Development of chloroplast simple sequence repeats (cpSSRs) for the intraspecific study of Gracilaria tenuistipitata (Gracilariales, Rhodophyta) from different populations

BMC Research Notes

Anchana Prathep²  Dang Diem Hong⁴  Weng-Wah Lee³  Siew-Moi Phang¹  Phaik-Eem Lim¹  Sze-Looi Song¹ 

[1] Institute of Ocean and Earth Sciences (IOES), University of Malaya, 50603 Kuala Lumpur, Malaysia;Seaweed and Seagrass Research Unit, Excellence Centre for Biodiversity of Peninsular Thailand, Department of Biology, Faculty of Science, Prince of Songkla University, HatYai, Songkhla 90112, Thailand;ACGT Laboratories, Lot L3-I-1, Enterprise 4, Technology Park Malaysia, Bukit Jalil, 57000 Kuala Lumpur, Malaysia;Algal Biotechnology Department, Institute of Biotechnology (IBT), Vietnamese Academy of Science and Technology (VAST), Hanoi, Vietnam

关键词: Rhodophyta;    Haplotype;    Genetic analysis;    cpSSRs;   

Others  :  1134601
DOI  :  10.1186/1756-0500-7-77

 received in 2013-10-17, accepted in 2014-01-14,  发布年份 2014

【 摘 要 】

Background

Gracilaria tenuistipitata is an agarophyte with substantial economic potential because of its high growth rate and tolerance to a wide range of environment factors. This red seaweed is intensively cultured in China for the production of agar and fodder for abalone. Microsatellite markers were developed from the chloroplast genome of G. tenuistipitata var. liui to differentiate G. tenuistipitata obtained from six different localities: four from Peninsular Malaysia, one from Thailand and one from Vietnam. Eighty G. tenuistipitata specimens were analyzed using eight simple sequence repeat (SSR) primer-pairs that we developed for polymerase chain reaction (PCR) amplification.

Findings

Five mononucleotide primer-pairs and one trinucleotide primer-pair exhibited monomorphic alleles, whereas the other two primer-pairs separated the G. tenuistipitata specimens into two main clades. G. tenuistipitata from Thailand and Vietnam were grouped into one clade, and the populations from Batu Laut, Middle Banks and Kuah (Malaysia) were grouped into another clade. The combined dataset of these two primer-pairs separated G. tenuistipitata obtained from Kelantan, Malaysia from that obtained from other localities.

Conclusions

Based on the variations in repeated nucleotides of microsatellite markers, our results suggested that the populations of G. tenuistipitata were distributed into two main geographical regions: (i) populations in the west coast of Peninsular Malaysia and (ii) populations facing the South China Sea. The correct identification of G. tenuistipitata strains with traits of high economic potential will be advantageous for the mass cultivation of seaweeds.

【 授权许可】

   
2014 Song et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

【 参考文献 】

• [1]Chang CF, Xia BM: On two new Gracilaria (Gigartinales, Rhodophyta) from South China. Taxonomy of economic seaweeds with reference to some Pacific and Caribbean species 1988, 2:127-129.
• [2]Terada R, Kawaguchi S, Masuda M, Phang SM: Taxonomic notes on marine algae from Malaysia. III. Seven species of Rhodophyceae. Bot Mar 2000, 43:347-357.
• [3]Chiang YM, Lin JL: Nitrate uptake by nitrogen-starved plants of the red alga Gracilaria tenuistipitata var. liui. Jpn J Phycol 1989, 37:187-193.
• [4]Lin M-C, Liao C-M: 65Zn(II) accumulation in the soft tissue and shell of abalone Haliotis diversicolor supertexta via the alga Gracilaria tenuistipitata var. liui and the ambient water. Aquaculture 1999, 178:89-101.
• [5]Collén J, Pinto E, Pedersén M, Colepicolo P: Induction of oxidative stress in the red macroalga Gracilaria tenuistipitata by pollutant metals. Arch Environ Contam Toxicol 2003, 45:337-342.
• [6]Lee TM, Chang YC, Lin YH: Differences in physiological responses between winter and summer Gracilaria tenuistipitata (Gigartinales, Rhodophyta) to varying temperature. Bot Bul Acad Sin 1999, 40:93-100.
• [7]Oliveira EC, Alveal K: Introduction to applied phycology. In The mariculture of Gracilaria (Rhodophyta) for the production of agar. Edited by Akatsuka I. The Hague: SPB Academic Publishing; 1990:553-564.
• [8]Nguyen HD: Vietnamese species of Gracilaria and Gracilariopsis. In Taxonomy of economic Seaweeds. Edited by Abbott IA. La Jolla, California: California Sea Grant College; 1992:207-210. vol. 3
• [9]Tseng CK, Xia BM: On the Gracilaria in the western Pacific and Southeastern Asia region. Bot Mar 1999, 42:209-217.
• [10]Tsutsui I, Huynh QN, Nguyên HD, Arai S, Yoshida T: The common marine plants of southern Vietnam. Numerous colour photographs Usa: Japan Seaweed Association 2005, 251:1-250.
• [11]Lewmanomont K: The species of Gracilaria from Thailand. In Taxonomy of Economic Seaweeds. Edited by Abbott IA. La Jolla, California: California Sea Grant College Program; 1994:135-148. vol. 4
• [12]Abbott IA: New Records and a Reassessment of Gracilaria (Rhodophyta) from the Philippines. In Taxonomy of Economic Seaweeds with Reference to some Pacific Species. Edited by Abbott IA. California: California Sea Grant College; 1994:111-118.
• [13]Lim PE, Phang SM: Gracilaria species (Gracilariales, Rhodophyta) of Malaysia including two new records. Malays J Sci 2004, 23:71-80.
• [14]Phang SM: Seaweed resources in Malaysia: current status and future prospects. Aquat Ecosyst Health Manag 2006, 9:185-202.
• [15]Wattier R, Maggs CA: Intraspecific variation in seaweeds: the application of new tools and approaches. Adv Bot Res 2001, 35:171-212.
• [16]O’Brien SJ, Menotti-Raymond M, Murphy WJ, Nash WG, Wienberg J, Stanyon R, Copeland NG, Jenkins NA, Womack JE, Marshall Graves JA: The promise of comparative genomics in mammals. Science 1999, 286:458-481.
• [17]Lim PE, Wong CL, Phang SM: Molecular taxonomy of seaweeds with emphasis on Rhodophyta and Phaeophyta. In Advances in Seaweed Cultivation and Utilization in Asia. Edited by Phang SM, Critchley AT, Ang POJr. Kuala Lumpur: University of Malaya Maritime Research Center Publication; 2006:105-142.
• [18]Powell W, Machray GC, Provan J: Polymorphism revealed by simple sequence repeats. Trends Plant Sci 1996, 1:215-222.
• [19]Rafalski A, Vogel MJ, Morgante M, Powell W, Andre C, Tingey SV: Generating and using DNA markers in plants. In Non-mammalian genome analysis: a practical guide. Edited by Biren B, Lai E. London: Academic Press; 1996:75-134.
• [20]Sun JW, Jin MD, Zhou CJ, Yang QK, Weng ML, Duan LD, Xu P, Ma JH, Wang B: Identification of Porphyra lines (Rhodophyta) by AFLP DNA fingerprinting and molecular markers. Plant Mol Biol Report 2005, 23:251-262.
• [21]Pang Q, Sui Z, Kang KH, Kong F, Zhang X: Application of SSR and AFLP to the analysis of genetic diversity in Gracilariopsis lemaneiformis (Rhodophyta). J Appl Phycol 2010, 22:607-612.
• [22]Kostamo K, Blomster J, Korpelainen H, Kelly J, Maggs CA, Mineur F: New microsatellite markers for Ulva Intestinalis (Chlorophyta) and the transferability of markers across species of Ulvaceae. Phycologia 2008, 47:580-587.
• [23]Liu F, Wang X, Yao J, Fu W, Duan D: Development of expressed sequence tag-derived microsatellite markers for Saccharina (Laminaria) japonica. J Appl Phycol 2010, 22:109-111.
• [24]Eujayl I, Sledge MK, Wang L, May GD, Chekhovskiy K, Zwonitzer JC, Mian MA: Medicago truncatula EST-SSRs reveal cross-species genetic markers for Medicago spp. Theor Appl Genet 2004, 108(3):414-422.
• [25]Kantety RV, la Rota M, Matthews DE, Sorrells ME: Data mining for simple-sequence repeats in expressed sequence tags from barley, maize, rice, sorghum, and wheat. Plant Mol Biol 2002, 48:501-510.
• [26]Varshney RK, Thiel T, Stein N, Langridge P, Graner A: In silico analysis on frequency and distribution of microsatellites in ESTs of some cereal species. Cell Mol Biol Lett 2002, 7:537-546.
• [27]Yu J-K, Dake TM, Singh S, Benscher D, Li W, Gill B, Sorrells ME: Development and mapping of EST-derived simple sequence repeat markers for hexaploid wheat. Genome 2004, 47:805-818.
• [28]Wang ML, Mosjidis JA, Morris JB, Chen ZB, Barkley NA, Pederson GA: Evaluation of Lespedeza germplasm genetic diversity and its phylogenetic relationship with the genus Kummerowia. Conserv Genet 2008, 10:79-85.
• [29]Wattier R, Dallas JF, Destombe C, Saumitou-Laprade P, Valero M: Single locus microsatellites in Gracilariales (Rhodophyta): high level of genetic variability within Gracilaria gracilis and conservation in related species. J Phycol 1997, 33:868-880.
• [30]Xie C-T, Chen C-S, Ji D-H, Xu Y: Characterization, development and exploitation of EST-derived microsatellites in Porphyra haitanensis Chang and Zheng (Bangiales, Rhodophyta). J Appl Phycol 2008, 21:367-374.
• [31]Voisin M, Engel CR, Viard F: Differential shuffling of native genetic diversity across introduced regions in a brown alga: aquaculture vs. maritime traffic effects. Proc Natl Acad Sci USA 2005, 102:5432-5437.
• [32]Sun J, Liu T, Guo B, Jin D, Weng M, Feng Y, Xu P, Duan D, Wang B: Development of SSR primers from EST sequences and their application in germplasm identification of Porphyra lines (Rhodophyta). Eur J Phycol 2006, 41:329-336.
• [33]Andreakis N, Kooistra WHCF, Procaccini G: Microsatellite markers in an invasive strain of Asparagopsis taxiformis (Bonnemaisoniales, Rhodophyta): insights in ploidy level and sexual reproduction. Gene 2007, 406:144-151.
• [34]Provan J, Maggs CA: Unique genetic variation at a species’ rear edge is under threat from global climate change. Proc R Soc B 2012, 279:39-47.
• [35]Lim PE, Thong KL, Phang SM: Molecular differentiation of two morphological variants of Gracilaria salicornia. J Appl Phycol 2001, 13:335-342.
• [36]Sim MC, Lim PE, Gan SY, Phang SM: Identification of random amplified polymorphic DNA (RAPD) marker for differentiating male from female and sporophytic thalli of Gracilaria changii (Rhodophyta). J Appl Phycol 2007, 19:763-769.
• [37]Yow Y-Y, Lim P-E, Phang S-M: Genetic diversity of Gracilaria changii (Gracilariaceae, Rhodophyta) from west coast, Peninsular Malaysia based on mitochondrial cox1 gene analysis. J Appl Phycol 2011, 23:219-226.
• [38]Teo SS, Ho CL, Teoh S, Lee WW, Tee JM, Rahim RA, Phang SM: Analyses of expressed sequence tags (ESTs) from an agarophyte, Gracilaria changii (Gracilariales, Rhodophyta). Eur J Phycol 2007, 42:41-46.
• [39]Wong TKM, Ho CL, Lee WW, Rahim RA, Phang SM: Analyses of expressed sequence tags (ESTs) from Sargassum binderi (Phaeophyta). J Phycol 2007, 43:528-534.
• [40]Zuccarello GC, Burger G, West JA, King RJ: A mitochondrial marker for red algal intraspecific relationships. Mol Ecol 1999, 8:1443-1447.
• [41]Reith M, Munholland J: Complete nucleotide sequence of the Porphyra purpurea chloroplast genome. Plant Mol Biol Report 1995, 13:333-335.
• [42]Burger G, Saint-Louis D, Gray MW, Lang BF: Complete sequence of the Mitochondrial DNA of the red Alga Porphyra Purpurea: cyanobacterial Introns and shared ancestry of red and green Algae. Plant Cell 1999, 11:1675-1694.
• [43]Leblanc C, Boyen C, Richard O, Bonnard G, Grienenberger J-M, Kloareg B: Complete sequence of the mitochondrial DNA of the rhodophyte Chondrus crispus (Gigartinales). Gene content and genome organization. J Mol Biol 1995, 250:484-495.
• [44]Hagopian JC, Reis M, Kitajima JP, Bhattacharya D, de Oliveira MC: Comparative analysis of the complete plastid genome sequence of the red alga Gracilaria tenuistipitata var. liui provides insights into the evolution of rhodoplasts and their relationship to other plastids. J Mol Evol 2004, 59:464-477.
• [45]Barufi JB, Cabral de Oliveira E, Plastino EM, Cabral de Oliveira M: Life history, morphological variability and growth rates of the life phases of Gracilaria tenuistipitata (Rhodophyta: Gracilariales) in vitro. Sci Mar 2010, 74:297-303.
• [46]Takahashi MM: Sequênciamento e análise do genoma mitocondrial de Gracilaria tenuistipitata (Gracilariales, Rhodophyta). Brazil: University of São Paulo, Institute of Biosciences; 2010. [Master Thesis]
• [47]Collén PN, Collén J, Reis MS, Pedersen M, Setubal JC, Varani AM, Colepicolo P, Oliveira MC: Analysis of expressed sequence tags from the agarophyte Gracilaria tenuistipitata (Rhodophyta). J Appl Phycol 2011, 24:1-7.
• [48]Chung S-M, Staub JE: The development and evaluation of consensus chloroplast primer pairs that possess highly variable sequence regions in a diverse array of plant taxa. Theor Appl Genet 2003, 107:757-767.
• [49]Provan J, Biss PM, McMeel D, Mathews S: Universal primers for the amplification of chloroplast microsatellites in grasses (Poaceae). Mol Ecol Notes 2004, 4:262-264.
• [50]Cheng YJ, Meng HJ, Guo WW, Deng XX: Universal chloroplast primer pairs for simple sequence repeat analysis in diverse genera of fruit crops. J Hortic Sci Biotechnol 2006, 81:132-138.
• [51]Provan J, Murphy S, Maggs C: Universal plastid primers for Chlorophyta and Rhodophyta. Eur J Phycol 2004, 39:43-50.
• [52]Rozen S, Skaletsky HJ: Primer3 on the WWW for general users and for biologist programmers. In Bioinformatics methods and protocols: methods in molecular biology: 2000. Totowa, NJ: Humana Press; 2000:365-386.
• [53]Hepperle D: Fingerprinter©. a software for the analysis, bin-assignment and 01-matrix construction of molecular fingerprints (AFLPs). 2002. Win32-Version Distributed by the author via: http://science.do-mix.de/ webcite
• [54]Hepperle D: TreeMe©. a software for visualization, manipulation, layouting and labelling of phylogenetic trees. 2004. Win32-Version Distributed by the author via: http://www.sequentix.de/ webcite
• [55]Hall TA: BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 1999, 41:95-98.
• [56]Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG: The Clustal X windows interface: flexible stratrgies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 1997, 24:4876-4882.
• [57]Ebert D, Peakall ROD: Chloroplast simple sequence repeats (cpSSRs): technical resources and recommendations for expanding cpSSR discovery and applications to a wide array of plant species. Mol Ecol Resour 2009, 9:673-690.
• [58]Powell W, Morgante M, Andre C, McNicol J, Machray G, Doyle J, Tingey S, Rafalski J: Hypervariable microsatellites provide a general source of polymorphic DNA markers for the Chloroplast genome. Curr Biol 1995, 5:1023-1029.
• [59]Powell W, Morgante M, McDevitt R, Vendramin G, Rafalski J: Polymorphic simple sequence repeat regions in chloroplast genomes: applications to the population genetics of pines. Proc Natl Acad Sci USA 1995, 92:7759-7763.
• [60]Provan J, Powell W, Hollingsworth P: Chloroplast microsatellites: new tools for studies in plant ecology and evolution. Trends Ecol Evol 2001, 16:142-147.
• [61]Ellis JR, Burke JM: EST-SSRs as a resource for population genetic analyses. Heredity 2007, 99:125-132.
• [62]Fao: The state of world fisheries and aquaculture 2000. 2001. Electronic edition, http://fao.org
• [63]Chan CX, Ho CL, Phang SM: Trends in seaweed research. Trends Plant Sci 2006, 11:165-166.
• [64]Cho YG, Ishii T, Temnykh S, Chen X, Lipovich L, McCouch SR, Park WD, Ayres N, Cartinhour S: Diversity of microsatellites derived from genomic libraries and GenBank sequences in rice (Oryza sativa L.). Theor Appl Genet 2000, 100:713-722.
• [65]Temnykh S, Park WD, Ayres N, Cartinhour S, Hauck N, Lipovich L, Cho YG, Ishii T, McCouch SR: Mapping and genome organization of microsatellite sequences in rice (Oryza sativa L.). Theor Appl Genet 1999, 100:697-712.
• [66]Eujayl I, Sorrells M, Baum M, Wolters P, Powell W: Assessment of genotypic variation among cultivated durum wheat based on EST-SSRS and genomic SSRS. Euphytica 2001, 119:39-43.
• [67]Robinson AJ, Love CG, Batley J, Barker G, Edwards D: Simple sequence repeat marker loci discovery using SSR primer. Bioinformatics 2004, 20:1475-1476.
• [68]Morgante M, Olivieri AM: PCR-amplified microsatellites as markers in plant genetics. Plant J 1993, 3:175-182.
• [69]Wang Z, Weber JL, Zhong G, Tanksley SD: Survey of plant short tandem DNA repeats. Theor Appl Genet 1994, 88:1-6.
• [70]Cardlea L, Ramsaya L, Milbournea D, Macaulaya M, Marshalla D, Waugha R: Computational and experimental characterization of physically clustered simple sequence repeats in plants. Genetics 2000, 156:847-854.
• [71]Schaal BA, Hayworth DA, Olsen KM, Rauscher JT, Smith WA: Phylogeographic studies in plants: problems and prospects. Mol Ecol 1998, 7:465-474.
• [72]McCauley DE: The use of chloroplast DNA polymorphism in studies of gene flow in plants. Trends Ecol Evol 1995, 10:198-202.
• [73]Petit RJ, Duminil J, Fineschi S, Hampe A, Salvini D, Vendramin G: Comparative organization of chloroplast, mitochondrial and nuclear diversity in plant populations. Mol Ecol 2005, 14:689-701.