Developing molecular tools and insights into the Penstemon genome using genomic reduction and next-generation sequencing
Tóm tắt
Penstemon’s unique phenotypic diversity, hardiness, and drought-tolerance give it great potential for the xeric landscaping industry. Molecular markers will accelerate the breeding and domestication of drought tolerant Penstemon cultivars by, creating genetic maps, and clarifying of phylogenetic relationships. Our objectives were to identify and validate interspecific molecular markers from four diverse Penstemon species in order to gain specific insights into the Penstemon genome. We used a 454 pyrosequencing and GR-RSC (genome reduction using restriction site conservation) to identify homologous loci across four Penstemon species (P. cyananthus, P. davidsonii, P. dissectus, and P. fruticosus) representing three diverse subgenera with considerable genome size variation. From these genomic data, we identified 133 unique interspecific markers containing SSRs and INDELs of which 51 produced viable PCR-based markers. These markers produced simple banding patterns in 90% of the species × marker interactions (~84% were polymorphic). Twelve of the markers were tested across 93, mostly xeric, Penstemon taxa (72 species), of which ~98% produced reproducible marker data. Additionally, we identified an average of one SNP per 2,890 bp per species and one per 97 bp between any two apparent homologous sequences from the four source species. We selected 192 homologous sequences, meeting stringent parameters, to create SNP markers. Of these, 75 demonstrated repeatable polymorphic marker functionality across the four sequence source species. Finally, sequence analysis indicated that repetitive elements were approximately 70% more prevalent in the P. cyananthus genome, the largest genome in the study, than in the smallest genome surveyed (P. dissectus). We demonstrated the utility of GR-RSC to identify homologous loci across related Penstemon taxa. Though PCR primer regions were conserved across a broadly sampled survey of Penstemon species (93 taxa), DNA sequence within these amplicons (12 SSR/INDEL markers) was highly diverse. With the continued decline in next-generation sequencing costs, it will soon be feasible to use genomic reduction techniques to simultaneously sequence thousands of homologous loci across dozens of Penstemon species. Such efforts will greatly facilitate our understanding of the phylogenetic structure within this important drought tolerant genus. In the interim, this study identified thousands of SNPs and over 50 SSRs/INDELs which should provide a foundation for future Penstemon phylogenetic studies and breeding efforts.
Tài liệu tham khảo
St Hilaire R, Arnold MA, Wilkerson DC, Devitt DA, Hurd BH, Lesikar BJ, Lohr VI, Martin CA, McDonald GV, Morris RL, Pittenger DR, Shaw DA, Zoldoske DF: Efficient water use in residential urban landscapes. HortScience. 2008, 43: 2081-2092.
Martin CA: Landscape water use in Phoenix, Arizona. Desert Plants. 2001, 17: 26-31.
Bradley BA, Blumenthal DM, Early R, Grosholz ED, Lawler JJ, Miller LP, Sorte CJB, D’Antonio CM, Diez JM, Dukes JS, Ibanez I, Olden JD: Global change, global trade, and the next wave of plant invasions. Front Ecol Environ. 2012, 10: 20-28. 10.1890/110145.
Burt JW, Muir AA, Piovia-Scott J, Veblen KE, Chang AL, Grossman JD, Weiskel HW: Preventing horticultural introductions of invasive plants: potential efficacy of voluntary initiatives. Biol Invasions. 2007, 9: 909-923. 10.1007/s10530-007-9090-4.
Broderick SR, Stevens MR, Geary B, Love SL, Jellen EN, Dockter RB, Daley SL, Lindgren DT: A survey of Penstemon’s genome size. Genome. 2011, 54: 160-173. 10.1139/G10-106.
Lindgren D, Wilde E: Growing Penstemons: Species, Cultivars and Hybrids. 2003, Haverford, PA: Infinity Publishing Com
Lindgren DT: Breeding Penstemon. Breeding Ornamental Plants. Edited by: Callaway DJ, Callaway MB. 2000, Portland, Oregon: Timber Press, 196-212.
Nold R: Penstemons. 1999, Portland, Oregon: Timber Press
Viehmeyer G: Let’s breed better Penstemon. Bul Amer Penstemon Soc. 1955, 14: 275-288.
Way D, James P: The Gardener’s Guide to Growing Penstemon. 1998, Portland, OR: Timber Press
Lindgren DT, Schaaf DM: Penstemon: a summary of interspecific crosses. HortScience. 2007, 42: 494-498.
Lindgren D: List and Description of Named Cultivars in the Genus Penstemon (2006). 2006, Lincoln, Nebraska: University of Nebraska-Lincoln Extension; EC1255
Straw RM: A redefinition of Penstemon (Scrophulariaceae). Brittonia. 1966, 18: 80-95. 10.2307/2805112.
Wolfe AD, Randle CP, Datwyler SL, Morawetz JJ, Arguedas N, Diaz J: Phylogeny, taxonomic affinities, and biogeography of Penstemon (Plantaginaceae) based on ITS and cpDNA sequence data. Amer J Bot. 2006, 93: 1699-1713. 10.3732/ajb.93.11.1699.
Uhlinger RD, Viehmeyer G: Penstemon in your Garden. 1971, Lincoln, Nebraska: University of Nebraska College of Agriculture The Agricultural Experiment Station, Station Circular 105
Viehmeyer G: Reversal of evolution in the genus Penstemon. Am Nat. 1958, 92: 129-137. 10.1086/282021.
Viehmeyer G: Advances in Penstemon breeding. Bul Amer Penstemon Soc. 1973, 32: 16-21.
Cronn R, Knaus BJ, Liston A, Maughan PJ, Parks M, Syring JV, Udall J: Targeted enrichment strategies for next-generation plant biology. Amer J Bot. 2012, 99: 291-311. 10.3732/ajb.1100356.
Heslop-Harrison JS: Exploiting novel germplasm. Aust J Agric Res. 2002, 53: 873-879. 10.1071/AR02078.
Maughan PJ, Smith SM, Fairbanks DJ, Jellen EN: Development, characterization, and linkage mapping of single nucleotide polymorphisms in the grain amaranths (Amaranthus sp.). Plant Gen. 2011, 4: 1-10. 10.3835/plantgenome2011.12.0001.
Bernardo R: Molecular markers and selection for complex traits in plants: learning from the last 20 years. Crop Sci. 2008, 48: 1649-1664. 10.2135/cropsci2008.03.0131.
Tanksley SD, McCouch SR: Seed banks and molecular maps: unlocking genetic potential from the wild. Science. 1997, 277: 1063-1066. 10.1126/science.277.5329.1063.
Dockter RB: Genome snapshot and molecular marker development in Penstemon (Plantaginaceae). M.S. Thesis. 2011, Brigham Young University, Department of Plant and Wildlife Sciences
Santana QC, Coetzee MPA, Steenkamp ET, Mlonyeni OX, Hammond GNA, Wingfield MJ, Wingfield BD: Microsatellite discovery by deep sequencing of enriched genomic libraries. Biotechniques. 2009, 46: 217-223. 10.2144/000113085.
Maughan PJ, Yourstone SM, Jellen EN, Udall JA: SNP discovery via genomic reduction, barcoding and 454-pyrosequencing in amaranth. Plant Gen. 2009, 2: 260-270. 10.3835/plantgenome2009.08.0022.
Păcurar DI, Păcurar ML, Street N, Bussell JD, Pop TI, Gutierrez L, Bellini C: A collection of INDEL markers for map-based cloning in seven Arabidopsis accessions. J Exp Bot. 2012, 63: 2491-2501. 10.1093/jxb/err422.
Althoff DM, Gitzendanner MA, Segraves KA: The utility of amplified fragment length polymorphisms in phylogenetics: a comparison of homology within and between genomes. Syst Biol. 2007, 56: 477-484. 10.1080/10635150701427077.
Sambrook J, Fritcsh EF, Maniatis T: Molecular Cloning: A Laboratory Manual. 1989, Cold Spring Harbor, N.Y: Cold Spring Harbor Lab
Todd JJ, Vodkin LO: Duplications that suppress and deletions that restore expression from a chalcone synthase multigene family. Plant Cell. 1996, 8: 687-699.
Holmgren NH: Penstemon. Intermountain Flora: Vascular Plants of the Intermountain West. Volume 4. Edited by: Cronquist A, Holmgren AH, Holmgren NH, Reveal JL, Holmgren PK. 1984, Bronx, New York, USA: New York Botanical Garden, 370-457.
Welsh SL, Atwood ND, Goodrich S, Higgins LC: A Utah Flora. 2008, Provo, Utah: Brigham Young University, 4
RepeatMasker. [http://www.repeatmasker.org]
Bao Z, Eddy SR: Automated de novo identification of repeat sequence families in sequenced genomes. Genome Res. 2002, 12: 1269-1276. 10.1101/gr.88502.
Price AL, Jones NC, Pevzner PA: De novo identification of repeat families in large genomes. Bioinformatics. 2005, 21 (Suppl 1): I351-I358. 10.1093/bioinformatics/bti1018.
Maughan PJ, Yourstone SM, Byers RL, Smith SM, Udall JA: Single-nucleotide polymorphism genotyping in mapping populations via genomic reduction and next-generation sequencing: proof-of-concept. Plant Gen. 2010, 3: 1-13.
Rhee SY, Beavis W, Berardini TZ, Chen GH, Dixon D, Doyle A, Garcia-Hernandez M, Huala E, Lander G, Montoya M, Miller N, Mueller LA, Mundodi S, Reiser L, Tacklind J, Weems DC, Wu YH, Xu I, Yoo D, Yoon J, Zhang PF: The Arabidopsis Information Resource (TAIR): a model organism database providing a centralized, curated gateway to Arabidopsis biology, research materials and community. Nucleic Acids Res. 2003, 31: 224-228. 10.1093/nar/gkg076.
Thiel T, Michalek W, Varshney RK, Graner A: Exploiting EST databases for the development and characterization of gene-derived SSR-markers in barley (Hordeum vulgare L.). Theor Appl Genet. 2003, 106: 411-422.
Stajich JE, Block D, Boulez K, Brenner SE, Chervitz SA, Dagdigian C, Fuellen G, Gilbert JGR, Korf I, Lapp H, Lehväslaiho H, Matsalla C, Mungall CJ, Osborne BI, Pocock MR, Schattner P, Senger M, Stein LD, Stupka E, Wilkinson MD, Birney E: The Bioperl toolkit: Perl modules for the life sciences. Genome Res. 2002, 12: 1611-1618. 10.1101/gr.361602.
Rozen S, Skaletsky HJ: Primer3 on the WWW for general users and for biologist programmers. Bioinformatics Methods and Protocols: Methods in Molecular Biology. Edited by: Krawetz S, Misener S. 2000, Totowa, NJ: Humana Press, 365-386.
PAUP* Phylogenetic analysis using parsimony (*and other methods). [http://paup.csit.fsu.edu/]
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ: Basic local alignment search tool. J Mol Biol. 1990, 215: 403-410.
GenBank. [http://www.ncbi.nlm.nih.gov/genbank/]
Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M: Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics. 2005, 21: 3674-3676. 10.1093/bioinformatics/bti610.
Kawabe A, Miyashita NT: Patterns of codon usage bias in three dicot and four monocot plant species. Genes Genet Syst. 2003, 78: 343-352. 10.1266/ggs.78.343.
Morgante M, Hanafey M, Powell W: Microsatellites are preferentially associated with nonrepetitive DNA in plant genomes. Nat Genet. 2002, 30: 194-200. 10.1038/ng822.
Robinson JP, Harris SA: Amplified fragment length polymorphisms and microsatellites: a phylogenetic perspective. EU-Compendium: Which DNA Marker for Which Purpose?. Edited by: Gillet EM. 1999, Göttingen, Germany: Institut für Forstgenetik und Forstpflanzenzüchtung, Universität Göttingen, 95-121.
Ochieng JW, Steane DA, Ladiges PY, Baverstock PR, Henry RJ, Shepherd M: Microsatellites retain phylogenetic signals across genera in eucalypts (Myrtaceae). Genet Mol Biol. 2007, 30: 1125-1134. 10.1590/S1415-47572007000600016.
Nadir E, Margalit H, Gallily T, Ben-Sasson SA: Microsatellite spreading in the human genome: evolutionary mechanisms and structural implications. Proc Natl Acad Sci USA. 1996, 93: 6470-6475. 10.1073/pnas.93.13.6470.
Viehmeyer G: Reports dealing in large part with hybridization and selection. Bul Amer Penstemon Soc. 1965, 24: 95-100.
Zamir D, Tadmor Y: Unequal segregation of nuclear genes in plants. Bot Gaz. 1986, 147: 355-358. 10.1086/337602.
Eshed Y, Zamir D: A genomic library of Lycopersicon pennellii in L. esculentum: A tool for fine mapping of genes. Euphytica. 1994, 79: 175-179. 10.1007/BF00022516.
Robbins MD, Masud MAT, Panthee DR, Gardner RG, Francis DM, Stevens MR: Marker assisted selection for coupling phase resistance to Tomato spotted wilt virus and Phytophthora infestans (late blight) in tomato. HortScience. 2010, 45: 1424-1428.
Canady MA, Meglic V, Chetelat RT: A library of Solanum lycopersicoides introgression lines in cultivated tomato. Genome. 2005, 48: 685-697. 10.1139/g05-032.
Canady MA, Ji YF, Chetelat RT: Homeologous recombination in Solanum lycopersicoides introgression lines of cultivated tomato. Genetics. 2006, 174: 1775-1788. 10.1534/genetics.106.065144.
Temnykh S, DeClerck G, Lukashova A, Lipovich L, Cartinhour S, McCouch S: Computational and experimental analysis of microsatellites in rice (Oryza sativa L.): frequency, length variation, transposon associations, and genetic marker potential. Genome Res. 2001, 11: 1441-1452. 10.1101/gr.184001.
Parida SK, Kalia SK, Kaul S, Dalal V, Hemaprabha G, Selvi A, Pandit A, Singh A, Gaikwad K, Sharma TR, Srivastava PS, Singh NK, Mohapatra T: Informative genomic microsatellite markers for efficient genotyping applications in sugarcane. Theor Appl Genet. 2009, 118: 327-338. 10.1007/s00122-008-0902-4.
Zhang FK, Zhao ZM: The influence of neighboring-nucleotide composition on single nucleotide polymorphisms (SNPs) in the mouse genome and its comparison with human SNPs. Genomics. 2004, 84: 785-795. 10.1016/j.ygeno.2004.06.015.
Morton BR, Bi IV, McMullen MD, Gaut BS: Variation in mutation dynamics across the maize genome as a function of regional and flanking base composition. Genetics. 2006, 172: 569-577.
Schmuths H, Meister A, Horres R, Bachmann K: Genome size variation among accessions of Arabidopsis thaliana. Ann Bot. 2004, 93: 317-321. 10.1093/aob/mch037.
Lynch M: The Origins of Genome Architecture. 2007, Sunderland, MA: Sinauer Associates, Inc
Lynch M, Conery JS: The origins of genome complexity. Science. 2003, 302: 1401-1404. 10.1126/science.1089370.
Kidwell MG: Transposable elements and the evolution of genome size in eukaryotes. Genetica. 2002, 115: 49-63. 10.1023/A:1016072014259.
Raskina O, Barber JC, Nevo E, Belyayev A: Repetitive DNA and chromosomal rearrangements: speciation-related events in plant genomes. Cytogenet Genome Res. 2008, 120: 351-357. 10.1159/000121084.
Kolano B, Gardunia BW, Michalska M, Bonifacio A, Fairbanks D, Maughan PJ, Coleman CE, Stevens MR, Jellen EN, Maluszynska J: Chromosomal localization of two novel repetitive sequences isolated from the Chenopodium quinoa Willd. genome. Genome. 2011, 54: 710-717. 10.1139/g11-035.
Kubis S, Schmidt T, Heslop-Harrison JS: Repetitive DNA elements as a major component of plant genomes. Ann Bot. 1998, 82 (Suppl A): 45-55.
Meyers B: A summary of Bruce Meyers’ Penstemon hybridizations. Bul Amer Penstemon Soc. 1998, 57: 2-11.
Friedt W, Snowdon RJ, Ordon F, Ahlemeyer J: Plant breeding: assessment of genetic diversity in crop plants and its exploitation in breeding. Prog Bot. 2007, 68: 151-178. 10.1007/978-3-540-36832-8_7.
Wolfe AD, Elisens WJ: Diploid hybrid speciation in Penstemon (Scrophulariaceae) revisited. Amer J Bot. 1993, 80: 1082-1094. 10.2307/2445754.
Wolfe AD, Elisens WJ: Nuclear ribosomal DNA restriction site variation in Penstemon section Peltanthera (Scrophulariaceae): an evaluation of diploid hybrid speciation and evidence for introgression. Amer J Bot. 1994, 81: 1627-1635. 10.2307/2445341.
Wolfe AD, Elisens WJ: Evidence of chloroplast capture and pollen-mediated gene flow in Penstemon sect. Peltanthera (Scrophulariaceae). Syst Bot. 1995, 20: 395-412. 10.2307/2419800.
Datwyler SL, Wolfe AD: Phylogenetic relationships and morphological evolution in Penstemon subg. Dasanthera (Veronicaceae). Syst Bot. 2004, 29: 165-176. 10.1600/036364404772974077.
Wolfe AD, Xiang Q-Y, Kephart SR: Assessing hybridization in natural populations of Penstemon (Scrophulariaceae) using hypervariable intersimple sequence repeat (ISSR) bands. Mol Ecol. 1998, 7: 1107-1125. 10.1046/j.1365-294x.1998.00425.x.
Wolfe AD, Xiang Q-Y, Kephart SR: Diploid hybrid speciation in Penstemon (Scrophulariaceae). Proc Natl Acad Sci USA. 1998, 95: 5112-5115. 10.1073/pnas.95.9.5112.
Elshire RJ, Glaubitz JC, Sun Q, Poland JA, Kawamoto K, Buckler ES, Mitchell SE: A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS One. 2011, 6: e19379-10.1371/journal.pone.0019379.
