STUDENT DIGEST

Comparative anatomy sheds light on the evolution of sympetaly of mimosoid legumes

Monique Maianne, PhD candidate,
Universidade de São Paulo, Ribeirão Preto, Brazil
Universidade Federal de São Carlos, São Carlos, Brazil

The breathtaking diversity of flowers stems not only from evolutionary change driven by extrinsic factors, such as biotic interactions, but also intrinsic factors, such as genetics and development. Developmental changes resulting from genetic mutations over time and/or from changes in the physical environment of apical meristems may lead to modification or elaboration of floral structures (Ronse De Craene 2018). For example, tubular corollas formed by fusion of petals (i.e., sympetaly) may be associated with protection of reproductive organs (Endress 2011). Moreover, tubular corollas can augment pollination efficiency, by restricting access to floral resources for pollinators with specific morphologies (Endress 2011), impacting on reproductive success and thereby influencing evolutionary diversification.

One of the largest groups of Angiosperms, the asterids, is well-known for its sympetalous corollas, a trait that evolved multiple times within that clade (Zhong & Preston 2015). The complex evolution of sympetaly in asterids is consistent with the multiple developmental trajectories of petal fusion. Fused corollas may form at early developmental stages in which petals emerge already fused in a ring primordium (congenital fusion), or later by fusion or joining of the margins of individually formed petals (post-genital fusion) (Philips et al., 2020). Sympetaly is not unique to asterids, but also occurs in other angiosperm lineages, and is particularly prevalent in mimosoid legumes (LPWG 2017), a clade deeply nested in the rosids. As corollas with free petals are prevalent in rosids, understanding how sympetaly develops in mimosoids may hint at mechanisms underlying variation in the morphology, function, and evolution of tubular flowers.

Left to right: Inflorescence of Inga vera Willd.; Inflorescences with some flowers removed from Stryphnodendron rotundifolium Mart. and Mimosa nuda Benth. Photos by Monique Maianne.

In a recent paper published in Perspectives in Plant Ecology, Evolution and Systematics, Pedersoli et al. (2023) investigated the development of sympetaly in 16 of 100 mimosoid genera. They found that sympetaly is post-genital and arises by tissue fusion (connation), interlacing of epidermal papillae (coherence), or a mixture of both (connation-coherence). Additionally, some of the investigated genera have special mucilage cells (Matthews & Endress 2006) on the abaxial surface and distal part of the petals. While such mucilage cells could be enhancing the protective role of the corolla during floral development, Pedersoli et al. suggested that mucilage secretions could provide additional support and flexibility to the corolla tube and, therefore, may be associated with sympetaly in mimosoids.

What insights can the phylogenetic distribution and type of sympetaly provide regarding the evolution of mimosoids and diversification of their flowers? Pedersoli et al. proposed that cohered petals are phylogenetically over-dispersed , while connation is apparently restricted to the derived Ingoid clade. Although more taxa need to be studied to verify these claims, this pattern suggests that gamopetalous corollas formed by interlacing of epidermal papillae on petal margins and evolved before connation in mimosoids.

Pedersoli et al. also demonstrated that, despite variation in the type and extent of petal fusion the resulting corolla macro-morphologies are similar. Indeed, floral morphology is relatively uniform across mimosoids, which have small radially symmetrical flowers with valvate petal aestivation and synchronous floral development. Although there are exceptions, phenotypic variation occurs mainly in the size of the organs, number of parts per whorl and the degree of fusion of floral organs (Ronse De Craene 2010; Koenen et al., 2020). As shown by Pedersoli et al., comparative studies of development have the potential to provide new insights into the diversity of mechanisms underlying the evolution of the distinctive mimosoid flower.

References

Endress, P. K. (2011). Evolutionary diversification of the flowers in angiosperms. American Journal of Botany 98(3): 370-396.

Koenen, E. J., Kidner, C., de Souza, É. R., Simon, M. F., Iganci, J. R., Nicholls, J. A., … & Hughes, C. E. (2020). Hybrid capture of 964 nuclear genes resolves evolutionary relationships in the mimosoid legumes and reveals the polytomous origins of a large pantropical radiation. American Journal of Botany 107(12): 1710-1735.

LPWG (2017). A new subfamily classification of the Leguminosae based on a taxonomically comprehensive phylogeny: The Legume Phylogeny Working Group (LPWG). Taxon 66(1): 44-77.

Matthews, M. L., & Endress, P. K. (2006). Floral structure and systematics in four orders of rosids, including a broad survey of floral mucilage cells. Plant Systematics and Evolution 260, 199-221.

Pedersoli, G. D., Mansano, V. F., de Barros, T. C., Paulino, J. V., & Teixeira, S. P. (2023). Sympetaly in the mimosoid clade (Leguminosae, Caesalpinioideae): an unusual trait in the rosid group. Perspectives in Plant Ecology, Evolution and Systematics 125747.

Phillips, H. R., Landis, J. B., & Specht, C. D. (2020). Revisiting floral fusion: the evolution and molecular basis of a developmental innovation. Journal of Experimental Botany 71(12): 3390-3404.

Ronse De Craene, L. (2018). Understanding the role of floral development in the evolution of angiosperm flowers: clarifications from a historical and physico-dynamic perspective. Journal of Plant Research, 131 367-393.

Ronse De Craene, L. P. (2010). Floral diagrams: an aid to understanding flower morphology and evolution. Cambridge University Press.

Zhong, J., & Preston, J. C. (2015). Bridging the gaps: evolution and development of perianth fusion. New Phytologist 208(2): 330-335.