Developmental origins of the world’s largest flowers, Rafflesiaceae

Abstract

Rafflesiaceae, which produce the world's largest flowers, have captivated the attention of biologists for nearly two centuries. Despite their fame, however, the developmental nature of the floral organs in these giants has remained a mystery. Most members of the family have a large floral chamber defined by a diaphragm. The diaphragm encloses the reproductive organs where pollination by carrion flies occurs. In lieu of a functional genetic system to investigate floral development in these highly specialized holoparasites, we used comparative studies of structure, development, and gene-expression patterns to investigate the homology of their floral organs. Our results surprisingly demonstrate that the otherwise similar floral chambers in two Rafflesiaceae subclades, Rafflesia and Sapria, are constructed very differently. In Rafflesia, the diaphragm is derived from the petal whorl. In contrast, in Sapria it is derived from elaboration of a unique ring structure located between the perianth and the stamen whorl, which, although developed to varying degrees among the genera, appears to be a synapomorphy of the Rafflesiaceae. Thus, the characteristic features that define the floral chamber in these closely related genera are not homologous. These differences refute the prevailing hypothesis that similarities between Sapria and Rafflesia are ancestral in the family. Instead, our data indicate that Rafflesia-like and Sapria-like floral chambers represent two distinct derivations of this morphology. The developmental repatterning we identified in Rafflesia, in particular, may have provided architectural reinforcement, which permitted the explosive growth in floral diameter that has arisen secondarily within this subclade.ABC model | comparative gene expression | evo-devo | gigantism | parasitic plants

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“…Species of Rafflesiaceae are holoparasitic; and the family is endemic to Southeast Asia and contains the largest flower of angiosperms in the world (Rafflesia arnoldii R.Br. ; Barkman et al, 2008;Nikolov et al, 2013;Nikolov & Davis, 2017).…”

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“…Although it has been recognized that some aspects of the ABC model do not apply to all angiosperms, the specification of petal, stamen, and carpel identity by B‐ and C‐class genes is generally conserved in the core eudicots, where Rafflesiaceae belong (Litt & Kramer, ). We reasoned that if this combinatorial code is conserved in Rafflesiaceae, it could provide a frame of reference to identify the homology of the different floral organs (Nikolov et al, ). Cloned floral identity genes from Rafflesiaceae did not show aberrant patterns of molecular evolution and confounding gene lineage evolution, and thus could be unambiguously assigned to a gene family.…”

“…It has been argued that the presence of the floral chamber was ancestral in Rafflesiaceae, and the chamber has been lost in Rhizanthes (Bendiksby et al, 2010). Developmental data paints a more nuanced picture of the evolution of this trait (Nikolov et al, 2013) (Fig. 4).…”