Embryology in Helosis cayennensis (Balanophoraceae): Structure of Female Flowers, Fruit, Endosperm and Embryo

Abstract

Helosis cayennensis (Balanophoraceae s.str.) is a holoparasite characterised by aberrant vegetative bodies and tiny, reduced unisexual flowers. Here, we analysed the development of female flowers to elucidate their morpho-anatomy and the historical controversy on embryo sac formation. We also studied the developmental origin of inflorescences and the ontogeny of fruits, embryo and endosperm and discussed in a phylogenetic framework. Inflorescences were analysed by optical, fluorescence and scanning electron microscopy. Inflorescences of H. cayennensis arise endogenously. Female flowers lack perianth organs, thus only consist of the ovary, two styles and stigmata. Ovules are undifferentiated; two megaspore mother cells develop inside a nucellar complex. The female gametophyte, named Helosis-type, is a bisporic four-celled embryo sac, provided with a typical egg apparatus and a uni-nucleated central cell. Fertilization was not observed, yet a few-celled embryo and cellular endosperm developed. In sum, results confirm that, among Santalales holoparasites, Helosis is intermediate in the reduction series of its floral organs. Although perianth absence best supports the Balanophoraceae s.str. clade, our literature survey on female flower developmental data across Balanophoraceae s.l. highlights the many gaps that need to be filled to really understand these features in the light of new phylogenetic relationships.

A specialized avian seed dispersal system in a dry‐fruited nonphotosynthetic plant, Balanophora yakushimensis

“…The family Balanophoraceae are among the most unusual of plants because they have aberrant vegetative bodies, highly reduced flowers, and small and reduced embryos (Hansen 1972, Gonzalez et al 2019). Because the plants lack chlorophyll and are incapable of photosynthesis, they draw nutrition from other organisms.…”

First Record of Ategmic Ovules in Orchidaceae Offers New Insights Into Mycoheterotrophic Plants

“…Reduction of integuments occurs independently in different groups. They have been described in mycoheterotrophic species of Gentianales (Gentianaceae), parasite species of Santalales (Balanophoraceae, Loranthaceae, Olacaeae, and Santalaceae), and in a photosynthetic species of Aquifoliales (Cardiopteridaceae) (Maas and Ruyters, 1986; Bouman et al, 2002; Brown et al, 2010; Polli et al, 2016; Sato and Maria Gonzalez, 2016; Suaza-Gaviria et al, 2016; Tobe, 2016; Gonzalez et al, 2019). Molecular studies show that in ategmic ovules of Santalales, the genes associated with the expression of the integument are expressed in the periphery of the ovary, and that the reduction found in these species is the result of the fusion between the integument and the nucellus (Brown et al, 2010).…”

Anatomy, Embryology and Life Cycle of Lophophytum, a Root-Holoparasitic Plant

“…The reduction of ovules, fusion of the ovules with the carpels, and the number of loculi are variable characteristics in the family (Table 2). The complete fusion between the ovules and the carpels determines the absence of a locular cavity in Balanophora [41] and Helosis [46][47][48][49]. In Corynaea [45] and Rhopalocnemis [44] they have a single locule due to the absence of postgenital fusion.…”

“…The ovules of Lophophytum are the only ones in the whole family that are still distinguishable from the placenta, although they are ategmic. In Corynaea, Dactylanthus and Rhopalocnemis [42,44,49] the term placental-nucellar complex (PNC) has been used instead of ovules, as the boundary between the nucellus and the placenta is blurred. The most extreme reduction occurs in Helosis and Balanophora, where there are no recognizable ovules; the ovary, placenta and nucellus are completely fused into a compact mass where the embryo sacs develop, there is no ovarian cavity [41,44,50].…”