument and has contact with nutritive tissue, appeared independently in different Utricularia lineages and as a consequence of this, the egg apparatus changes position from apical to lateral.

Fig. 1

Ultrastructure of the ovule and embryo sac of G. aurea. a Sections through the micropylar canal and the micropylar part of synergids, In integument, MC micropylar canal, sy synergid, bar = 1.2 μm. b Sections through the micropylar and the central parts of the synergids, Fa filiform apparatus, N nucleus, bar = 1.6 μm. c Chalazal parts of the synergids, V vacuole, Int thick-walled integument cells, bar = 2 μm. d A part of a filiform apparatus, arrow microtubules, bar = 0.45 μm. e Synergid cytoplasm with dictyosomes (d), bar = 0.6 μm. f middle part of a synergid, the wall between the central cell and the synergid, circle plasmodesmata, sy synergid, Cc central cell, wl wall packet, bar = 0.4 μm. g Chalazal parts of the synergid, sy synergid, eg egg cell, bar = 1.2 μm

Fig. 2

Anatomy and ultrastructure embryo sac of a G. aurea. a Egg apparatus after PAS reaction, note PAS-positive wall on the chalazal part of the egg cell (white arrow) and synergid (black arrow), bar = 4 μm; b egg apparatus Fa filiform apparatus, sy synergid, eg egg cell, red arrows attachment of egg wall to the wall of the embryo sac, Cc central cell, bar = 1.7 μm; c wall between the central cell and the egg cell, circle plasmodesmata, eg egg cell, bar = 0.4 μm; d the micropylar part of egg cell, eg egg cell, Cc central cell, bar = 1 μm

Fig. 3

Ultrastructure of a G. aurea egg cell and central cell. a Micropylar part of egg cell, Egn egg nucleus, m mitochondrion, d dictyosome, P plastid, bar = 0.9 μm; b the part of egg cytoplasm with mitochondria and microtubules (red arrows), bar = 0.3 μm; c the part of the central cell with polar nuclei (Pn), eg egg cell, bar = 1,4 μm; d the part of central cell cytoplasm with active dictyosomes (d), v vacuole, bar = 0,7 μm

Fig. 4

Ultrastructure of a G. aurea embryo sac. a Egg cell (eg) central cell with secondary nucleus (N), bar = 1.8 μm. b The part of central cell cytoplasm with secondary nucleus, plastids (P), mitochondria (m), dictyosomes (d), bar = 0.9 μm. c The part of the central cell cytoplasm with numerous cortical microtubules (red arrows), bar = 0.2 μm

Fig. 5

Anatomy of the ovule and embryo sac of U. quelchii. a Sections through placenta with ovule; P placenta, Nt nutritive tissue, In integument, sy synergid, eg egg cell, Cc central cell, bar = 12 μm. b Sections through thick-walled nutritive tissue (Nt) and the extra-ovular part of the central cell (Cc), bar = 3 μm. c The part of the extra-ovular central cell cytoplasm; m mitochondrion, L lipid body, d dictyosome, P placental cell, red arrows microtubules, bar = 0.7 μm. d The micropylar part of the embryo sac; In integument, sy synergid, Cc central cell, Fa filiform apparatus, W secretion, framed part shown in Fig. e, bar = 2 μm. e Extra-ovular “naked” part of the central cell; mv multivesicular body, P placenta, bar = 0.6 μm

Fig. 6

Anatomy of the ovule and embryo sac of U. quelchii. a Section through the part of placenta with the ovule in the horizontal plane, arrows indicate parts of the central cell which grows into the ovary chamber; Nt nutritive tissue, In integument, Sy synergid, Fa filiform apparatus, eg egg cell, Cc central cell, bar = 6 μm. b The micropylar part of the synergid; Sy synergid, Cc central cell, m mitochondrion, L lipid body, d dictyosome, Fa filiform apparatus, bar = 0.9 μm. c The chalazal part of the synergid; arrows depict the narrow zone between the two plasma membranes of the synergid and the central cell, Sy synergid, Cc central cell, bar = 0.7 μm. d Ultrastructure of the egg cell and the central cell; Eg egg cell, red arrows attachment of the egg wall to the wall of the embryo sac; Cc central cell, framed parts shown in Fig. E (blue) and F (red) bar = 2 μm. e The cell wall between the egg cell and the central cell; Eg egg cell, Cc central cell, circle plasmodesmata, bar = 0.9 μm. e The cell wall between the egg cell and the central synergid; Eg egg cell, circle plasmodesmata, bar = 0.35 μm

Fig. 7

Ultrastructure of a U. quelchii egg cell and central cell. a The micropylar part of the egg cell; Eg egg cell, En egg nucleus, m mitochondrion, d dictyosome, P plastid, Cc central cell, framed part shows microtubules near the egg plasma membrane, bar = 0.6 μm. b Polar nuclei during fusion; red arrows nuclear bridges, m mitochondrion, d dictyosome, bar = 0.4 μm. c The central cell with a secondary nucleus; m mitochondrion, S starch grain in an amyloplast, N secondary nucleus, bar = 0.9 μm