Linking gene expression to unilateral pollen-pistil reproductive barriers

CC-BY-NC-ND 4.0 International license peer-reviewed) is the author/funder. It is made available under a The copyright holder for this preprint (which was not. Abstract 1 Unilateral incompatibility (UI) is an asymmetric reproductive barrier that unidirectionally 2 prevents gene flow between species and/or populations. UI is characterized by a compatible 3 interaction between partners in one direction, but in the reciprocal cross fertilization fails, 4 generally due to pollen tube rejection by the pistil. Although UI has long been observed in 5 crosses between different species, the underlying molecular mechanisms are only beginning to 6 be characterized. The wild tomato relative Solanum habrochaites provides a unique study 7 system to investigate the molecular basis of this reproductive barrier, as populations within the 8 species exhibit both interspecific and interpopulation UI. Here we used a transcriptomic 9 approach to identify genes in both pollen and pistil tissues that may be probable key players in 10 UI. We confirmed UI at the pollen-pistil level between a self-incompatible population and a self-11 compatible population of S. habrochaites. A comparison of gene expression between pollinated 12 styles exhibiting the incompatibility response and unpollinated controls revealed only a small 13 number of differentially expressed transcripts. Many more differences in transcript profiles were 14 identified between UI-competent versus UI-compromised reproductive tissues. A number of 15 intriguing candidate genes were highly differentially expressed, including a putative pollen 16 arabinogalactan protein, a stylar Kunitz family protease inhibitor, and a stylar peptide hormone 17 Rapid Alkalinization Factor. Our data also provide transcriptomic evidence that fundamental 18 processes including reactive oxygen species signaling are likely key in UI pollen-pistil 19 interactions between both populations and species. Our transcriptomic analysis highlighted 20 specific genes, including those in ROS signaling pathways that warrant further study in 21 investigations of UI. To our knowledge, this is the first report to identify candidate genes 22 involved in unilateral barriers between populations of the same species. 23. CC-BY-NC-ND 4.0 International license peer-reviewed) is the author/funder. It is made available under a The copyright holder for this preprint (which was not .