Research

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 molecular biology with whole genome sequencing, transcriptomics, and phylogenetics. We use plants and insects as models to study adaptation and current projects examine the underlying genetics and evolution of chemical and structural defense.

We seek to understand how plants and insects acquire novel phenotypes through co-option of existing genes, tissues, and organs. Specifically, we investigate the role, regulation, and diversity of chemical defense genes, and examine the evolution of multi-step enzyme-catalyzed pathways that form defensive compounds in specialized tissues and organs. This research has broad implications for understanding how plants repurpose defense genes for nutrient acquisition and which genes are key players in the formation of compounds important for insect defense.

We have three main research areas: (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 in insects. Topics we are currently 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 chemical defense

(A) Carnivorous plant class I chitinases form two distinct clades and are involved in either digestion or defense. (B) Nepenthes pitcher plant defense chitinases are under positive selection at site Phe276*, which interacts with the substrate. For more information Renner & Specht 2012 MBE.

Co-option and molecular diversity of enzymes used in plant carnivory

Carnivorous plants provide ideal model systems for investigating both evolutionary transitions and convergence, because this unusual adaptation arose multiple times among angiosperms (possibly 10 times, among 5 orders) with remarkable cases of morphological and molecular convergence across deep time. Shared among these lineages is the ability to digest metazoans as a means to obtain essential nutrients (primarily nitrogen and phosphorus), a process that is determined in part by suites of digestive enzymes associated with morphologically diverse modified leaves that serve as trapping mechanisms. In all carnivorous plants studied so far, evidence points to co-option of common defense proteins for prey-responsive functions such as digestion; however, details concerning the origins, evolution and mechanisms of action of the relevant gene families remain only poorly understood.

We examine the extent that co-option has played in the functional diversification and regulation of defense proteins used in prey digestion among independently evolved carnivorous plants. To do this, we combine methods in comparative transcriptomics with third-generation genomics. Our research has been funded under NSF DEB 1011021. For publications, see Lan et al. 2018 Proc Natl Acad Sci USA, Renner et al. 2018 & Matusikova et al. 2018 “Carnivorous Plants: Physiology, Ecology, and Evolution” (peer-reviewed book chapters), Michalko et al. 2017 Planta, Renner & Specht 2013 Curr Opin Plant Biol, and Renner & Specht 2012 MBE.

 


Plant form and function, including morphological adaptations for insect capture

Phylogenetic relationships of carnivorous non-core Caryophyllales. Circles indicate carnivorous habit (red) and loss (white) events. For more information, see Renner & Specht, 2011. Plant images: Renner & Specht, 2011 and Vincaye/Vecteezy.com

The diversity of specialized morphological adaptations that carnivorous plants use to trap and digest insects provides an optimal system for studying the extent at which plant-insect interactions drive the evolution of plant form and function. Within the Caryophyllales lineage of carnivorous plants, we have investigated leaf morphology within a phylogenetic framework, 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.

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). Our research has been supported by NSF DEB 1011021. For publications on carnivorous plant morphology, see for example Renner & Specht 2011 IJPS and Bauer, Clemente, Renner, & Federle, 2012 J Evol Biol.


Evolutionary mechanisms behind insect chemical defense 

Secretory lobe section of Harpalus pensylvanicus viewed via CLSM. Glandular spheres (sph) show red-green autofluorescence while the collecting duct (cd) and ductules (duc) connecting the collecting duct with the glandular spheres autofluoresce in the blue interval showing the typical emission wavelength for resilin in response to the 405 nm (violet) excitation laser. Image and description from Rork et al. 2019.

Our research seeks to identify which genes are essential for the formation of chemicals that provide defense against predators. Ground beetles (Coleoptera: Carabidae) are an ideal model for understanding how genetic variation drives functional diversification of chemical biosynthesis, as members of this diverse (~40,000 species) lineage produce >250 individual compounds – sometimes at extremely hot temperatures (>100 degrees Celsius). Our group uses methods in tissue-specific comparative transcriptomics to identify genes highly expressed within specialized tissues and organs, which are generally thought to be sites of chemical biosynthesis. Through collaborations with researchers at other U.S. institutions, we have combined results of transcriptome sequencing with methods in traditional gas chromatography–mass spectrometry (GC/MS) to characterize roles the roles our candidate genes play in the biosynthesis of defensive compounds. Our work is currently funded under NSF DEB 1762760 to study the genetic basis, biosynthetic pathways and evolution of geadephagan chemical defense. This project addresses 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). For publications, see Rork et al. 2019 Arthropod Struct Dev and Rork & Renner 2018 J Chem Ecol.

In addition to our genetic studies, we have worked toward understanding the complex morphology of the tissues responsible production of these chemicals. Our Arthropod Struct Dev (Rork et al. 2019) publication revealed for the first time resilin in an insect glandular duct system, which may serve to manage pressure generated by reservoir pump contraction and prevent autointoxification. This integrative research has the potential to advance understanding of enzyme-catalyzed pathways and the processes by which they have evolved, as well as how toxic compounds can be stored within specialized tissues and organs.

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