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Analysis of EST sequences suggests recent origin of allotetraploid colonial and creeping bentgrasses

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Abstract

Advances in plant genomics have permitted the analysis of several members of the grass family, including the major domesticated species, and provided new insights into the evolution of the major crops on earth. Two members, colonial bentgrass (Agrostis capillaris L.) and creeping bentgrass (A. stolonifera L.) have only recently been domesticated and provide an interesting case of polyploidy and comparison to crops that have undergone human selection for thousands of years. As an initial step of characterizing these genomes, we have sampled roughly 10% of their gene content, thereby also serving as a starting point for the construction of their physical and genetic maps. Sampling mRNA from plants subjected to environmental stress showed a remarkable increase in transcription of transposable elements. Both colonial and creeping bentgrass are allotetraploids and are considered to have one genome in common, designated the A2 genome. Analysis of conserved genes present among the ESTs suggests the colonial and creeping bentgrass A2 genomes diverged from a common ancestor approximately 2.2 million years ago (MYA), thereby providing an enhanced evolutionary zoom in respect to the origin of maize, which formed 4.8 MYA, and tetraploid wheat, which formed only 0.5 MYA and is the progenitor of domesticated hexaploid wheat.

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References

  • Belanger FC, Plumley K, Day PR, Meyer WA (2003) Interspecific hybridization as a potential method for improvement of Agrostis species. Crop Sci 43:2172–2176

    Article  Google Scholar 

  • Belanger FC, Bonos S, Meyer WA (2004) Dollar spot resistant hybrids between creeping bentgrass and colonial bentgrass. Crop Sci 44:581–586

    Google Scholar 

  • Bennetzen JL (2000) Transposable element contributions to plant gene and genome evolution. Plant Mol Biol 42:251–269

    Article  PubMed  CAS  Google Scholar 

  • Bhattramakki D, Dolan M, Hanafey M, Wineland R, Vaske D, Register III JC, Tingey SV, Rafalski A (2002) Insertion-deletion polymorphisms in 3′ regions of maize genes occur frequently and can be used as highly informative genetic markers. Plant Mol Biol 48:539–547

    Article  PubMed  CAS  Google Scholar 

  • Birnboim HC, Doly J (1979) A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res 7:1513–1523

    Article  PubMed  CAS  Google Scholar 

  • Bonos SA, Casler MD, Meyer WA (2003) Inheritance of dollar spot resistance in creeping bentgrass. Crop Sci 43:2189–2196

    Article  Google Scholar 

  • Bonos SA, Honig J, Kubik C (2005) The identification of quantitative trait loci for dollar spot resistance in creeping bentgrass using simple sequence repeats. In: The ASA-CSSA-SSSA international annual meeting, Salt Lake City

  • Brady KP, Rowe LB, Her H, Stevens TJ, Eppig J, Sussman DJ, Sikela J, Beier DR (1997) Genetic mapping of 262 loci derived from expressed sequences in a murine interspecific cross using single-strand conformational polymorphism analysis. Genome Res 7:1085–1093

    PubMed  CAS  Google Scholar 

  • Bruggmann R, Bharti AK, Gundlach H, Lai J, Young S, Pontaroli AC, Wei F, Haberer G, Fuks G, Du C, Raymond C, Estep MC, Liu R, Bennetzen JL, Chan AP, Rabinowicz PD, Quackenbush J, Barbazuk WB, Wing RA, Birren B, Nusbaum C, Rouonsley S, Mayer KF, Messing J (2006) Uneven chromosome contraction and expansion in the maize genome. Genome Res 16:1241–1251

    Article  PubMed  CAS  Google Scholar 

  • Carbone I, Kohn LM (1993) Ribosomal DNA sequence divergence within internal transcribed spacer 1 of the Sclerotiniaceae. Mycologia 85:415–427

    Article  CAS  Google Scholar 

  • Casacuberta JM, Santiago N (2003) Plant LTR-retrotransposons and MITEs: control of transposition and impact on the evolution of plant genes and genomes. Gene 311:1–11

    Article  PubMed  CAS  Google Scholar 

  • Chakraborty N, Bae J, Warnke S, Chang T, Jung G (2005) Linkage map construction in allotetraploid creeping bentgrass (Agrostis stolonifera L.). Theor Appl Genet 111:795–803

    Article  PubMed  CAS  Google Scholar 

  • Chakraborty N, Chang T, Casler MD, Jung G (2006) Response of bentgrass cultivars to Sclerotinia homoeocarpa isolates representing ten vegetative compatibility groups. Crop Sci 46:1237–1244

    Article  Google Scholar 

  • Devos KM, Beales J, Ogihara Y, Doust AN (2005) Comparative sequence analysis of the Phytochrome C gene and its upstream region in allohexaploid wheat reveals new data on the evolution of its three constituent genomes. Plant Mol Biol 58:625–641

    Article  PubMed  CAS  Google Scholar 

  • Du C, Swigonova Z, Messing J (2006) Retrotranspositions in orthologouos regions of closely related grass species. BMC Evol Biol 6:62

    Article  PubMed  CAS  Google Scholar 

  • Feschotte C, Jiang N, Wessler SR (2002) Plant transposable elements: where genetics meets genomics. Nat Rev Genet 3:329–341

    Article  PubMed  CAS  Google Scholar 

  • Fulton TM, Van der Hoeven R, Eannetta NT, Tanksley SD (2002) Identification, analysis, and utilization of conserved ortholog set markers for comparative genomics in higher plants. Plant Cell 14:1457–1467

    Article  PubMed  CAS  Google Scholar 

  • Gale MD, Devos KM (1998) Comparative genetics in the grasses. Proc Natl Acad Sci USA 95:1971–1974

    Article  PubMed  CAS  Google Scholar 

  • Gaut BS (2002) Evolutionary dynamics of grass genomes. New Phytol 154:15–28

    Article  CAS  Google Scholar 

  • Gaut BS, Morton BR, McCaig BC, Clegg MT (1996) Substitution rate comparisons between grasses and palms: synonymous rate differences at the nuclear gene Adh parallel rate differences at the plastid gene rbcL. Proc Natl Acad Sci USA 93:10274–10279

    Article  PubMed  CAS  Google Scholar 

  • Grandbastien M-A (1998) Activation of plant retrotransposons under stress conditions. Trends Plant Sci 3:181–187

    Article  Google Scholar 

  • Grass Phylogeny Working Group (2001) Phylogeny and subfamilial classification of the grasses (Poaceae). Ann Mo Bot Gard 88:373–457

    Article  Google Scholar 

  • Griffiths S, Sharp R, Foote TN, Bertin I, Wanous M, Reader S, Colas I, Moore G (2006) Molecular characterization of Ph1 as a major chromosome pairing locus in polyploid wheat. Nature 439:749–752

    Article  PubMed  CAS  Google Scholar 

  • Haberer G, Young SK, Bharti AK, Gundlach H, Raymond C, Fuks G, Butler E, Wing RA, Rounsley S, Nusbaum C, Birren B, Mayer KFX, Messing J (2005) Structure and architecture of the maize genome. Plant Physiol 139:1612–1624

    Article  PubMed  CAS  Google Scholar 

  • Holst-Jensen A, Kohn LM, Schumacher T (1997) Nuclear rDNA phylogeny of the Sclerotiniaceae. Mycologia 89:885–899

    Article  CAS  Google Scholar 

  • Huang S, Sirikhachornkit A, Su X, Faris J, Gill B, Haselkorn R, Gornicki P (2002) Genes encoding plastid acetyl-CoA carboxylae and 3-phosphoglycerate kinase of the Triticum/Aegilops complex and the evolutionary history of polyploidy wheat. Proc Natl Acad Sci USA 99:8133–8138

    Article  PubMed  CAS  Google Scholar 

  • Huang X, Madan A (1999) CAP3: a DNA sequence assembly program. Genome Res 9:868–877

    Article  PubMed  CAS  Google Scholar 

  • International Rice Genome Sequencing Project (2005) The map-based sequence of the rice genome. Nature 436:793–800

    Article  CAS  Google Scholar 

  • Jones K (1956a) Species determination in Agrostis. Part I. Cytological relationships in Agrostis canina L. J Genet 54:370–376

    Google Scholar 

  • Jones K. (1956b) Species differentiation in Agrostis. Part II. The significance of chromosome pairing in the tetraploid hybrids of Agrostis canina subsp. montana Hartmn., A. tenuis Sibth. and A. stolonifera L. J Genet 54:377–393

    Google Scholar 

  • Jones K (1956c) Species determination in Agrostis. Part III. Agrostis gigantea Roth. and its hybrids with A. tenuis Sibth. and A. stolonifera L. J Genet 54:394–399

    Article  Google Scholar 

  • Kellogg EA (1998) Relationships of cereal crops and other grasses. Proc Natl Acad Sci USA 95:2005–2010

    Article  PubMed  CAS  Google Scholar 

  • Kellogg EA (2001) Evolutionary history of the grasses. Plant Physiol 125:1198–1205

    Article  PubMed  CAS  Google Scholar 

  • Kimura Y, Tosa Y, Betsuyaku S, Sasabe Y, Tomita R, Murakami J, Nakayashiki H, Mayama S (2002) Oat retrotransposon OARE-1 is activated in both compatible and incompatible interactions with pathogenic fungi. J Gen Plant Pathol 68:8–14

    Article  CAS  Google Scholar 

  • Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163

    Article  PubMed  CAS  Google Scholar 

  • McClintock B (1984) The significance of responses of the genome to challenge. Science 226:792–801

    Article  PubMed  CAS  Google Scholar 

  • Messing J, Llaca V (1998) Importance of anchor genomes for any plant genome project. Proc Natl Acad Sci USA 95:2017–2020

    Article  PubMed  CAS  Google Scholar 

  • Messing J, Bharti AK, Karlowski WM, Gundlach H, Kim HR, Yu Y, Wei F, Fuks G, Soderlund CA, Mayer KFX, Wing RA (2004) Sequence composition and genome organization of maize. Proc Natl Acad Sci USA 101:14349–14354

    Article  PubMed  CAS  Google Scholar 

  • Meyer WA, Funk CR (1989) Progress and benefits to humanity from breeding cool-season grasses for turf. In: Sleeper DA, Asay KH, Pederson JF (eds) Contributions from breeding forage and turfgrasses. Crop Science Society of America Special Publication Number 15, Madison, WI, USA

  • Ogihara Y, Isono K, Kojima T, Endo A, Hanaoka M, Shiina T, Terachi T, Utsugi S, Murata M, Mori N, Takumi S, Ikeo K, Gojobori T, Murai R, Murai K, Matsuoka Y, Ohnishi Y, Tajiri H, Tsunewaki K (2002) Structural features of a wheat plastome as revealed by complete sequencing of chloroplast DNA. Mol Genet Genomics 266:740–746

    Article  PubMed  CAS  Google Scholar 

  • Plumley KA, Meyer WA, Murphy JA, Clarke BB, Bonos SA, Dickson WK, Clark JB, Smith DA (2000) Performance of bentgrass cultivars and selections in New Jersey turf trials. Rutgers Turfgrass Proc 32:1–21

    Google Scholar 

  • Renvoize SA, Clayton WD (1992) Classification and evolution of the grasses. In: Chapman GP (ed) Grass evolution and domestication. Cambridge University Press, Cambridge, pp 3–37

    Google Scholar 

  • Rice Chromosomes 11 and 12 Sequencing Consortia (2005) The sequence of rice chromosomes 11 and 12, rich in disease resistance genes and recent gene duplications. BMC Biol 3:20

    Article  CAS  Google Scholar 

  • Rotter D, Warnke S, Bonos SA, Meyer W, Belanger FD (2006) Colonial bentgrass genetic linkage mapping. In: The ASA-CSSA-SSSA international annual meeting, Indianapolis

  • Rudd S (2005) openSputnik—a database to ESTablish comparative plant genomics using unsaturated sequence collections. Nucleic Acids Res 33:D622–D627

    Article  PubMed  CAS  Google Scholar 

  • Ruemmele BA (2003) Agrostis capillaris (Agrostis tenuis Sibth.) colonial bentgrass. In: Casler MD, Duncan RR (eds) Turfgrass biology, genetics, and breeding. Wiley, Hoboken, pp 187–200

    Google Scholar 

  • Ruepp A, Zollner A, Maier D, Albermann K, Hani J, Mokrejs M, Tetko I, Guldener U, Mannhaupt G, Munsterkotter M, Mewes HW (2004) The FunCat, a functional annotation scheme for systematic classification of proteins from whole genomes. Nucleic Acids Res 32:5539–5545

    Article  PubMed  CAS  Google Scholar 

  • Senchina DS, Alvarez I, Cronn RC, Liu B, Rong J, Noyes RD, Paterson AH, Wing RA, Wilkins TA, Wendel JF (2003) Rate variation among nuclear genes and the age of polyploidy in Gossypium. Mol Biol Evol 20:633–643

    Article  PubMed  CAS  Google Scholar 

  • Song R, Llaca V, Messing J (2002) Mosaic organization of orthologous sequences in grass genomes. Genome Res 12:1549–1555

    Article  PubMed  CAS  Google Scholar 

  • Soreng RJ, Davis JI (1998) Phylogenetics and character evolution in the grass family (Poaceae): simultaneous analysis of morphological and chloroplast DNA restriction site character sets. Bot Rev 64:1–85

    Google Scholar 

  • Swigonova Z, Lai J, Ma J, Ramakrishna W, Llaca V, Bennetzen JL, Messing J (2004) Close split of sorghum and maize genome progenitors. Genome Res 14:1916–1923

    Article  PubMed  CAS  Google Scholar 

  • Swofford L (2002) PAUP*: phylogenetic analysis using parsimony (*and other methods), Version 4. Sinauer Associates, Sunderland

    Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL-X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    Article  PubMed  CAS  Google Scholar 

  • Tikhonov AP, SanMiguel PJ, Nakajima Y, Gorenstein NM, Bennetzen JL, Avramova Z (1999) Colinearity and its exceptions in orthologous adh regions of maize and sorghum. Proc Natl Acad Sci USA 96:7409–7414

    Article  PubMed  CAS  Google Scholar 

  • Vicient CM, Jaaskelainen MJ, Kalendar R, Schulman AH (2001) Active retrotransposons are a common feature of grass genomes. Plant Physiol 125:1283–1292

    Article  PubMed  CAS  Google Scholar 

  • Viji G, Uddin W, O’Neill NR, Mischke S, Saunders JA (2004) Genetic diversity of Sclerotinia homoeocarpa isolates from turfgrasses from various regions in North America. Plant Dis 88:1269–1276

    Article  CAS  Google Scholar 

  • Walsh B, Ikeda SS, Boland GJ (1999) Biology and management of dollar spot (Sclerotinia homoeocarpa); an important disease of turfgrass. HortScience 34:13–21

    Google Scholar 

  • Warnke SE (2003) Creeping bentgrass (Agrostis stolonifera L.). In: Casler MD, Duncan RR (eds) Turfgrass biology, genetics, and breeding. Wiley, Hoboken, pp 175–185

    Google Scholar 

  • Watson L (1990) The grass family, Poaceae. In: Chapman GP (ed) Reproductive versatility in the grasses. Cambridge University Press, Cambridge, pp 1–31

    Google Scholar 

  • Wessler SR (1996) Plant retrotransposons: turned on by stress. Curr Biol 6:959–961

    Article  PubMed  CAS  Google Scholar 

  • Xu JH, Messing J (2006) Maize haplotype with a helitron-amplified cytidine deaminase gene copy. BMC Genet 7:52

    Article  PubMed  CAS  Google Scholar 

  • Young WC (2004) Extension estimates for Oregon forage and turf grass seed crop production, 2004. http://www.cropandsoil.oregonstate.edu/seed-ext/Agronomy/04ftprod.html

  • Zimmer R, Gibbins AMV (1997) Construction and characterization of a large-fragment chicken bacterial artificial chromosome library. Genomics 42:217–226

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported with funds provided by The Rutgers Center for Turfgrass Science, The United States Department of Agriculture, Michigan State University, and the United States Golf Association. We thank M. Murillo and G. Zylstra for assistance with the colony picking. We thank G. Fuks, G. Keizer, A.B. Nelson, S. Young, and V. Zohovetz at PGIR for technical assistance.

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Authors and Affiliations

  1. Department of Plant Biology and Pathology and The Biotechnology Center for Agriculture & the Environment, School of Environmental and Biological Sciences, Rutgers, The State University of New Jersey, New Brunswick, NJ, 08903, USA

    David Rotter, Huaijun Michael Li, Chongyuan Luo, Stacy A. Bonos, William A. Meyer & Faith C. Belanger

  2. The Plant Genome Initiative at Rutgers, Waksman Institute, Rutgers, The State University of New Jersey, Piscataway, NJ, 08854, USA

    Arvind K. Bharti & Joachim Messing

  3. Department of Crop and Soil Science, Michigan State University, East Lansing, MI, 48824, USA

    Suleiman Bughrara

  4. Department of Plant, Soil, and Insect Sciences, University of Massachusetts-Amherst, Amherst, MA, 01003, USA

    Geunhwa Jung

  5. Turku Center for Biotechnology, Tykistoekatu 6, Turku, Finland

    Stephen Rudd

  6. USDA-ARS, Beltsville, MD, 20705, USA

    Scott E. Warnke

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  1. David Rotter
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  2. Arvind K. Bharti
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  3. Huaijun Michael Li
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  9. William A. Meyer
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  12. Faith C. Belanger
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Correspondence to Faith C. Belanger.

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Communicated by R. Hagemann.

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Rotter, D., Bharti, A.K., Li, H.M. et al. Analysis of EST sequences suggests recent origin of allotetraploid colonial and creeping bentgrasses. Mol Genet Genomics 278, 197–209 (2007). https://doi.org/10.1007/s00438-007-0240-2

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