Dr. Tanya Renner and members of her laboratory explore evolutionary patterns and processes that drive functional diversification. We are particularly interested in how multi-species interactions shape diversity on a genome-wide scale and influence form and function. Our research combines applied molecular biology with next-generation sequencing, bioinformatics, and phylogenetics. We use plants and insects as models to study adaptation and current projects focus on the evolution of chemical and structural defenses.
My research program focuses on three integrated components: (1) an examination of the underlying genetics both linking and separating chemical defense and nutrient acquisition in plants, (2) investigations of plant structural defense mechanisms and adaptations for insect capture, and (3) studies of chemical defense and detection in insects. Topics we are investigating:
- Co-option and molecular diversity of enzymes used in plant carnivory
- Plant form and function, including morphological adaptations for insect capture
- Evolutionary mechanisms behind insect defense, host preference and detection
Co-option and molecular diversity of enzymes used in plant carnivory
Plants use an array of chemical defense mechanisms to protect themselves against herbivorous insects and insect-vectored diseases. These include the production of pathogenesis-related (PR) proteins that are produced in response to pathogens and induced as part of systemic acquired resistance.
Increasing evidence suggests that PR proteins involved in plant defense have been co-opted to function in plant carnivory in the Caryophyllales, a major group of plants that includes the Venus flytrap (Dionaea), sundews (Drosera), and tropical pitcher plants (Nepenthes), among others (Renner & Specht, 2013). Within the “carnivorous Caryophyllales”, two subclasses of PR proteins produced by the large and diverse chitinase gene family have been identified. Members of these two subclasses are either constitutively expressed and localized to the vacuole (subclass Ia) or induced in response to prey and secreted from specialized digestive glands found within the morphologically diverse traps that develop from carnivorous plant leaves (subclass Ib).
Molecular evolutionary studies within the angiosperms support that during the evolution of carnivory within the Caryophyalles, class I chitinase genes that were primarily utilized for pathogenesis response by ancestral non-carnivorous plants diverged, allowing for subfunctionalization of subclass Ia (for pathogenesis-response) and Ib chitinases (for carnivory). Additionally, there is evidence that selection pressures acting on subclass Ib chitinases have shifted as pathogenesis response gave way to a role specific to carnivory, affecting structure and likely function. In subclass Ia, amino acid substitutions that are the result of positive or diversifying selection and within the catalytic cleft are thought to be the result of an evolutionary arms-race between chitinolytic enzymes and competitive inhibitors produced by pathogens, whereas a relaxation in substitution rates as in subclass Ib, is due to a shift in access to extracellular materials (e.g. chitin primarily sourced from insects within the trap). This study was the first to conduct an in-depth analysis of the flowering plant class I chitinases used in pathogenesis-response, while focusing on the functional evolution of Ia and Ib subclasses in the carnivorous plants of the Caryophyllales (Renner & Specht 2012). This research has been funded by NSF DEB 1011021. We are now combining methods in comparative transcriptomics and third-generation genomics to study the evolution of plant carnivory across independent lineages.
Plant form and function, including morphological adaptations for insect capture
The diversity of specialized morphological adaptations used to trap and digest insects makes the carnivorous Caryophyllales an ideal model system for addressing whether plant-insect interactions drive the evolution of leaf form and function. Previous research has used a phylogenetic framework to investigate leaf morphology, including the evolution of multicellular glands and specialized slippery surfaces for prey capture.
Shared among the noncore Caryophyllales is the presence of various types of multicellular glands that are distributed across the above-ground portion of the plant. In carnivorous taxa, glands are associated with leaves that have been modified to capture and digest insects and are sessile, stalked, or pitted, and can contain xylem and phloem. Families sister to the carnivorous Caryophyllales exhibit similar morphologies called glandular trichomes that function in the immobilization of herbivorous insects and perform additional ecological roles (e.g. protection in halophytic conditions and seed dispersal). This may suggest that such basic structures have been modified in the evolution of carnivorous plants to function specifically in carnivory. Our studies support that the ancestral state for the carnivorous Caryophyllales are sessile glands without vasculature, while stalked and pitted glands were acquired secondarily and independently by the non-carnivorous sister families and by various lineages of carnivores. Such independent origins are reflected in differences in vascularization and overall gland morphology (Renner & Specht, 2011). This research has been funded by NSF DEB 1011021.
In addition to sticky glands, plants have a variety of insect repellent surfaces that inhibit insect attachment or slow movement. In carnivorous plant traps, leaf surfaces are modified to aid in the capture of prey. For example, Nepenthes pitcher traps have at least two forms of slippery surfaces: firstly, inner pitcher walls and lids with wax crystals, and secondly, peristomes with extremely hydrophilic inward-facing trichomes that initiate ‘insect aquaplaning’. In a collaboration with researchers at the University of Bristol and Harvard University, we found that Nepenthes trapping strategies are closely tied to adaptations of the functional leaf morphology (Bauer, Clemente, Renner, & Federle, 2012). We are currently studying the genes underlying slippery Nepenthes surfaces.
Evolutionary mechanisms behind insect defense, host preference and detection
News! We were recently funded by NSF (DEB 1556931) to study the genetic basis, biosynthetic pathways and evolution of geadephagan chemical defense (2016-2019)! This project will address how the bombardier beetle evolved its explosive defense abilities. For more info, see this video and article to learn about our collaborative research with Kip Will (UC Berkeley), Wendy Moore (U. Arizona), and Athula Attygalle (Stevens Institute of Technology).
Chemical defense is one of the most ecologically and taxonomically prevalent means of predator avoidance among terrestrial animals. Geadephaga (carabid beetles) is an ideal group to investigate the evolution of chemical defense as all species have homologous defensive glands that can produce an exceptionally wide array of defensive chemicals. Among these, quinones have been reported as a defensive compound in 170 species from 50 families of arthropods and are thought to be present in hundreds more species. Quinones are also known to be involved in a common mechanism of sclerotization, or the stiffening of the cuticle in all arthropods.
Focusing on four lineages that span carabids and are known to produce defensive quinones, two of which are commonly known as bombardiers famous for delivering hot defensive sprays, our research aims to (1) infer the biosynthetic pathways for quinone production in each using labeled amino acids, (2) characterize genes involved in quinone synthesis using comparative transcriptomics and validate their function experimentally using RNAi, (3) determine the extent of gene diversity in quinone production, and (4) compare the evolutionary rates of those genes relative to rates of change in chemical biosynthetic pathways. Our results will reveal whether, despite millions of years of evolution, independent lineages have co-opted similar genes and biochemical pathways in the production of defensive quinones. This work is a collaboration with Kipling Will (UC Berkeley), Wendy Moore (University of Arizona), and Athula Attygalle (Stevens Institute of Technology). This Research is funded by NSF DEB 1556931 and NIH K12 GM000708.
Host preference and detection
In insects, olfaction plays a major role in many behaviors, including the detection of odorants or pheromones associated with food sources, toxins, predators, potential mates, and hosts. The process of chemoreception is initialized by small antennary proteins such as odorant-binding proteins (OBPs) that transport semiochemicals from the air-fluid interface of the antennae to odorant receptors (ORs) embedded within the dendritic membrane of chemosensory neurons. Our current study focuses on understanding the molecular evolution of chemosensory gene families within Coleoptera, and includes the first sequences from the second-largest suborder of beetles, Adephaga.
Utilizing a transcriptomics approach, novel OBP and OR homologs have been recovered from members of flanged bombardier beetles (Carabidae: Paussinae) that are either generalist arthropod predators or obligate myrmecophiles. This work is a collaboration with Wendy Moore at the University of Arizona and funded by NIH K12 GM000708.