Evolution of Catkins: Inflorescence Morphology of Selected Salicaceae in an Evolutionary and Developmental Context

Abstract

Poplars (Populus sp.) and willows (Salix sp.) are well known woody plants common throughout the northern hemisphere, both with fully sequenced genomes. They bear compact unisexual inflorescences known as "catkins." Closely related genera of the "salicoid clade" within the family Salicaceae include the Asian genera Bennettiodendron, Idesia, Itoa, Poliothyrsis, and Carrierea and the Central American genera Olmediella and Macrohasseltia. Like willow and poplar, most of these genera are dioecious, but unlike willow and poplar they generally have loosely branched panicles rather than catkins, and less highly reduced flowers. However, the early developing inflorescences of Carrierea and Idesia show similarities to catkins which suggest possible pathways by which the salicoid catkin may have evolved.

Keywords: dioecy; floral reduction; genome-enabled model system; heterochrony; inflorescence architecture; inflorescence evolution; preformation; synorganization.

FIGURE 1

Summary phylogenetic diagram showing the relative phylogenetic position (arrowed) of selected groups that have formerly been included in the Amentiferae due to their catkins or catkin-like inflorescences (see text). The phylogeny reflects that of the Angiosperm Phylogeny Group (2009). Only major clades are shown: the position of minor clades is indicated with dashed lines.

FIGURE 2

Summary phylogenetic diagram showing the major groupings within the salicoid clade, after Alford et al. (2009).

FIGURE 3

Photographs of inflorescences. (A) Young inflorescence of Carrierea calycina Franch.) collected May 2015. The flowers are unopened. The floral bracts and calyces are visible. (B) Young male inflorescence of Idesia polycarpa Maxim., collected May 2015. The flower buds are still small but the branching of the paniculate inflorescence is evident. This inflorescence has developed in 3 months from an inflorescence meristem as shown in Figure 5B. (C) Previous year’s female inflorescence (infructescence) of I. polycarpa, collected February 2015, showing the extensive branching of the inflorescence.

FIGURE 4

Carrierea calycina. (A) Over-wintering bud with minute inflorescence meristem surrounded by protective bracts (bud scales) collected 13th February 2015. At this stage the inflorescence has not started developing. (B,C) Sequential longitudinal sections of dissected resting bud (pre-budbreak) collected 2nd April 2015, showing a fairly well-developed inflorescence with individual flowers differentiated. Floral bracts and calyx are visible but other organs have not formed and gender is not visible at this stage (bud scales removed). (D) Detail of developing flower from (C). Scale bars = 1 mm.

FIGURE 5

Idesia polycarpa. (A) SEM of bisected over-wintering bud collected 13th February 2015 showing an inflorescence meristem surrounded by protective bracts (bud scales; B) Detail of (A) showing just the inflorescence meristem, At this stage the inflorescence meristem shows inflorescence bract primordia but not floral primordia. Later branch primordia will form in the axils of the inflorescence bracts and develop into the paniculate (i.e., branched) inflorescence. At the same stage Salix and Populus inflorescences are fully developed with completely formed flowers (Figures 6 and 7). (C) Longitudinal section of dissected over-wintering (pre-budbreak) bud collected 2nd April 2015 showing development of panicle (bud scales removed). Flowers can be seen in early development, with some development of the calyx but not other organs. At the same date Salix and Populus have finished flowering. (D) Enlarged portion of (C). Scale bars = 1 mm.

FIGURE 6

Populus. (A) Populus nigra L., male inflorescence (catkin) with nearly fully developed flowers. Longitudinal section of catkin, collected 2nd February 2015, showing well-developed stamens with short filaments and longer anthers with red-staining developing pollen (bud scales removed). (B) P. purdomii Rehder, female inflorescence with flowers in a late stage of development. Longitudinal section of catkin collected 2nd February 2015, showing single ovary per flower. (C) P. wilsonii C.K.Schneid., SEM detail showing a well developed ovary from a female inflorescence, collected 2nd February 2015. Scale bars = 1 mm. Bud scales removed.

FIGURE 7

Salix. (A) Salix miyabeana Seem., male inflorescence (catkin). Longitudinal section of over-wintering bud (bud scales removed), collected 16th February 2015, showing well-developed flowers, each with an apparent single stamen (actually two stamens completely united except at the anther). The anthers are well differentiated pre-anthesis. (B) Salix sp., SEM showing three well developed female flowers in the axils of bracts, from an inflorescence in over-wintering bud collected 16th February 2015. Scale bars = 0.5 mm. Bud scales removed.