Abstract
BackgroundUnilateral incompatibility (UI) is an asymmetric reproductive barrier that unidirectionally prevents gene flow between species and/or populations. UI is characterized by a compatible interaction between partners in one direction, but in the reciprocal cross fertilization fails, generally due to pollen tube rejection by the pistil. Although UI has long been observed in crosses between different species, the underlying molecular mechanisms are only beginning to be characterized. The wild tomato relative Solanum habrochaites provides a unique study system to investigate the molecular basis of this reproductive barrier, as populations within the species exhibit both interspecific and interpopulation UI. Here we utilized a transcriptomic approach to identify genes in both pollen and pistil tissues that may be key players in UI.ResultsWe confirmed UI at the pollen-pistil level between a self-incompatible population and a self-compatible population of S. habrochaites. A comparison of gene expression between pollinated styles exhibiting the incompatibility response and unpollinated controls revealed only a small number of differentially expressed transcripts. Many more differences in transcript profiles were identified between UI-competent versus UI-compromised reproductive tissues. A number of intriguing candidate genes were highly differentially expressed, including a putative pollen arabinogalactan protein, a stylar Kunitz family protease inhibitor, and a stylar peptide hormone Rapid ALkalinization Factor. Our data also provide transcriptomic evidence that fundamental processes including reactive oxygen species (ROS) signaling are likely key in UI pollen-pistil interactions between both populations and species.ConclusionsGene expression analysis of reproductive tissues allowed us to better understand the molecular basis of interpopulation incompatibility at the level of pollen-pistil interactions. Our transcriptomic analysis highlighted specific genes, including those in ROS signaling pathways that warrant further study in investigations of UI. To our knowledge, this is the first report to identify candidate genes involved in unilateral barriers between populations within a species.
Highlights
Unilateral incompatibility (UI) is an asymmetric reproductive barrier that unidirectionally prevents gene flow between species and/or populations
Pollen-pistil interactions in SI LA1777 and SC LA0407 Using pollen tube growth assays, we confirmed that all LA1777 (SI) individuals used in RNA-seq experiments rejected both self-pollen tubes and those of LA0407, but accepted pollen from other LA1777 individuals
We confirmed that each LA0407 (SC) individual accepted pollen tubes from LA1777, self, and intrapopulation crosses
Summary
Unilateral incompatibility (UI) is an asymmetric reproductive barrier that unidirectionally prevents gene flow between species and/or populations. The unidirectionality of UI in crosses between species has been linked to plant mating system and to the self-incompatibility response. Distinct from the sporophytic SI of the Brassicaseae in which pollen is rejected at the stigma surface [13, 14], in gametophytic SI growing pollen tubes are actively rejected within the style [11, 15,16,17] This type of S-RNase-based SI is genetically determined by the polymorphic S-locus, which harbors pistil- (S-RNase) and pollen- (S-locus Fbox) expressed factors that are required for the specificity of the SI response [18,19,20,21]. These include pistil-expressed HT-proteins and 120 K glycoproteins [22,23,24], as well as pollen-expressed components of the E3 ubiquitin ligase complex (Cullin and SKP1) [15, 25,26,27,28,29]
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