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.
Seagrasses play a vital role in structuring coastal marine ecosystems, but their distributional range and genetic diversity have declined rapidly over the past decades. In order to improve conservation of seagrass species, it is important to predict how climate change may impact their ranges. Such predictions are typically made with correlative species distribution models (SDMs), which can estimate a species’ potential distribution under present and future climatic scenarios given species’ presence data and climatic predictor variables. However, these models are typically constructed with species-level data, and thus ignore intraspecific genetic variability of populations that potentially have adaptations to heterogeneous climatic conditions. Here, we explore the link between intraspecific adaptation and niche differentiation in Thalassia hemprichii, a seagrass broadly distributed in the tropical Indo-Pacific Ocean and a crucial provider of habitat for numerous marine species. Using microsatellite-based genotyping, we identified two distinct phylogeographical lineages within the nominal species and found an intermediate level of differentiation in their multidimensional environmental niches, suggesting the possibility for local adaptation. We then compared projections of the species’ habitat suitability under climate change scenarios using species-level and lineage-level SDMs. In the Central Tropical Indo-Pacific region, both models predicted considerable range contraction in the future, but the lineage-level model predicted more severe habitat loss. The two modelling approaches predicted opposite pattern in habitat change in the Western Tropical Indo-Pacific region. Our results highlight the necessity of conserving distinct populations and genetic pools under climate change and have important implications for guiding future management of seagrasses.
Photoinhibition is the popular topic in plant photosynthesis. However, restricted to experimental systems of in vitro membranes, knowledge of photosystem II (PSII) donor-side photoinhibition remains limited. Here, we report the first in vivo study of the mechanism in the marine higher plant Zostera marina. Preferential oxygen-evolving complex photoinactivation decreased the light-harvesting capacity and enhanced photosystem I cyclic electron flow (CEF). Non-photochemical quenching was inefficient and alternative electron flows, e.g. chlororespiration, Mehler reaction, malic acid synthesis, and photorespiration, remained unactivated, thereby reducing the unnecessary consumption of limited electron resources and maintaining a well carbon assimilation level. At variance with the PSII acceptor-side photoinhibition, the PSII photodamage of Z. marina was not attributed to 1O2 but was associated with the long-lived P680+ resulted from the photoinactivated OEC. Furthermore, we provided the novel insights into the PSII donor-side photoinhibition that rare PSII-CEF and ascorbate assumed photoprotective roles in Z. marina, which could donate electrons to the PSII reaction center to prevent the oxidative damage by P680+. This study addressed an important knowledge gap in PSII donor-side photoinhibition, providing a novel understanding of photosynthetic regulation mechanism responding to light stress.