Spartina alterniflora Loisel. J. Hered. ), Gulf of Mexico–Origins, Waters, and Biota. RESEARCH ARTICLE Open Access Transcriptome analysis of smooth cordgrass (Spartina alterniflora Loisel), a monocot halophyte, reveals candidate genes involved in its adaptation to salinity Renesh Bedre1†, Venkata Ramanarao Mangu1†, Subodh Srivastava2, Luis Eduardo Sanchez1,3 and Niranjan Baisakh1* Abstract Background: Soil salinity affects growth and yield of crop plants. Monospecific stands grow in low intertidal areas. invading the Pacific coast of the U.S. (Castillo et al., 2018). Hydrobiologia 745 (1), 313–327. Haplotype C2, C3, and C4 of Group C consisting of multiple haplotypes are shown in green, yellow, and pink, respectively, and other C members are shown in blue. “Ecological engineering of coastline with salt marsh plantations,” in Ecological Engineering: An Introduction to Eco-Technology. in Japan. Spartina versicolor Fabre: Another case of Spartina trans-Atlantic introduction? (2001). The reason was that the number of alleles per marker on each S. alterniflora population in Japan was less than and/or equal to 2 (Supplementary Table 2). YM, MT, and DH designed and coordinated the research. 2.9.3 (Goudet, 2001). In addition to the evidence based on genetic analyses, we assumed that countries or regions having high trade with Japan would be likely to become donor spots for spreading the invasive S. alterniflora irrespective of intentional/unintentional pathways. Images from the web. According to the cpDNA analysis, S. alterniflora populations in Japan had a single haplotype (haplotype C4) that is the most dominant genotype around the Florida Peninsula, the region of its origin, and is also widely found in the introduced populations in the East Asia. Scudder, G. G. E., Reveal, J. L. (Pittsburgh, PA: Carnegie–Mellon University), 351–363. Plant Sci. Principal coordinate analysis (PCoA) based on co-dominant genotypic distances revealed that genetic distances of S. alterniflora populations were clearly different between each studied river. (2013). Agric. Over the last 25 years, introduced species have spread rapidly, becoming established in numerous intertidal Spartina The findings revealed that when compared the amount of trade between the Yatsushiro Port (southern Kumamoto), which includes the Oono River and the U.S. ($51,869,672–$131,308,447) and the East Asian countries (China: $62,434,491–$106,800,742; Taiwan: $6,504–$13,843,516; Hong Kong: $0–$22,622), differences in the trade value with both countries were similar and/or slightly higher in the East Asian countries. Ecol. 4 (2), 359–361. Ministry of the Environment, Japan (2005). Spartina alterniflora . Three case studies for control of invasive alien ant species, fire ant (Solenopsis invicta, Formicidae) in Japan. Reconstructing a century of Spartina alterniflora invasion with historical records and contemporary remote sensing. (2009). This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). |, https://www.frontiersin.org/articles/10.3389/fpls.2020.556039/full#supplementary-material, http://www2.unil.ch/popgen/softwares/fstat.htm, https://www.env.go.jp/nature/intro/2outline/files/siteisyu_list_e.pdf, Creative Commons Attribution License (CC BY). Then, the genetic variance of S. alterniflora was compared between populations in the region of origin (the eastern U.S.) and those in several introduced regions (the Pacific coast of the U.S. and some East Asian countries). 0.6.93 (Earl and von Holdt, 2012), and then the K value with the highest ΔK was defined as the optimum number of clusters. Resour. Natl. 94 (3), 197–204. Spartina alterniflora Loisel. Impacts of invasive Iris pseudacorus L. (yellow flag) establishing in an abandoned urban pond on native semi-wetland vegetation. doi: 10.1093/molbev/mst197, Thompson, J. D., Higgins, D. G., Gibson, T. J. Ecol. Sci. Genotypic diversity enhances invasive ability of Spartina alterniflora. The ΔK value was clearly the highest at K = 3 (Figure 4A). 16 (4), 582–592. This value indicates the rate of genetic loci with polymorphisms compared to all the genetic loci for each local population. 28 (17), 4012–4027. is an accepted name This name is the accepted name of a species in the genus Spartina (family Poaceae). Unintentionally introduced species—the clam-eating moon snail Euspira fortunei. An alignment method, ClustalW (Thompson et al., 1994), in statistical software MEGA ver. B., Ainouche, M. L., Ayres, D., Bertness, M. D., et al. Discussion. Grass family (Poaceae) Download PDF version formatted for print (311 KB) **NOTE: Smooth cordgrass is native to coastal states of eastern and southern U.S. On the other hand, low g values were found in samples from the Shirakawa River (g = 0.33) and Guangdong province in China (g = 0.32), where almost all analyzed samples had the same genotype. We thank Dr. Francisco Sánchez-Bayo (The University of Sydney), Dr. Jean Beran Tanangonan, and Robert John Sheridan (Kindai University) for English editing of the original manuscript. For polymerase chain reaction (PCR) amplification and sequencing of the trnT–trnF region of cpDNA, two primer pairs were used: Tab A (5′-CAT TAC AAA TGC GAT GCT CT-3′) and Tab B (5′-TCT ACC GAT TTC GCC ATA TC-3′) targeting the trnT–trnL region; and Tab C (5′-CGA AAT CGG TAG ACG CTA CG-3′) and Tab F (5′-ATT TGA ACT GGT GAC ACG AG-3′) targeting the trnL–trnF region were used (Taberlet et al., 1991). In addition, no S. alterniflora population was found in Japan before 2008 (Tamaoki and Takizaki, 2015). Mol. The collected samples were naturally dried in our laboratory for genetic experiments. 2.3.4 (Pritchard et al., 2000) was used for this analysis. 25 (5), 425–444. 40 (2), 212–225. doi: 10.1371/journal.pone.0009743. doi: 10.1111/j.1365-294X.2004.02384.x, Pyšek, P., Richardson, D. M. (2010). Spartina anglica C.E. In addition, each group was practically unmixed with any other group. Grasping at the routes of biological invasions: a framework for integrating pathways into policy. Supporting Spartina: interdisciplinary perspective shows Spartina as a distinct solid genus. However, the degree of genetic diversity and differentiation of introduced populations obviously varies for each invasion event (e.g., Amsellem et al., 2000; McCauley et al., 2003; Provan et al., 2005). Since the cause of a lower genetic diversity among invasive Spartina species is of great interest, we discuss below the reason why S. alterniflora populations had lower genetic diversity when invading Japan. In this study, SPR3 was excluded from the analysis because no polymorphisms were detected across Japan’s local populations. Among invasive species, aquatic plants pose serious threats to local biodiversity and ecosystem functions. DC. ex Elliott) St.-Yves, Candollea 5: 24, 49 (1932) Spartina maritima subvar. Front. DOC Research & Development Series 292-42. B., et al. Luikart, G., Sherwin, W. B., Steele, B. M., Allendorf, F. W. (1998a). Spartina alterniflora can become an invasive plant, either by itself or by hybridizing with native species and interfering with the propagation of the pure native strain. To compare the chloroplast DNA (cpDNA) haplotypes of S. alterniflora between the United States (Blum et al., 2007; Bernik et al., 2016) and Japanese populations, firstly the haplotypes were identified for all the collected samples. Similar trend on the amount of trade with U.S. ($109,554,232–$326,703,330) and the East Asian countries (China: $127,673,513–$341,455,118; Taiwan: $1,471,897–$35,106,109; Hong Kong: $0–$1,937,044) was observed at Mikawa Port (Aichi) including the Umeda River. Simenstad, C. A., Thom, R. M. (1995). In particular, we hypothesized that there was a high possibility of “secondary introduction” from China since many biological invaders such as Solenopsis invicta Buren (fire ant) and Limnoperna fortunei Dunker (golden mussel) invaded Japan associated with recent vigorous trade with China (e.g., Magara et al., 2001; Murakami, 2018). The forward primer was fluorescently labeled with 5′-FAM, TAMRA, and 5′-JOE. Spartina alterniflora Loisel. On the other hand, populations of this species in the San Francisco Bay, California, and China, which were introduced intentionally, had a relatively high genetic diversity (Blum et al., 2007; Bernik et al., 2016). Based on the microsatellite analysis, individuals which had an exact genotype match were considered as “clones” and then were excluded from the analyses. Austral Ecol. Similarly, S. alterniflora in the western U.S. was also introduced unintentionally from the eastern U.S. when Crassostrea virginica Gmelin seedlings were imported for cultivation (Civille et al., 2005). The DNA sequences of the trnT–trnL and trnL–trnF were combined into a sequence, which was designated as the trnT–trnF. (New York, NY: Wiley & Sons), 255–289. 14 (1), 189–194. Baisakh N(1), Subudhi PK, Varadwaj P. Author information: (1)School of Plant, Environmental and Soil Sciences, Louisiana State University Agricultural Center, Baton Rouge, LA 70803, USA. Projects: China, IPCN, New World Grasses, PAPGI Common Names: hu hua mi cao No References available Smooth cordgrass (English, United States) Hitchcock, A. doi: 10.1046/j.1365-294x.1998.00414.x, Luikart, G., Allendorf, F. W., Cornuet, J.-M., Sherwin, W. B. Spartina alterniflora Loisel. Nevertheless, it suggests that only one S. alterniflora strain or a few individuals with the same genotype might have introduced into each Japanese river at separate timings. in Japanese with English Abstract. Mol. Resour. Information on the origin and invasion history of each invasive species is essential for preventing its further spread successfully (Schaal et al., 2003). Mol. (2019). Accordingly, Spartina anglica C.E. Proc. (2018). doi: 10.1007/s10530-016-1128-z, Bernik, B. M., Li, H., Blum, M. J. Plant Symbol = SPAL. Ecology 100 (11), e02863. Texas A&M Press, College Station, Texas. Proc. Ecol. Invasion of the non-indigenous nuisance mussel, Limnoperna fortunei, into water supply facilities in Japan. Rates of change in the numbers of dunlin, Calidris alpina, wintering in British estuaries in relation to the spread of Spartina anglica. (2004). Two additional monosaccharides were found but were not identified. doi: 10.6165/tai.2009.54(2).168. This plant has no children Legal Status. 89 (3), 238–247. Also, Blum et al. Alaska Spartina Prevention, Detection and Response Plan (Juneau, AK: National Marine Fisheries Service Alaska Region). Primary responses to salt stress in a halophyte, smooth cordgrass (Spartina alterniflora Loisel.). Some like it hot: maternal-switching with climate change modifies formation of invasive Spartina hybrids. Saccaggi, D. L., Karsten, M., Robertson, M. P., Kumschick, S., Somers, M. J., Wilson, J. R. U., et al. Characterization of microsatellite loci in Spartina species (Poaceae). Bioinformatics 28 (19), 2537–2539. A global assessment of invasive plant impacts on resident species, communities and ecosystems: the interaction of impact measures, invading species’ traits and environment. Results of the microsatellite analysis made it clear that some S. alterniflora individuals (St. 13, 15, 16, and 18) in the Tsuboi River (northern Kumamoto) had a heterozygous at only one locus, while two individuals growing sympatrically (St. 14 and 17) had a homozygous at all of the loci (Supplementary Table 2). Lockwood, J. L., Hoopes, M. F., Marchetti, M. P. (2007). Invasion significantly shifts soil bacterial communities with the successional gradient of saltmarsh in eastern China March 2020 Therefore, it is important to strengthen the quarantine control on the importation of commodities, especially of transport vehicles at potential donor spots (i.e., border control/border biosecurity system), and to share information networks on invasive species between each region/port for minimizing further risks of biological species such as Spartina. The PCR amplification was performed using a TaKaRa PCR Thermal Cycler (TaKaRa Bio, Shiga, Japan) at 95°C for 30 s, 55°C for 30 s (65°C for 30 s only for SPR4), 72°C for 90 s, and 72°C for 25 min as the last elongation step. Acad. 17 (8), 1881–1887. 47 (3), 183–191. Table 2 Bottleneck analysis of Spartina alterniflora populations in Japan using three models: IAM, SMM, and TPM. Natl. The principal coordinate analysis and The STRUCTURE analysis indicated that no gene mixing among Japanese local populations (Aichi, northern and southern Kumamoto) was observed, indicating that Spartina invasion occurred independently into these regions. Plants (Embryophyta) of the Gulf of Mexico, Pp. Thus, to validate this hypothesis, trade histories were compared between countries/regions where S. alterniflora has grown (the United States, China, Taiwan, Hong Kong) (Blum et al., 2007; Guo et al., 2015; Bernik et al., 2016) and the ports nearest to each studied river in Japan (i.e., Kumamoto Port, Yatsushiro Port, and Mikawa Port) using historical trade data from the 2003 to 2013 in the Global Trade Atlas (https://www.gtis.com/gta/). Mitsch, W. J., Jorgensen, S. A. (2016). 8 (10), 4992–5007. The polymorphic locus rate (P) was calculated for each local population. 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The number of clusters of individuals using the site alterniflora might have successfully invaded Japan Atlantic coast of the.! The rate of the trnT–trnL and trnL–trnF were combined into a sequence which! Few polymorphic loci, reveal, J. D. ( 2002 ) was carried out following method. Relationship to salt marsh plantations, ” in ecological engineering of coastline with marsh..., ClustalW ( Thompson et al., 2018 ) of marsh plants,!