The Development and Evolution of Glands in the Malpighiaceae

Abstract

Plant-animal interactions are a critical driver of the floral and faunal biodiversity on our planet, and understanding these interactions requires exploration of the contributions of each participant. While pollen and nectar are the most frequent and best-studied rewards that plants provide, floral lipids are an often-overlooked reward offered by many plants from oil glands called “elaiophores.” These plants, typically mutualists with oil-gathering bees, comprise 1,000 species across 11 different flowering plant families, including important crops. Despite the importance of oil glands, little is known regarding their development, molecular genetic control, or fine-scaled evolutionary trait history. In the presented dissertation, I used a complementary set of approaches to investigate oil gland evolution in the oldest and most species-diverse family to bear the structures, the Malpighiaceae. This work also encompassed the family’s extrafloral glands, which may play a role in plant defense and have been suggested to have given rise to the floral oil glands. In Chapter 1, I used histology to compare gland development across many representatives of the family, providing a novel developmental perspective and sampling a much broader scope of taxa than previous studies. In Chapter 2, I conducted ancestral character reconstruction on a Malpighiaceae species-level phylogeny to examine evolutionary aspects of gland gain/loss and gland patterning, considering both floral and extrafloral glands as well as distinct mutualist regimes. This dataset includes a family-wide archival trait matrix database of all gland types and arrangements found across ~1000 species, based on hundreds of years of taxonomic descriptions. This database will enable many future studies of gland evolution. This chapter has provided the most fine-scale gland trait reconstruction to date for the Malpighiaceae. In Chapter 3, I then produced novel molecular characters for gland development by performing comparative RNA-Seq for two developmental timepoints of eglandular and glandular sepals. This work is the first transcriptomic study of any oil glands in any system and provided the first molecular characterization of secretory structures in the Malpighiaceae. This has also identified a suite of potential candidate genes for the control of gland morphogenesis. These diverse results highlight a family with great variation in its secretory structures, potential plasticity in the gland developmental program(s), responses of extrafloral glands to as-yet-unknown ecological relationships, and a body of evidence to guide future studies into the origin and patterning of these glands.