Organ homologies in orchid flowers re-interpreted using the Musk Orchid as a model

Abstract

Background and Aims. The presence of novel structures in orchid flowers, including auricles, rostellum and bursicles on the gynostemium and a lobed labellum, has prompted long-standing homology disputes, fuelled by conflicting evidence from a wide range of sources. Re-assessment of this debate using an improved model is timely, following recent phylogenetic insights and on the cusp of a revolution in developmental genetics.Methods. We use new data from floral development and anatomy in the small-flowered terrestrial orchid Herminium monorchis as a model to explore organ homologies in orchid flowers within the context of a review of recent literature on developmental genetics.Key Results. The apex of the median carpel of Herminium is trilobed, and the bursicles develop from its lateral lobes, relatively late in flower ontogeny. The bursicles enclose the viscidia, which adhere to the tapetal remnants to form a caudicle linking the viscidium with the pollinium. The auricles are initiated earlier than the bursicles, but they also remain unvascularized. The deeply trilobed labellum possesses three vascular traces, in contrast with the lateral petals, each of which contains a single vascular trace. The two lateral labellum traces diverge from the traces supplying the two adjacent lateral sepals. Data from flower ontogeny and anatomy conflict with respect to organ homologies.Conclusions. Much progress has recently been made in understanding the exceptional differentiation shown by orchids among perianth segments, focusing on multiple copies of the DEF/AP3 subclass of B-class MADS-box genes. In contrast, untangling homologies of profound congenital union of multiple floral organs forming the orchid gynostemium is hampered by their profound congenital union, which we ascribe to overlap in gene expression between organs. Thus, the functional morphology of the orchid flower could ultimately reflect extreme synorganization and associated genetic integration. Analogizing the deeply lobed orchid labellum with a compound leaf, we speculate that KNOX genes could be implicated not only in their demonstrated role in spur development but also in the development of both the characteristic lobed morphology of the orchid labellum and the lobing of the median carpel that differentiates the bursicles and rostellum.

Himantoglossum hircinum(Lizard Orchid) reviewed in the light of new morphological and molecular observations

“…The early stages of floral development in H. hircinum (Figs 10, 11) broadly follow those documented for other genera of Orchideae (Kurzweil, 1987;Box et al, 2008;Rudall et al, 2013). The greater size of the labellum of the H. hircinum-jankae clade does not simply represent giantism, as changes in its dimensions are non-allometric; the central lobe increases greatly in length, whereas its width decreases relative to those of sisterspecies H. formosum and H. robertianum.…”

“…In addition, the evolutionary origin and ontogenetic underpinning of the remarkable floral morphology of H. hircinum have received little attention relative to those of other genera (cf. Kurzweil, 1987;Box et al, 2008;Rudall et al, 2013).…”

Evolution and Expression Patterns of TCP Genes in Asparagales

“…Conversely, orchid flowers are variously bilateral and undergo extreme elaboration of some organs, including differentiation of perianth parts, stamen abortion, and fusion of floral parts from the same whorl or from different whorls (Rudall, 2002). In the bilateral resupinated orchid flowers the two dorsal petals are very similar to each other, whereas the ventral one (the lip or labellum) often undergoes extreme elaboration in shape, color, size and epidermal specializations (Rudall and Bateman, 2004; Pabón-Mora and González, 2008; Mondragón-Palomino and Theißen, 2009; Rudall et al, 2013; Endress, 2016). In the inner floral whorls bilateral symmetry is evident by the formation of a gynostemium that results from the congenital fusion between the single fertile stamen (sometimes two fertile stamens) and stigmas (Rudall and Bateman, 2002; Pabón-Mora and González, 2008; Endress, 2016).…”

Exploring the evolutionary origin of floral organs of Erycina pusilla, an emerging orchid model system

“…This structure is thought to result from a fusion of a maximum of six fertile to (partly) sterile stamens and parts of the pistil, in particular the style and stigma. It is a complex organ and the evolutionary origin of its different parts is not yet clear [9, 13, 14]. During the evolution of the orchids over the past 100 million years a reduction in the number of fertile stamens and fusion with the carpels occurred [15–17].…”