Evolution of sexual reproduction in plants

Research during the past five years has delivered tremendous new insights into gamete physiology and the mechanisms involved in fertilization in Arabidopsis. This progress has established the view that gametes are hyper-differentiated cell types with highly specific transcriptional profiles. Advances in microscopy based on fluorescent reporters and live cell imaging have also transformed research capability and provided insights into the mechanisms involved in gamete delivery, interaction and the reprogramming of chromatin. Yet, our understanding of the complexity of double fertilization that characterises flowering plants is far from complete. Importantly, we lack any knowledge on the origin of mechanisms that predate double fertilization. Here, we propose to use emerging models, representing key stages in plant evolution, to provide insight into the ancestral mechanisms of gamete differentiation and fertilization. We will establish gene co-function networks by generating expression atlases for the liverwort Marchantia, the moss Physcomitrella and the extant basal flowering plant Amborella. These will be complemented with cofunction networks from Arabidopsis and the important crops maize, tomato and rice. The green alga Chlamydomonas will serve as an outgroup. These networks will be used to study the conservation of gene co-function networks governing male and female gametogenesis, pollen tube growth and fertilization mechanisms in flowering plants. Moreover, these investigations will provide novel molecular markers of fertility in crops. We aim to identify, for example, fertilization factors which were lost from ancient angiosperms during the evolution of monocots (grasses) and eudicots and those which have evolved de novo in the angiosperm lineage. We will also directly test the function of established regulators required for male gamete development, as well as those newly identified from our network analyses, to assess the extent of evolutionary conservation of these regulatory networks. The expected findings will allow the identification of specific mechanisms that are targeted by environmental stresses during sexual reproduction in crops and will assist in the selection of stressresistant cultivars. Finally, the reprogramming of chromatin modifications is an established feature of sexual reproduction in animals. Data generated in this project will provide the first comprehensive map of the occurrence of chromatin reprogramming in plant gametes and fertilization products. A better understanding of the epigenetic reprogramming events is pivotal for understanding transgenerational inheritance of epigenetic marks following exposure to biotic and abiotic stress and thus is an essential component for the improvement of crop productivity under environmental changes. In summary, the outputs of the EVOREPRO project will provide a deeper understanding of the evolution of sexual reproduction of economically important plant species.

The EVOREPRO project aim is to deliver the first comprehensive view of the molecular evolution of plant sexual reproduction and to provide insights into the origins of double fertilization in flowering plants. To this end the eight partner laboratories from Europe and the US are taking a comparative gene expression-based approach to investigate regulatory networks underlying sexual reproduction across a range of crop species of flowering plants and the model species Arabidopsis as well as the basal flowering plant Amborella, and two representative of basal land plants, Marchantia and Physcomitrella. These partners have identified novel key components involved in gamete development and fertilization processes such as germ cell division and specification, gamete interaction and activation. The Berger group has elucidated the evolutionary origin of sperm differentiation in the plant lineage and discovered a novel mechanism involved in chromatin re-programming of epigenetic information in male gametes. This knowledge will participate in overcoming fertilization barriers and enhancing crop productivity.