Invasive species can successfully and rapidly colonize new niches and expand ranges via founder effects and enhanced tolerance towards environmental stresses. However, the underpinning molecular mechanisms (i.e., gene expression changes) facilitating rapid adaptation to harsh environments are still poorly understood. The red seaweed Gracilaria vermiculophylla, which is native to the northwest Pacific but invaded North American and European coastal habitats over the last 100 years, provides an excellent model to examine whether enhanced tolerance at the level of gene expression contributed to its invasion success. We collected G. vermiculophylla from its native range in Japan and from two non-native regions along the Delmarva Peninsula (Eastern United States) and in Germany. Thalli were reared in a common garden for four months at which time we performed comparative transcriptome (mRNA) and microRNA (miRNA) sequencing. MRNA-expression profiling identified 59 genes that were differently expressed between native and non-native thalli. Of these genes, most were involved in metabolic pathways, including photosynthesis, abiotic stress, and biosynthesis of products and hormones in all four non-native sites. MiRNA-based target-gene correlation analysis in native/non-native pairs revealed that some target genes are positively or negatively regulated via epigenetic mechanisms. Importantly, these genes are mostly associated with metabolism and defense capability. Thus, our gene expression results indicate that resource reallocation to metabolic processes is most likely a predominant mechanism contributing to the range-wide persistence and adaptation of G. vermiculophylla in the invaded range. This study therefore provides a novel molecular insight into the speed and nature of invasion-mediated rapid adaption.

Zostera marina among seagrass suffering from global decline is a representative species in temperate regions in the Northern Hemisphere. Given our recent findings, the decline of seagrasses may be associated with the photosensitivity of the oxygen-evolving complex (OEC). Therefore, understanding the mechanism of OEC photosensitivity is key to understanding the continued decline in seagrasses. Herein, we explored the screening-based photoprotection function in Z. marina by examining the inactivation spectrum of OEC and the differences in photoresponse pathways following exposure to different spectrums. The OEC inactivation was spectral-dependent. High-energy light significantly reduced the PSII performance, OEC peripheral protein expression, and photosynthetic O 2 release capacity. The increased synthesis of carotenoids under blue light with severe OEC damage implied its weak photoprotection property in Z. marina. However, anthocyanins key synthetic genes were lowly expressed with inefficient accumulation under high-energy light. Furthermore, the acylation modifications of anthocyanins, especially aromatic acylation modifications were insufficient, leading to poor stability and light absorption of anthocyanins. Based on the role of blue light receptors in regulating the synthesis of anthocyanins in vascular plant, we hypothesized that the absence of blue light receptor CRY2 in Z. marina causes the insufficient synthesis of anthocyanins and acyl modifications, reducing the shielding against high-energy light, subsequently causing OEC photoinactivation.