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Spartina species of the mid-low intertidal areas are powerful ecological engineers that are highly valued where they are native. Elsewhere, they overgrow native salt marsh and open intertidal mudflats, diminish biota, increase costs of managing wildlife, and interfere with human uses of estuaries. Huge efforts have been mounted to kill some populations of invading Spartina. All large Spartina invasions are by S. densiflora (2n = 7x = 70) or S. alterniflora (2n = 6x = 62) or hybrids between the hexaploid species (2n = 6x). Hybridization is a recurrent theme in Spartina; the allododecaploid S. anglica (2n = 12x = 120) and the hybrid swarm in San Francisco Bay arose through the introductions of S. alterniflora into the range of native Spartina species. The ancient hybrid S. densiflora also hybridized with native Spartina species. Hybridization promotes the evolution of highly invasive populations and hampers control efforts. Whether Spartina, native and not, would protect the shore as sea levels rise depends upon unimpeded areas for upward marsh growth and sufficient sediment, conditions that are often not satisfied.

In many wetland plants, belowground transport of O2 via aerenchyma tissue and subsequent O2 loss across root surfaces generates small oxic root zones at depth in the rhizosphere with important consequences for carbon and nutrient cycling. This study demonstrates how roots of the intertidal salt-marsh plant Spartina anglica affect not only O2, but also pH and CO2 dynamics, resulting in distinct gradients of O2, pH, and CO2 in the rhizosphere. A novel planar optode system (VisiSens TD®, PreSens GmbH) was used for taking high-resolution 2D-images of the O2, pH, and CO2 distribution around roots during alternating light–dark cycles. Belowground sediment oxygenation was detected in the immediate vicinity of the roots, resulting in oxic root zones with a 1.7 mm radius from the root surface. CO2 accumulated around the roots, reaching a concentration up to threefold higher than the background concentration, and generally affected a larger area within a radius of 12.6 mm from the root surface. This contributed to a lowering of pH by 0.6 units around the roots. The O2, pH, and CO2 distribution was recorded on the same individual roots over diurnal light cycles in order to investigate the interlinkage between sediment oxygenation and CO2 and pH patterns. In the rhizosphere, oxic root zones showed higher oxygen concentrations during illumination of the aboveground biomass. In darkness, intraspecific differences were observed, where some plants maintained oxic root zones in darkness, while others did not. However, the temporal variation in sediment oxygenation was not reflected in the temporal variations of pH and CO2 around the roots, which were unaffected by changing light conditions at all times. This demonstrates that plant-mediated sediment oxygenation fueling microbial decomposition and chemical oxidation has limited impact on the dynamics of pH and CO2 in S. anglica rhizospheres, which may in turn be controlled by other processes such as root respiration and root exudation.

The cordgrass Spartina anglica C.E. Hubbard (Poaceae) is an invasive transformer in many salt marsh ecosystems worldwide. Relatively little is known about the capacity of Spartina to accelerate salt marsh succession and to protect salt marshes against sea level rise. We analyzed long-term changes in vegetation and elevation in mainland salt marshes of the European Wadden Sea in Schleswig-Holstein, Germany, to estimate the impact of non-native Spartina on the geomorphological resistance of salt marshes to sea level rise and on changes in species diversity. From 1989 to 2019, the Spartina-zone shifted and expanded upwards to elevations of the high marsh zone and Spartina increased in frequency in several salt marsh vegetation communities. At sites where Spartina dominated the vegetation already three decades ago, elevation and species diversity increased with a higher rate compared to sites lacking Spartina. The median change rates reached for elevation MHT +8.6 versus +1.5 mm per year, for species richness +3 versus ±0 species per three decades, and for evenness +0.04 versus −0.08 per three decades, regarding plots with versus without former Spartina dominance, respectively. Invasion of salt marshes by Spartina and its continued, long-term presence were associated with increased elevation and species diversity in the face of sea level rise.

Salt marshes provide wave and flow attenuation, making them attractive for coastal protection. It is necessary to predict their coastal protection capacity in the future, when climate change will increase hydrodynamic forcing and environmental parameters such as water temperature and CO 2 content. We exposed the European salt marsh species Spartina anglica and Elymus athericus to enhanced water temperature (+ 3°) and CO 2 (800 ppm) levels in a mesocosm experiment for 13 weeks in a full factorial design. Afterwards, the effect on biomechanic vegetation traits was assessed. These traits affect the interaction of vegetation with hydrodynamic forcing, forming the basis for wave and flow attenuation. Elymus athericus did not respond to any of the treatments suggesting that it is insensitive to such future climate changes. Spartina anglica showed an increase in diameter and flexural rigidity, while Young’s bending modulus and breaking force did not differ between treatments. Despite some differences between the future climate scenario and present conditions, all values lie within the natural trait ranges for the two species. Consequently, this mesocosm study suggests that the capacity of salt marshes to provide coastal protection is likely to remain constantly high and will only be affected by future changes in hydrodynamic forcing.

The organosulfur compound dimethylsulfoniopropionate (DMSP) has key roles in stress protection, global carbon and sulfur cycling, chemotaxis, and is a major source of climate-active gases. Saltmarshes are global hotspots for DMSP cycling due to Spartina cordgrasses that produce exceptionally high concentrations of DMSP. Here, in Spartina anglica , we identify the plant genes that underpin high-level DMSP synthesis: methionine S -methyltransferase ( MMT ), S -methylmethionine decarboxylase ( SDC ) and DMSP-amine oxidase ( DOX ). Homologs of these enzymes are common in plants, but differences in expression and catalytic efficiency explain why S. anglica accumulates such high DMSP concentrations and other plants only accumulate low concentrations. Furthermore, DMSP accumulation in S. anglica is consistent with DMSP having a role in oxidative and osmotic stress protection. Importantly, administration of DMSP by root uptake or over-expression of Spartina DMSP synthesis genes confers plant tolerance to salinity and drought offering a route for future bioengineering for sustainable crop production. Invasive Spartina grasses accumulate high levels of intracellular dimethylsulfoniopropionate (DMSP). Here, the authors report the isolation and characterization of the genes involved in DMSP biosynthesis and show that administration of DMSP by root uptake or overexpression of the DMSP biosynthesis genes results in salinity and drought tolerance in Arabidopsis.

Transposable elements (TE) induce structural and epigenetic alterations in their host genome, with major evolutionary implications. These alterations are examined here in the context of allopolyploid speciation, on the recently formed invasive species Spartina anglica, which represents an excellent model to contrast plant genome dynamics following hybridization and genome doubling in natural conditions. Methyl-sensitive transposon display was used to investigate the structural and epigenetic dynamics of TE insertion sites for several elements, and to contrast it with comparable genome-wide methyl-sensitive amplified polymorphism analyses. While no transposition burst was detected, we found evidence of major structural and CpG methylation changes in the vicinity of TE insertions accompanying hybridization, and to a lesser extent, genome doubling. Genomic alteration appeared preferentially in the maternal subgenome, and the environment of TEs was specifically affected by large maternal-specific methylation changes, demonstrating that TEs fuel epigenetic alterations at the merging of diverged genomes. Such genome changes indicate that nuclear incompatibilities in Spartina trigger immediate alterations, which are TE-specific with an important epigenetic component. Since most of this reorganization is conserved after genome doubling that produced a fertile invasive species, TEs certainly play a central role in the shock-induced dynamics of the genome during allopolyploid speciation.

Environmental contamination by xenobiotics represents a major threat for natural ecosystems and public health. In response, xenobiotic detoxification is a fundamental trait of organisms for developmental plasticity and stress tolerance, but the underlying molecular mechanisms remain poorly understood in plants. To decipher this process, we explored the consequences of allopolyploidy on xenobiotic tolerance in the genus Spartina Schreb. Specifically, we focused on microRNAs (miRNAs) owing to their central function in the regulation of gene expression patterns, including responses to stress. Small RNA-Seq was conducted on the parents S. alterniflora and S. maritima, their F1 hybrid S. x townsendii and the allopolyploid S. anglica under phenanthrene-induced stress (phe), a model Polycyclic Aromatic Hydrocarbon (PAH) compound. Differentially expressed miRNAs in response to phe were specifically identified within species. In complement, the respective impacts of hybridization and genome doubling were detected, through changes in miRNA expression patterns between S. x townsendii, S. anglica and the parents. The results support the impact of allopolyploidy in miRNA-guided regulation of plant response to phe. In total, we identified 17 phe-responsive miRNAs in Spartina among up-regulated MIR156 and down-regulated MIR159. We also describe novel phe-responsive miRNAs as putative Spartina-specific gene expression regulators in response to stress. Functional validation using Arabidopsis (L.) Heynh. T-DNA lines inserted in homologous MIR genes was performed, and the divergence of phe-responsive miRNA regulatory networks between Arabidopsis and Spartina was discussed.Key messagePhenanthrene-responsive microRNAs were identified in the context of allopolyploid speciation in Spartina. The results support the relative impacts of hybridization and genome doubling in miRNA-guided regulation mechanisms in response to xenobiotics.

Spartina anglica (hereafter Spartina) is an invasive perennial marsh grass shifting hydrodynamic regime and sediment characteristics in invaded area, thereby reducing macrobenthic diversity. There have been only a few studies focusing on the patch structure of Spartina according to size and its effects on macrofauna. A field experiment was conducted to identify effects of Spartina patches where they have been introduced no later than 5 years after invasion occurred on macrofauna assemblages in Ganghwa Island, South Korea. The survey area was divided into two sections according to vegetation: (1) Suaeda japonica vegetation from 0 to 60 m away from the levee, and (2) bare mudflat from 60 to 90 m away from the levee. The patch sizes of Spartina were categorized into small (1–4 m2), medium (5–11 m2), and large (13–40 m2) in area with four replicates for each section. The biomass ratio of the belowground and aboveground in the small size patch of Spartina was significantly higher than those in the medium and large size patch of Spartina. It indicated that more resource was allocated to rhizomes in small size patch with short invasion history (1 ~ 2 years). After Spartina invaded, macrofauna richness (70%), Shannon–Wiener diversity (80%), and density (67%) were decreased. However, infaunal deposit-feeding polychaete Perinereis linea and epifaunal gastropods Batillaria cumingi and Lactiforis takii increased by Spartina. Ordination of macroinvertebrate assemblages separated the habitat with Spartina invasion from the adjacent uninvaded tidal flat and Suaeda japonica habitats. This study offers a significant insight into early invasion strategies of an aggressive plant invader, Spartina for management of coastal wetlands and its impacts on macrofaunal assemblages.

Key MessageDifferential expression of mi-RNAs targeting developmental processes and progressive downregulation of repeat-associated siRNAs following genome merger and genome duplication in the context of allopolyploid speciation in Spartina.The role of small RNAs on gene expression regulation and genome stability is arousing increased interest and is being explored in various plant systems. In spite of prominence of reticulate evolution and polyploidy that affects the evolutionary history of all plant lineages, very few studies analysed RNAi mechanisms with this respect. Here, we explored small RNAs diversity and expression in the context of recent allopolyploid speciation, using the Spartina system, which offers a unique opportunity to explore the immediate changes following hybridization and genome duplication. Small RNA-Seq analyses were conducted on hexaploid parental species (S. alterniflora and S. maritima), their F1 hybrid S. x townsendii, and the neoallododecaploid S. anglica. We identified 594 miRNAs, 2197 miRNA-target genes, and 3730 repeat-associated siRNAs (mostly targeting Class I/Copia-Ivana- Copia-SIRE and LINEs elements). For both mi- and ra-siRNAs, we detected differential expression patterns following genome merger and genome duplication. These misregulations include non-additive expression of miRNAs in the F1 hybrid and additional changes in the allopolyploid targeting developmental processes. Expression of repeat-associated siRNAs indicates a strengthen of transposable element repression during the allopolyploidization process. Altogether, these results confirm the central role small RNAs play in shaping regulatory changes in naturally formed recent allopolyploids.

In this paper, we examine how the Spartina system has helped our understanding of the genomic aspects of allopolyploid speciation in the context of biological invasion. More specifically the respective roles of hybridization and genome duplication in the success of newly formed allopolyploid species are explored. Hybridization appears to have triggered genetic and epigenetic changes in the two recently formed European homoploid hybrids S. x towsendii and S. x neyrautii. Deviation from parental structural additivity is observed in both hybrids, with different patterns when considering transposable element insertions or AFLP and methylation alteration. No important changes are observed in the invasive allopolyploid Spartina anglica that inherited the identical genome to S. x townsendii. The repeated rRNA genes are not homogenized in the allopolyploid, and both parental repeats are expressed in the populations examined. Transcriptomic changes suggest possible gene silencing in both hybrids and allopolyploid. In the long-term of evolutionary time, older hexaploid Spartina species (Spartina alterniflora, Spartina maritima and Spartina foliosa) appear to have selectively retained differential homeologous copies of nuclear genes. Waxy gene genealogies suggest a hybrid (allopolyploid) origin of this hexaploid lineage of Spartina. Finally, nuclear and chloroplast DNA data indicate a reticulate origin (alloheptaploid) of the invasive Spartina densiflora. All together these studies stress hybridization as a primary stimulus in the invasive success of polyploid Spartina species.