Micro- and Macroscale Patterns of Petal Morphogenesis in Nigella damascena (Ranunculaceae) Revealed by Geometric Morphometrics and Cellular Analyses

Abstract

Petals, the inner organs in a differentiated perianth, generally play an important role in pollinator attraction. As such they exhibit an extraordinary diversity of shapes, sizes, and colors. Being involved in pollinator attraction and reward, they are privileged targets of evolution. The corolla of the Ranunculaceae species Nigella damascena consists of elaborate nectariferous petals, made of a stalk, upper, and lower lips forming a nectar pouch, shiny pseudonectaries, and pilose ears. While the main events of petal development are properly described, a few is known about the pattern of organ size and shape covariation and the cellular dynamics during development. In this study, we investigated the relationships between morphogenesis and growth of N. damascena petals using geometric morphometrics coupled with the study of cell characteristics. First, we found that petal shape and size dynamics are allometric during development and that their covariation suggests that petal shape change dynamics are exponentially slower than growth. We then found that cell proliferation is the major driver of shape patterning during development, while petal size dynamics are mostly driven by cell expansion. Our analyses provide a quantitative basis to characterize the relationships between shape, size, and cell characteristics during the development of an elaborate floral structure. Such studies lay the ground for future evo-devo investigations of the large morphological diversity observed in nectariferous structures, in Ranunculaceae and beyond.

Three-dimensional study of spur morphogenesis in the flower ofStaphisagria picta(Ranunculaceae) – from cellular level to organ scale

“…These studies are focused on the epidermal cells, or are based on two-dimensional observations of this organ, often addressing the question of the origin of the interspecific diversity within a genus (e.g. Puzey et al, 2012;Galipot et al, 2021;Edwards et al, 2022). Comprehensive 3-dimensional information on all cells of the spur (not only the epidermal cells) is missing, hindering our full understanding of the mechanisms involved in complex petal forms.…”

“…At the cellular level, the development of the invagination of the petal of Nigella damascena is organized in two successive steps of cell proliferation and cell expansion, as observed in Staphisagria and Aquilegia. The first phase is responsible for most of the shape (Galipot et al, 2021). The two lips are formed by the differential expression domains of adaxial and abaxial genes during morphogenesis (Yao et al, 2019;Cheng et al, 2023).…”