Fields of research
How do evolutionary novelties arise?
One of the central goals of evolutionary research is to understand how changes in gene regulatory networks leads to the origin of novel, complex traits, or, in short: How do evolutionary novelties arise? We propose to use the origin of novel traits emerging in the order Ranunculales (buttercups) as model system to study the molecular nature of their origin. Ranunculales are early branching eudicots that comprise morphologically diverse species such as buttercups, poppies, columbines and larkspur. Ranunculales are special because several morphological novelties evolved repeatedly, e.g., spurred floral organs and zygomorphy, or the reduction of perianth. Moreover, novel floral organs, reduction to spiral floral phyllotaxy from whorled, dioecy, and wind pollination originated in this order, in some cases repeatedly. Many species within the Ranunculales are amenable to Virus-Induced Gene Silencing, which allows for functional characterization of candidate genes in later stages of the proposed project.
We propose to sequence 20 transcriptomes of eight Ranunculales species (Eschscholzia californica, Papaver somniferum, Capnoides sempervirens, Pteridophyllum racemosum, Thalictrum thalictroides, Aquilegia coerulea, Nigella damascena and Staphisagria picta) that encompass these novelties including two outgroup species. For the species without genome information available, we plan to sequence their genomes. The transcriptomes will be obtained from a variety of tissues, including floral buds at different developmental stages, dissected floral organs, petal time-series and vegetative tissues. Our ultimate goal is to uncover the GRN modules required for the emergence of novel, often convergently emerging traits. Furthermore, we hope to unravel in the future the processes by which GRN modules are reused and coopted to generate complex floral morphologies and thus drive species diversification. In the proposed project, we want to provide the resources for comparative analysis of genomes and transcriptomes in Ranunculales. This will pave the way to unravel the genetic base novel morphological trait origin.
Funding: 2021 - 2025 German Research Foundation (DFG)
Kooperationspartner: Alexander Goesmann (JLU), Elena Kramer (Harvard), Veronica di Stilio (Seattle), Paula Elomaa (Helsinki), Sophie Nadot (Paris), Catherine Damerval (Paris), Florian Jabbour (Paris), Ian Grahan (York).
Plant cells are interconnected by plasmodesmata (PD), i.e. complex cytoplasmic channels that mediate intercellular communication and symplasmic exchange of (macro)molecules. The invention of PD was a crucial step in plant evolution, since it allowed i) the development of increasingly complex plant bodies with division of labour between spatially patterned tissues and organs and it enabled ii) coordinated strategies to face the hazardous biotic and abiotic stresses occurring during the conquest of land.
In seed plants, PD networks are highly dynamic and undergo drastic functional and structural changes controlling developmental processes, metabolic acclimatisation and pathogen responses. Yet, information on PD networks in non-seed plants and streptophyte algae is scarce and often inconsistent. Within the streptophytes, homology of PD-like structures in the ZCC grade algae and land plant PD is hypothesised, although there are still uncertainties pertaining to a uniform PD architecture and a common mode of PD formation which will be addressed in the present project.
Postcytokinetic formation of secondary PD in pre-existing cell walls is an appropriate mode to adjust PD numbers (and transport capacities) to changing requirements and has evolved (independently?) at least in some lycophyte lineages and spermatophytes. Whether secondary PD formation also occurs in other land plant lineages is unclear and will be investigated in the project.
Since the project is part of the DFG priority programme 2237 “MAdLand - Molecular Adaptation to Land: plant evolution to change”, we will perform our microscopic analyses on the MAdLand model plant species which represent distinct taxa of streptophyte algae and non-seed land plants. We aim to discover basic differences in PD structure and origin among the streptophyte lineages, the molecular basis of which will be addressed in the second funding period.
Funding: 2020-2023 German research Foundation (DFG)
Cooperation partners: Stefan Rensing, University of Marburg (MAdLand coordinator), cf.and
Phylotranscriptomics of the carpel developmental toolkit - an evodevo study towards understanding the origin of flowering plants
We know relatively little about the origin of angiosperms, a group of plants that dominate most terrestrial ecosystems and provides us with most of our food. Despite the fact that genomes and transcriptomes of angiosperms and their sister group, the gymnosperms are available already; some early angiosperm fossils are described; and the phylogeny of seed plants, comprising angiosperms and seed plants is generally solved, answers to the key questions of how did the first angiosperm look like and which genes were required to build this ancestral angiosperm remain unanswered.
The general aim of this project is to identify a minimal set of genes required for carpel development in angiosperms to understand which genetic prerequisites were required to build the ancestral carpel, and thus, how a crucial step during angiosperm origin was completed. Subsequently, the molecular functions and genetic interactions of this set of genes will be identified to predict the ancestral state of the carpel development network and to learn which genes carried out which functions in the ancestral angiosperm. This project is the first to systematically analyze carpel developmental regulators in an unbiased way across a wide range of phylogenetically important taxa by a combination of laser capture microdissection and phylotranscriptomics. With the newly published genomes of A. trichopoda and P. abies and the availability of the W. mirabilis transcriptomes as second gymnosperm from a divergent lineage, this project is now a timely and realistic undertaking.
Funding: 2016 – 2019 German Research Foundation (DFG)
Cooperation partners: Alexander Goesmann and Oliver Rupp, Institute for Bioinformatics and Systems Biology, JLU Gießen, Knut Beuerlein, Rudolph-Buchheim-Institute for Pharmacology, JLU Gießen
Evolutionary genetics of carpel development using California poppy (Eschscholzia californica) as a new model species
All flowering plants have carpels, female reproductive structures that enclose the eggs and subsequently develop into seedpods and fruits. Carpel development genes are being defined in the model species Arabidopsis, an advanced flowering plant. But the evolutionary origin of carpels is not clear. In this project, we will identify and characterize genes that control carpel development in a more primitive plant, California poppy (Eschscholzia californica). This new model species is a basal eudicot that can be manipulated transgenically. Comparison of carpel genes in poppy and Arabidopsis will help reveal core genes that underlie carpel development in all flowering plants. This will allow us to identify genes that play the same important role in carpel development across dicots, and also those that play more specialized roles. The underlying question is how gene networks, consisting of developmental genes from different gene families, govern plant development and how these networks evolve resulting in changes to plant structure.
Funding: 2005-2014 German Research Foundation (DFG), continuation with JLU funding
Comparative transcriptome analysis and phenotypic monitoring of Trifolium pratense (red clover, Fabaceae) under land use scenarios (TRATSCH)
Trifolium pratense (red clover) is an important fodder plant that can be found on almost all agriculturally used grasslands. We have shown that T. pratense, as many other grassland species responds to mowing or grazing with specific morphological changes. Further, we have identified datasets of genes that are differentially expressed between different plots and others, that show a mowing-specific response. We propose to (1) extend our data collection and analysis to all exploratories, (2) correlate differential gene expression with environmental data , (3) analyzed compensatory effects in respect to an increase of inflorescences in mowed plants, (4) carry out functional analysis of the mowing-response genes.
Funding: 2014 – now, German Research Foundation (DFG)
Co-PI’s: Birgit Gemeinholzer and Volker Wissemann (Institute of Botany, JLU Gießen)
Cooperation partners: Alexander Goesmann and Oliver Rupp, Institute for Bioinformatics and Systems Biology, JLU Gießen
Revealing ancestral functions of TCP transcription factors
Plants show a striking morphological variation in nature. This project aims to explain some aspects of the diversity observed by analyzing members of the plant specific TCP domain transcription factors. These genes are strongly conserved within higher plants but still the biological function for several of them remains obscure, for those whose functions are characterized it was shown that they all control plant growth and development. In the proposed joint project we aim to identify functions for CYCLOIDEA (CYC) genes, some of which have been shown to control flower symmetry in species with bilateral symmetry and are hence of special importance to the pollination syndromes.
The aim of this project is to understand the origin and evolution of CYC-like genes and to reveal ancestral function of these transcription factor encoding genes.
Funding: 2015 – 2017, German Academic Exchange Service (DAAD)
Co-PI: Paula Elomaa, University of Helsinki, Finnland
Understanding the molecular mechanisms underlying convergent evolution of the gynoecium architecture
The fruits and grains we eat are largely derived from carpels of flowering plants (angiosperms). Carpels, the female reproductive organs, are the unifying character (autapomorphy) of angiosperms. Many components and interactions of the genetic regulatory network (GRN) that orchestrates the development of this complex organ are well characterized in the model species Arabidopsis thaliana. Yet, the origin and conservation of the carpel’s developmental program remains mysterious, as functional data from non-Brassicaceae are lacking to a large extent.
The main aim of this study is to identify the common components and regulatory mechanisms orchestrating carpel development in dicotyledonous plants, among which many carry agronomically valued seeds and fruits. We aim to (1) identify common regulatory mechanisms and distinguish those from the specific ones, (2) identify conserved regulatory modules within the carpel GRN, (3) analyze a case of convergent evolution in carpel development.
We will characterize the carpel development transcription factor interactomes of three genetically tractable model species, A. thaliana and the two basal eudicot species Eschscholzia californica and Aquilegia coerulea. While the gynoecium (sum of all carpels) of A. coerulea is structurally comparatively simple with four to six free carpels, A. thaliana and E. californica show similar, more derived carpel morphologies, both with two carpels fused fully along their margins. We will analyze phylogenies to identify candidate genes, carry out protein interaction analysis and use bioinformatics tools to identify and visualize protein interactions and their evolution. Gene function analysis in basal eudicot species will be carried out using Virus-Induced-Gene Silencing to infer the conservation of gene functions.
Using these combined approaches we will be able to identify common carpel GRN hubs that are essential for carpel morphology across the dicots. These hubs will, in the medium-term provide marker genes to improve yield in dicot crop plants.
Funding: 2016 – 2017, German Academic Exchange Service (DAAD)
Co-PI: Stefan de Folter, CINVESTAV-IPN, Irapuato, Mexico