期刊论文详细信息
EvoDevo
Pattern and process in the evolution of the sole dioecious member of Brassicaceae
Verónica S Di Stilio1  Vietnam Le Huynh1  Valerie L Soza1 
[1] Department of Biology, University of Washington, Box 351800, Seattle, WA 98195-1800, USA
关键词: unisexual flowers;    sex differentiation;    PISTILLATA;    phylogenetic network;    organ arrest;    genome size;    floral ontogeny;    dioecy;    programmed cell death;    allopolyploidy;   
Others  :  1093176
DOI  :  10.1186/2041-9139-5-42
 received in 2014-06-21, accepted in 2014-10-07,  发布年份 2014
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【 摘 要 】

Background

Lepidium sisymbrioides, a polyploid New Zealand endemic, is the sole dioecious species in Brassicaceae and therefore the closest dioecious relative of the model plant Arabidopsis thaliana. The attractiveness of developing this system for future studies on the genetics of sex determination prompted us to investigate historical and developmental factors surrounding the evolution of its unisexual flowers. Our goal was to determine the evolutionary pattern of polyploidization of L. sisymbrioides and the timing and process of flower reproductive organ abortion. To that end, we used a combination of phylogenetics to place this species within the complex history of polyploidization events in Lepidium and histology to compare its floral ontogeny to that of its closest hermaphroditic relatives and to A. thaliana.

Results

Using a nuclear locus (PISTILLATA), we reconstructed the gene tree among Lepidium taxa and applied a phylogenetic network analysis to identify ancestral genomes that contributed to the evolution of L. sisymbrioides. Combining this phylogenetic framework with cytological and genome size data, we estimated L. sisymbrioides as an allo-octoploid resulting from three hybridization events. Our investigations of flower development showed that unisexual flowers appear to abort reproductive organs by programmed cell death in female flowers and by developmental arrest in male flowers. This selective abortion occurs at the same floral developmental stage in both males and females, corresponding to Arabidopsis stage nine.

Conclusions

Dioecy in Brassicaceae evolved once in L. sisymbrioides following several allopolyploidization events, by a process of selective abortion of reproductive organs at intermediate stages of flower development. Different developmental processes, but similar timing of abortions, affect male versus female flower development. An increased understanding of how and when reproductive organs abort in this species, combined with our estimates of ancestral genome contributions, ploidy and genome size, lay the foundation for future efforts to examine the genetic mechanisms involved in the evolution of unisexual flowers in the closest dioecious relative of the best studied model plant.

【 授权许可】

   
2014 Soza et al.; licensee BioMed Central Ltd.

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【 参考文献 】
  • [1]Al-Shehbaz IA, Beilstein MA, Kellogg EA: Systematics and phylogeny of the Brassicaceae (Cruciferae): an overview. Plant Syst Evol 2006, 259:89-120.
  • [2]Warwick SI, Al-Shehbaz IA: Brassicaceae: chromosome number index and database on CD-Rom. Plant Syst Evol 2006, 259:237-248.
  • [3]Endress PK: Evolution and floral diversity: the phylogenetic surroundings of Arabidopsis and Antirrhinum. Int J Plant Sci 1992, 153:S106-S122.
  • [4]Al-Shehbaz IA: The genera of Lepidieae (Cruciferae, Brassicaceae) in the Southeastern United States. J Arnold Arboretum 1986, 67:265-311.
  • [5]Lee JY, Mummenhoff K, Bowman JL: Allopolyploidization and evolution of species with reduced floral structures in Lepidium L. (Brassicaceae). Proc Natl Acad Sci 2002, 99:16835-16840.
  • [6]Kirk T: The Students’ Flora of New Zealand and the Outlying Islands. Wellington, New Zealand: John Mackay, Government Printer; 1899.
  • [7]Bateman AJ: Note on dioecy in the Cruciferae. Heredity 1955, 9:415-415.
  • [8]Webb CJ, Sykes WR, Garnock-Jones PJ: Flora of New Zealand: Naturalised Pteridophytes, Gymnosperms, Dicotyledons, Volume IV. Botany Division D. S. I. R.: Christchurch, New Zealand; 1988.
  • [9]Mummenhoff K, Brueggemann H, Bowman JL: Chloroplast DNA phylogeny and biogeography of Lepidium (Brassicaceae). Am J Bot 2001, 88:2051-2063.
  • [10]Heenan PB, Mitchell AD, McLenachan PA, Lockhart PJ, de Lange PJ: Natural variation and conservation of Lepidium sisymbrioides Hook, f. and L. solandri Kirk (Brassicaceae) in South Island, New Zealand, based on morphological and DNA sequence data. N Z J Bot 2007, 45:237-264.
  • [11]Allan HH: Flora of New Zealand. Volume I. Indigenous Tracheophyta (Psilopsida, Lycopsida, Filicopsida, Gymnospermae, Dicotyledones). R. E. Owen, Government Printer: Wellington, New Zealand; 1961.
  • [12]Mummenhoff K, Linder P, Friesen N, Bowman JL, Lee J-Y, Franzke A: Molecular evidence for bicontinental hybridogenous genomic constitution in Lepidium sensu stricto (Brassicaceae) species from Australia and New Zealand. Am J Bot 2004, 91:254-261.
  • [13]Miller JS, Venable DL: Polyploidy and the evolution of gender dimorphism in plants. Science 2000, 289:2335-2338.
  • [14]Miller JS, Venable DL: The transition to gender dimorphism on an evolutionary background of self-incompatibilty: an example from Lycium (Solanaceae). Am J Bot 2002, 89:1907-1915.
  • [15]Spigler RB, Lewers KS, Johnson AL, Ashman TL: Comparative mapping reveals autosomal origin of sex chromosome in octoploid Fragaria virginiana. J Hered 2010, 101:S107-S117.
  • [16]Sakai AK, Weller SG: Gender and sexual dimorphism in flowering plants: a review of terminology, biogeographic patterns, ecological correlates, and phylogenetic approaches. In Gender and Sexual Dimorphism in Flowering Plants. Berlin, Germany: Springer; 1999:1-32.
  • [17]Godley EJ: Flower biology in New Zealand. N Z J Bot 1979, 17:441-466.
  • [18]Jesson LK: Ecological correlates of diversification in New Zealand angiosperm lineages. N Z J Bot 2007, 45:35-51.
  • [19]Beilstein MA, Nagalingum NS, Clements MD, Manchester SR, Mathews S: Dated molecular phylogenies indicate a Miocene origin for Arabidopsis thaliana. Proc Natl Acad Sci 2010, 107:18724-18728.
  • [20]Bowman JL: Arabidopsis: An Atlas of Morphology and Development. New York: Springer; 1994.
  • [21]Ma H: Molecular genetic analyses of microsporogenesis and microgametogenesis in flowering plants. Annu Rev Plant Biol 2005, 56:393-434.
  • [22]Diggle PK, Di Stilio VS, Gschwend AR, Golenberg EM, Moore RC, Russell JRW, Sinclair JP: Multiple developmental processes underlie sex differentiation in angiosperms. Trends Genet 2011, 27:368-376.
  • [23]De Lange PJ, Norton DA, Courtney SP, Heenan PB, Barkla JW, Cameron EK, Hitchmough R, Townsend AJ: Threatened and uncommon plants of New Zealand (2008 revision). N Z J Bot 2009, 47:61-96.
  • [24]Mitchell AD, Heenan PB: Systematic relationships of New Zealand endemic Brassicaceae inferred from nrDNA ITS sequence data. Syst Bot 2000, 25:98.
  • [25]Mummenhoff K, Polster A, Muehlhausen A, Theissen G: Lepidium as a model system for studying the evolution of fruit development in Brassicaceae. J Exp Bot 2009, 60:1503-1513.
  • [26]Hughey JR, Silva PC, Hommersand MH: Solving taxonomic and nomenclatural problems in Pacific Gigartinaceae (Rhodophyta) using DNA from type material. J Phycol 2001, 37:1091-1109.
  • [27]Maddison DR, Maddison WP: MacClade 4: Analysis of Phylogeny and Character Evolution. Sunderland, MA: Sinauer Associates; 2005.
  • [28]Martin DP, Lemey P, Lott M, Moulton V, Posada D, Lefeuvre P: RDP3: a flexible and fast computer program for analyzing recombination. Bioinformatics 2010, 26:2462-2463.
  • [29]Martin D, Rybicki E: RDP: detection of recombination amongst aligned sequences. Bioinformatics 2000, 16:562-563.
  • [30]Martin DP, Posada D, Crandall KA, Williamson C: A modified bootscan algorithm for automated identification of recombinant sequences and recombination breakpoints. AIDS Res Hum Retroviruses 2005, 21:98-102.
  • [31]Padidam M, Sawyer S, Fauquet CM: Possible emergence of new geminiviruses by frequent recombination. Virology 1999, 265:218-225.
  • [32]Smith JM: Analyzing the mosaic structure of genes. J Mol Evol 1992, 34:126-129.
  • [33]Posada D, Crandall KA: Evaluation of methods for detecting recombination from DNA sequences: computer simulations. Proc Natl Acad Sci U S A 2001, 98:13757-13762.
  • [34]Gibbs MJ, Armstrong JS, Gibbs AJ: Sister-Scanning: a Monte Carlo procedure for assessing signals in recombinant sequences. Bioinformatics 2000, 16:573-582.
  • [35]Boni MF, Posada D, Feldman MW: An exact nonparametric method for inferring mosaic structure in sequence triplets. Genetics 2007, 176:1035-1047.
  • [36]Holmes EC, Worobey M, Rambaut A: Phylogenetic evidence for recombination in dengue virus. Mol Biol Evol 1999, 16:405-409.
  • [37]Guindon S, Gascuel O: A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 2003, 52:696-704.
  • [38]Darriba D, Taboada GL, Doallo R, Posada D: jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 2012, 9:772-772.
  • [39]Akaike H: A new look at the statistical model identification. IEEE Trans Autom Control 1974, AC19:716-723.
  • [40]Smith JF, Stillman AJ, Larson SR, Culumber CM, Robertson IC, Novak SJ: Phylogenetic relationships among Lepidium papilliferum (L. Henderson) A. Nels. & J. F. Macbr., L. montanum Nutt., and L. davisii Rollins (Brassicaceae). J Torrey Botanical Society 2009, 136:149-163.
  • [41]Huelsenbeck JP, Ronquist F: MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 2001, 17:754-755.
  • [42]Ronquist F, Huelsenbeck JP: MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 2003, 19:1572-1574.
  • [43]Miller MA, Pfeiffer W, Schwartz T: Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In Proceedings of the Gateway Computing Environments Workshop (GCE), 2010. New Orleans, LA: Institute of Electrical and Electronics Engineers; 2010:1-8.
  • [44]Yang ZH, Rannala B: Bayesian phylogenetic inference using DNA sequences: a Markov Chain Monte Carlo method. Mol Biol Evol 1997, 14:717-724.
  • [45]Rambaut A: FigTree Version 1.4. 2012. [http://tree.bio.ed.ac.uk/software/figtree/ webcite]
  • [46]Zwickl DJ: Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. Austin: The University of Texas; 2006.
  • [47]Felsenstein J: Confidence limits on phylogenies: an approach using the bootstrap. Evolution 1985, 39:783-791.
  • [48]Sukumaran J, Holder MT: DendroPy: a Python library for phylogenetic computing. Bioinformatics 2010, 26:1569-1571.
  • [49]Huson DH, Scornavacca C: Dendroscope 3: an interactive tool for rooted phylogenetic trees and networks. Syst Biol 2012, 61:1061-1067.
  • [50]Huber KT, Oxelman B, Lott M, Moulton V: Reconstructing the evolutionary history of polyploids from multilabeled trees. Mol Biol Evol 2006, 23:1784-1791.
  • [51]Kato A: Air drying method using nitrous oxide for chromosome counting in maize. Biotech Histochem 1999, 74:160-166.
  • [52]Matsushita SC, Tyagi AP, Thornton GM, Pires JC, Madlung A: Allopolyploidization lays the foundation for evolution of distinct populations: evidence from analysis of synthetic Arabidopsis allohexaploids. Genetics 2012, 191:535-547.
  • [53]Wright KM, Pires JC, Madlung A: Mitotic instability in resynthesized and natural polyploids of the genus Arabidopsis (Brassicaceae). Am J Bot 2009, 96:1656-1664.
  • [54]Greilhuber J, Dolezel J, Lysak MA, Bennett MD: The origin, evolution and proposed stabilization of the terms “genome size” and “C-value” to describe nuclear DNA contents. Ann Bot 2005, 95:255-260.
  • [55]Davison J, Tyagi A, Comai L: Large-scale polymorphism of heterochromatic repeats in the DNA of Arabidopsis thaliana. BMC Plant Biol 2007, 7:44. BioMed Central Full Text
  • [56]Gregory TR: Animal Genome Size Database. 2013. [http://www.genomesize.com webcite]
  • [57]Dolezel J, Greilhuber J: Nuclear genome size: are we getting closer? Cytometry A 2010, 77:635-642.
  • [58]Dolezel J, Bartos J, Voglmayr H, Greilhuber J: Nuclear DNA content and genome size of trout and human. Cytometry A 2003, 51A:127-128.
  • [59]Bowman JL, Smyth DR: Patterns of petal and stamen reduction in Australian species of Lepidium L. (Brassicaceae). Int J Plant Sci 1998, 159:65-74.
  • [60]Chehregani A, Sedaghat M: Pollen grain and ovule development in Lepidium vesicarium (Brassicaceae). Int J Agriculture & Biology 2009, 11:601-605.
  • [61]Muller A: Zur Charakterisierung der Bluten und Infloreszenzen von Arabidopsis thaliana (L.) Heynh. Kulturpflanze 1961, 9:364-393.
  • [62]Smyth DR, Bowman JL, Meyerowitz EM: Early flower development in Arabidopsis. Plant Cell 1990, 2:755-767.
  • [63]Kramer EM: Methods for studying the evolution of plant reproductive structures: comparative gene expression techniques. In Molecular Evolution: Producing the Biochemical Data, Part B. Volume 395. Edited by Zimmer EA, Roalson EH. San Diego, CA: Elsevier Academic Press; 2005:617-636.
  • [64]Johansen DA: Plant Microtechnique. New York. London: McGraw-Hill Book Company, Inc.; 1940.
  • [65]De Lange PJ, Murray BG: Contributions to a chromosome atlas of the New Zealand flora - 37. Miscellaneous families. N Z J Bot 2002, 40:1-23.
  • [66]Mitchell CH, Diggle PK: The evolution of unisexual flowers: morphological and functional convergence results from diverse developmental transitions. Am J Bot 2005, 92:1068-1076.
  • [67]Wu HM, Cheung AY: Programmed cell death in plant reproduction. Plant MolBiol 2000, 44:267-281.
  • [68]Noodén LD: Plant Cell Death Processes. San Diego, CA: Elsevier Academic Press; 2004.
  • [69]Van Doorn WG, Beers EP, Dangl JL, Franklin-Tong VE, Gallois P, Hara-Nishimura I, Jones AM, Kawai-Yamada M, Lam E, Mundy J: Morphological classification of plant cell deaths. Cell Death & Differentiation 2011, 18:1241-1246.
  • [70]Van Doorn WG: Classes of programmed cell death in plants, compared to those in animals. J Exp Bot 2011, 62:4749-4761.
  • [71]Crisp M, Cook L, Steane D: Radiation of the Australian flora: what can comparisons of molecular phylogenies across multiple taxa tell us about the evolution of diversity in present–day communities? Philos Trans R Soc Lond B Biol Sci 2004, 359:1551-1571.
  • [72]Carlquist S: The biota of long-distance dispersal. V. Plant dispersal to Pacific Islands. Bulletin of the Torrey Botanical Club 1967, 94:129-162.
  • [73]Niemi A: Lepidium ruderale L. on gull skerries in the archipelago SW of Helsingfors. Memoranda Societatis pro Fauna et Flora Fennica 1968, 44:5-12.
  • [74]Mummenhoff K, Hurka H, Bandelt H: Systematics of Australian Lepidium species (Brassicaceae) and implications for their origin - evidence from IEF analysis of RUBISCO. Plant Syst Evol 1992, 183:99-112.
  • [75]Garnock-Jones P, Norton D: Lepidium naufragorum (Brassicaceae), a new species from Westland, and notes on other New Zealand coastal species of Lepidium. N Z J Bot 1995, 33:43-51.
  • [76]Johnston JS, Pepper AE, Hall AE, Chen ZJ, Hodnett G, Drabek J, Lopez R, Price HJ: Evolution of genome size in Brassicaceae. Ann Bot 2005, 95:229-235.
  • [77]Oyama RK, Clauss MJ, Formanová N, Kroymann J, Schmid KJ, Vogel H, Weniger K, Windsor AJ, Mitchell-Olds T: The shrunken genome of Arabidopsis thaliana. Plant Syst Evol 2008, 273:257-271.
  • [78]Lysak MA, Koch MA, Beaulieu JM, Meister A, Leitch IJ: The dynamic ups and downs of genome size evolution in Brassicaceae. Mol Biol Evol 2009, 26:85-98.
  • [79]Bennett MD, Leitch IJ, Price HJ, Johnston JS: Comparisons with Caenorhabditis (similar to 100 Mb) and Drosophila (similar to 175 Mb) using flow cytometry show genome size in Arabidopsis to be similar to 157 Mb and thus similar to 25% larger than the Arabidopsis genome initiative estimate of similar to 125 Mb. Ann Bot 2003, 91:547-557.
  • [80]Bennett MD, Smith JB: Nuclear DNA amounts in angiosperms. Philos Trans R Soc Lond B Biol Sci 1991, 334:309-345.
  • [81]Burton JN, Adey A, Patwardhan RP, Qiu R, Kitzman JO, Shendure J: Chromosome-scale scaffolding of de novo genome assemblies based on chromatin interactions. Nat Biotechnol 2013, 31:1119-1125.
  • [82]Krasileva K, Buffalo V, Bailey P, Pearce S, Ayling S, Tabbita F, Soria M, Wang S, Consortium I, Akhunov E, Uauy C, Dubcovsky J: Separating homeologs by phasing in the tetraploid wheat transcriptome. Genome Biol 2013, 14:R66. BioMed Central Full Text
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