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Differential effects of polyploidy and diploidy on fitness of apomictic Boechera

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Abstract

The co-occurrence of apomixis (asexual reproduction) and polyploidy in plants has been the subject of debate in regard to the origin and evolution of asexuality. In recent years, polyploidy has been postulated as a maintenance and stabilization factor rather than as a source of apomixis origin. It is assumed polyploidy facilitates the compensation for mutation accumulation, and hence, the rare occurrence of diploid apomixis indirectly supports this finding. Nevertheless, diploid apomicts exist and are successful, especially in the genus Boechera. While comparing phenotypic traits, fitness-related traits and apomixis penetrance between both diploid and triploid apomicts in the genus Boechera, it was expected to find trait variance that can be attributed to ploidy. Surprisingly, little trait variation could be assigned to ploidy, but rather trait variations were mainly genotype-specific. Additionally, it is shown that paternal contribution is very important for trait success, even though all offspring are genetically identical to the mother plant. This harbors implications for the introduction of apomixis into crop plants, considering the effects of paternal contribution during asexual reproduction. Nevertheless, polyploidy is an efficient way to buffer deleterious mutations, but the flexibility of diploid apomicts of the genus Boechera for rare sexual events contributes to their success in nature.

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References

  • Adams S, Vinkenoog R, Spielman M, Dickinson HG, Scott RJ (2000) Parent-of-origin effects on seed development in Arabidopsis thaliana require DNA methylation. Development 127:2493–2502

    PubMed  CAS  Google Scholar 

  • Adamski NM, Anastasiou E, Eriksson S, O’Neill CM, Lenhard M (2009) Local maternal control of seed size by KLUH/CYP78A5-dependent growth signalling. Proc Natl Acad Sci USA 106:20115–20120

    PubMed  CAS  Google Scholar 

  • Aliyu OM, Schranz ME, Sharbel TF (2010) Quantitative variation for apomixis components in the genus Boechera. Am J Bot 97:1719–1731

    Article  PubMed  Google Scholar 

  • Alonso-Blanco C, Blankestijn-de Vries H, Hanhart CJ, Koornneef M (1999) Natural allelic variation at seed size loci in relation to other life history traits of Arabidopsis thaliana. Proc Natl Acad Sci USA 96:4710–4717

    Article  PubMed  CAS  Google Scholar 

  • Al-Shehbaz IA, Windham MD (2006) New and noteworthy species of Boechera (Brassicaceae) I: sexual diploids. Harv Paper Bot 11:61–88

    Article  Google Scholar 

  • Al-Shehbaz IA, Windham MD (2007a) New and noteworthy species of Boechera (Brassicaceae) II: apomictic hybrids. Harv Paper Bot 11:257–274

    Article  Google Scholar 

  • Al-Shehbaz IA, Windham MD (2007b) New and noteworthy species of Boechera (Brassicaceae) III: additional sexual diploids and apomictic hybrids. Harv Paper Bot 12:235–257

    Article  Google Scholar 

  • Asham TL, Penet L (2007) Direct and indirect effects of a sex-biased antagonist on male and female fertility: consequences for reproductive trait evolution in a gender dimorphic plant. Am Nat 169:595–608

    Article  Google Scholar 

  • Asker S, Jerling L (1992) Apomixis in plants. CRC Press, Boca Raton

    Google Scholar 

  • Bierzychudek P (1985) Patterns in plant parthenogenesis. Experientia 41:1255–1264

    Article  Google Scholar 

  • Böcher TW (1951) Cytological and embryological studies in the amphi-apomictic Arabis holboellii complex. K Dan Vidensk Selsk 6:1–59

    Google Scholar 

  • Bretagnolle F, Lumaret R (1995) Bilateral polyploidization in Dactylis glomerata L. subsp. lusitanica: occurrence, morphological and genetic characteristics of first polyploids. Euphytica 84:197–207

    Article  Google Scholar 

  • Carman JG (1997) Asynchronous expression of duplicate genes in angiosperms may cause apomixis, bispory, tetraspory, and polyembryony. Biol J Linn Soc 61:51–94

    Article  Google Scholar 

  • Casco H, Dias LS (2008) Estimating seed mass and volume from linear dimensions of seeds. Seed Sci Technol 36:230–236

    Google Scholar 

  • Chambers JM, Cleveland WS, Kleiner B, Tukey PA (1983) Graphical methods for data analysis. Duxbury Press, Boston

  • Comai L (2005) The advantages and disadvantages of being polyploid. Nat Rev Genet 6:836–846

    Article  PubMed  CAS  Google Scholar 

  • Cortex Nova (2005) DigiShape. Software for automatic morphometry. Cortex Nova, Bydgoszcz. http://www.cortex.nova.pro.wp.pl

  • Cosendai AC, Hörandl E (2010) Cytotype stability, facultative apomixis and geographical parthenogenesis in Ranunculus kuepferi (Ranunculaceae). Ann Bot 105:457–470

    Article  PubMed  Google Scholar 

  • Crawley MJ (2005) Statistics: an introduction using R. Wiley, Chichester, pp 181–185

    Book  Google Scholar 

  • D’Souza TG, Storhas M, Schulenburg H, Beukeboom LW, Michiels NK (2004) Occasional sex in an ‘asexual’ polyploid hermaphrodite. Proc R Soc London Ser B 271:1001–1007

    Article  Google Scholar 

  • de Jong TJ, Scott RJ (2007) Parental conflict does not necessarily lead to the evolution of imprinting. Trends Plant Sci 12:439–443

    Article  PubMed  Google Scholar 

  • de Jong TJ, Hermans CM, van der Veen-van Wijk KAM (2011) Paternal effects on seed mass in Arabidopsis thaliana. Plant Biol 13:71–77

    Article  PubMed  Google Scholar 

  • de Kovel CGF, de Jong G (1999) Responses of sexual and apomictic genotypes of Taraxacum officinale to variation in light. Plant Biol 1:541–546

    Article  Google Scholar 

  • Dilkes BP, Comai L (2004) A differential dosage hypothesis for parental effects in seed development. Plant Cell 16:3174–3180

    Article  PubMed  Google Scholar 

  • Dobeš C, Mitchell-Olds T, Koch MA (2004a) Intraspecific diversification in North American Boechera stricta (= Arabis drummondii), Boechera × divaricarpa, and Boechera holboellii (Brassicaceae) inferred from nuclear and chloroplast molecular markers-an integrative approach. Am J Bot 91:2087–2101

    Article  PubMed  Google Scholar 

  • Dobeš C, Mitchell-Olds T, Koch MA (2004b) Extensive chloroplast haplotype variation indicates Pleistocene hybridization and radiation of North American Arabis drummondii, A. xdivericarpa, and A. holboellii (Brassicaceae). Mol Ecol 13:349–370

    Article  PubMed  Google Scholar 

  • Dobritsa AA, Lei Z, Nishikawa SI, Urbanczyk-Wochniak E, Huhman DV, Preuss D, Sumner LW (2010) LAP5 and LAP6 encode anther-specific proteins with similarity to chalcone synthase essential for pollen exine development in Arabidopsis. Plant Physiol 153:937–955

    Article  PubMed  CAS  Google Scholar 

  • Dorcey E, Urbez C, Blázquez MA, Carbonell J, Perez-Amador MA (2009) Fertilization-dependent auxin response in ovules triggers fruit development through the modulation of gibberellin metabolism in Arabidopsis. Plant J 58:318–332

    Article  PubMed  CAS  Google Scholar 

  • Dorn RD (1984) Vascular plants of montana. Mountain West Publishing, Cheyenne

    Google Scholar 

  • Dumas C, Rogowsky P (2008) Fertilization and early seed formation. C R Biol 331:715–725

    Article  PubMed  Google Scholar 

  • Garcia D, Fitz Gerald JN, Berger F (2005) Maternal control of integument cell elongation and zygotic control of endosperm growth are coordinated to determine seed size in Arabidopsis. Plant Cell 17:52–60

    Article  PubMed  CAS  Google Scholar 

  • Greilhuber J, Doležel J (2009) 2C or not 2C: a closer look at the nuclei and their DNA content. Chromosoma 188:391–400

    Article  Google Scholar 

  • Grimanelli D, Leblanc O, Perotti E, Grossniklaus U (2001) Developmental genetics of gametophytic apomixis. Trends Genet 17:597–604

    Article  PubMed  CAS  Google Scholar 

  • Gustafsson Å (1946–1947) Apomixis in higher plants. I-III Lunds Univ Årsskr 2:42

  • Hahn SK, Bai KV, Asiedu R (1990) Tetraploids, triploids, and 2n pollen from diploid interspecific crosses with cassava. Theor Appl Genet 79:433–439

    Article  Google Scholar 

  • Haig D, Westoby M (1991) Genomic imprinting in endosperm: its effects on seed development in crosses between different ploidies of the same species, and its implications for the evolution of apomixis. Philos Trans R Soc B 333:1–13

    Article  Google Scholar 

  • Hochholdinger F, Hoecker N (2007) Towards the molecular basis of heterosis. Trends Plant Sci 12:427–432

    Google Scholar 

  • House C, Roth C, Hunt J, Kover PX (2010) Paternal effects in Arabidopsis indicate that offspring can influence their own size. Proc R Soc London Ser B 277:2885–2893

    Article  Google Scholar 

  • Izmaiłow R (1996) Reproductive strategy in the Ranunculus auricomus complex (Ranunculaceae). Acta Soc Bot Pol 65:167–170

    Google Scholar 

  • Jaranowski J, Kalasa M (1971) Comparative analysis of fertility in several Trifolium, Melilotus, Medicago and Trigonella species and forms on a di- and tetraploid level. Genet Pol 12:1–16

    Google Scholar 

  • Jofuku KD, Omidyar PK, Gee Z, Okamuro JK (2005) Control of seed mass and seed yield by the floral homeotic gene APETALA2. Proc Natl Acad Sci USA 102:3117–3122

    Article  PubMed  CAS  Google Scholar 

  • Kantama L, Sharbel TF, Schranz EM, Mitchell-Olds T, De Vries S, De Jong H (2007) Diploid apomicts of the Boechera holboellii complex display large scale chromosome substitutions and aberrant chromosomes. Proc Natl Acad Sci USA 104:14026–14031

    Article  PubMed  CAS  Google Scholar 

  • Kao RH (2007) Asexuality and the coexistence of cytotypes. New Phytol 175:764–772

    Article  PubMed  Google Scholar 

  • Kearney M (2005) Hybridization, glaciation and geographical parthenogenesis. Trends Ecol Evol 20:495–502

    Article  PubMed  Google Scholar 

  • Kiefer C, Dobeš C, Sharbel TF, Koch MA (2009) Phylogeographic structure of the chloroplast DNA gene pool in North American Boechera—a genus and continental-wide perspective. Mol Phylogenet Evol 52:303–311

    Article  PubMed  CAS  Google Scholar 

  • Koch M, Bishop J, Mitchell-Olds T (1999) Molecular systematics and evolution of Arabidopsis and Arabis. Plant Biol 1:529–537

    Article  Google Scholar 

  • Koch M, Dobeš C, Mitchell-Olds T (2003) Multiple hybrid formation in natural populations: concerted evolution of the internal transcribed spacer of nuclear ribosomal DNA (ITS) in North American Arabis divaricarpa (Brassicaceae). Mol Biol Evol 20:338–350

    Article  PubMed  CAS  Google Scholar 

  • Kuspira J, Bhambhani RN, Shimada T (1985) Genetic and cytogenetic analyses of the A genome of Tritium gonococcus. I. Cytology, breeding behaviour, fertility, and morphology of induced autotetraploids. Can J Genet Cytol 27:51–63

    Google Scholar 

  • Levin DA (1983) Polyploidy and novelty in flowering plants. Am Nat 122:1–25

    Article  Google Scholar 

  • Levin, DA (2002) The role of chromosomal change in plant evolution. Oxford University Press, New York

  • Li Y, Zheng L, Corke F, Smith C, Bevan MM (2008) Control of final seed and organ size by the DA1 gene family in Arabidopsis thaliana. Genes Dev 22:1331–1336

    Article  PubMed  CAS  Google Scholar 

  • Lin BY (1984) Ploidy barrier to endosperm development in maize. Genetics 107:103–115

    PubMed  CAS  Google Scholar 

  • Lo Eugenia YY, Stefanovic S, Dickinson TA (2009) Population genetic structure of diploid sexual and polyploid apomictic hawthorns (Crataegus; Rosaceae) in the Pacific Northwest. Mol Ecol 18:1145–1160

    Article  PubMed  CAS  Google Scholar 

  • Lynch M, Gabriel W (1983) Phenotypic evolution and parthenogenesis. Am Nat 122:745–764

    Article  Google Scholar 

  • Matzk F, Meister A, Schubert I (2000) An efficient screen for reproductive pathways using mature seeds of monocots and dicots. Plant J 21:97–108

    Article  PubMed  CAS  Google Scholar 

  • Mogie M, Britton NF, Stewart-Cox JA (2007) Asexuality, polyploidy and the male function. In: Hörandl E, Grossniklaus U, van Dijk P, Sharbel TF (eds) Evolution, mechanisms and perspectives. ARG Gantner Verlag, Apomixis

    Google Scholar 

  • Naumova TN, van der Laak J, Osadtchiy J, Matzk F, Kravtchenko A, Bergervoet J, Ramulu KS, Boutilier K (2001) Reproductive development in apomictic populations of Arabis holboellii (Brassicaceae). Sex Plant Reprod 14:195–200

    Article  Google Scholar 

  • Nogler GA (1984) Genetics of apospory in apomictic Ranunculus auricomus: 5 Conclusion. Bot Helv 94:411–423

    Google Scholar 

  • Ozias-Akins P, van Dijk PJ (2007) Mendelian genetics of apomixis in plants. Annu Rev Genet 41:509–537

    Article  PubMed  CAS  Google Scholar 

  • Pal M, Khoshoo TN (1977) Evolution and improvement of cultivated amaranths. VIII. Induced autotetraploidy in grain types. Zeitschrift für Pflanzenzüchtung 78:135–148

    Google Scholar 

  • Petit C, Lesbros P, Ge X, Thompson JD (1997) Variation in flowering phenology and selfing rate across a contact zone between diploid and tetraploid Arrhenatherum elatius (Poaceae). Heredity 79:31–40

    Article  Google Scholar 

  • Pichot C, El Maataoui M, Raddi S, Raddi P (2001) Surrogate mother for endangered Cupressus. Nature 412:39

    Article  PubMed  CAS  Google Scholar 

  • Quarin CL, Espinoza F, Martinez EJ, Pessino SC, Bovo OA (2001) A rise of ploidy level induces the expression of apomixis in Paspalum notatum. Sex Plant Reprod 13:243–249

    Article  Google Scholar 

  • Ramsey J, Schemske DW (2002) Neopolyploidy in flowering plants. Annu Rev Eco Sys 33:589–639

    Article  Google Scholar 

  • Roff DA (2006) Computer-intensive methods of data analysis in biology. Cambridge University Press, New York

    Book  Google Scholar 

  • Rollins RC (1981) Studies on Arabis (Cruciferae) of Western North America. Syst Bot 6:55–64

    Article  Google Scholar 

  • R Development Core Team (2007) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, http://www.R-project.org

  • Schranz ME, Osborn TC (2004) De novo variation of life-history traits and responses to growth conditions of resynthesized polyploid Brassica napus (Brassicaceae). Am J Bot 91:174–183

    Article  PubMed  Google Scholar 

  • Schranz ME, Kantama L, De Jong H, Mitchell-Olds T (2006) Asexual reproduction in a close relative of Arabidopsis: a genetic investigation of apomixis in Boechera (Brassicaceae). New Phytol 171:425–438

    Article  PubMed  Google Scholar 

  • Schruff MC, Spielman M, Tiwari S, Adams S, Fenby N, Scott RJ (2006) The AUXIN RESPONSE FACTOR 2 gene of Arabidopsis links auxin signalling, cell division, and the size of seeds and other organs. Development 133:251–261

    Article  PubMed  CAS  Google Scholar 

  • Scott RJ, Spielman M, Bailey J, Dickinson HG (1998) Parent-of-origin effects on seed development in Arabidopsis thaliana. Development 125:3329–3341

    PubMed  CAS  Google Scholar 

  • Scott RJ, Armstrong SJ, Doughty J, Spielman M (2008) Double fertilization in Arabidopsis thaliana involves a polyspermy block on the egg but not the central cell. Mol Plant 1:611–619

    Article  PubMed  CAS  Google Scholar 

  • Segraves KA, Thompson JN (1999) Plant polyploidy and pollination: floral traits and insect visits to diploid and tetraploid Heuchera grossulariifolia. Evolution 53:1114–1127

    Article  Google Scholar 

  • Sharbel TF, Mitchell-Olds T (2001) Recurrent polyploid origins and chloroplast phylogeography in the Arabis holboellii complex (Brassicaceae). Heredity 87:59–68

    Article  PubMed  CAS  Google Scholar 

  • Sharbel TF, Voigt ML, Mitchell-Olds T, Kantama L, de Jong H (2004) Is the aneuploid chromosome in an apomictic Boechera holboellii a genuine B chromosome? Cytogenet Genome Res 106:173–183

    Article  PubMed  CAS  Google Scholar 

  • Sharbel TF, Mitchell-Olds T, Dobeš C, Kantama L, de Jong H (2005) Biogeographic distribution of polyploidy and B chromosomes in the apomictic Boechera holboellii complex. Cytogenet Genome Res 109:283–292

    Article  PubMed  CAS  Google Scholar 

  • Shaw RG, Mitchell-Olds T (1993) ANOVA for unbalanced data: an overview. Ecology 74:1638–1645

    Google Scholar 

  • Simons AM, Johnston MO (2003) Suboptimal timing of reproduction in Lobelia inflata may be a conservative bet-hedging strategy. J Evol Biol 16:233–243

    Article  PubMed  CAS  Google Scholar 

  • Soltis DE, Soltis PS, Tate JA (2003) Advances in the study of polyploidy since plant speciation. New Phytol 161:173–191

    Article  Google Scholar 

  • Song BH, Clauss MJ, Pepper A, Mitchell-Olds T (2006) Geographic patterns of microsatellite variation in Boechera stricta, a close relative of Arabidopsis. Mol Ecol 15:357–369

    Article  PubMed  CAS  Google Scholar 

  • Suzuki T, Masaoka K, Nishi M, Nakamura K, Ishiguro S (2008) Identification of kaonashi mutants showing abnormal pollen exine structure in Arabidopsis thaliana. Plant Cell Physiol 49:1465–1477

    Article  PubMed  CAS  Google Scholar 

  • Tas ICQ, van Dijk PJ (1999) Crosses between sexual and apomictic dandelions (Taraxacum). I. The inheritance of apomixis. Heredity 83:707–714

    Article  PubMed  Google Scholar 

  • Van Dijk P (2003) Ecological and evolutionary opportunities of apomixis: insight from Taraxacum and Chondrilla. Philos Trans R Soc Lon B 358:113–1121

    Google Scholar 

  • Vandel A (1928) La parthénogénèse géographique: contribution à l’édude biologique et cytologique de la parthénogénèse naturelle. Bull Biol Fr Belg 62:64–281

    Google Scholar 

  • Venable DL (1992) Size-number trade-offs and the variation of seed size with plant resource status. Am Nat 140:287–304

    Article  Google Scholar 

  • Voigt ML, Melzer M, Rutten T, Mitchell-Olds T, Sharbel TF (2007) Gametogenesis in the apomictic Boechera holboellii complex: the male perspective. In: Hörandl E, Grossniklaus U, van Dijk P, Sharbel TF (eds) Apomixis: evolution, mechanisms and perspectives. ARG Gantner Verlag, pp 235–258

  • Wagner GP, Gabriel W (1990) Quantitative variation in finite parthenogenetic populations: what stops Muller’s ratchet in the absence of recombination? Evolution 44:715–731

    Article  Google Scholar 

  • Whitton JS, Christopher ÂJ, Baack EÂJ, Otto SÂP (2008) The dynamic nature of apomixis in the angiosperms. Int J Plant Sci 169:169–182

    Article  Google Scholar 

  • Xiao W, Brown RC, Lemmon BE, Harada JJ, Goldberg RB, Fischer LR (2006) Regulation of seed size by hypomethylation of maternal and paternal genomes. Plant Physiol 142:1160–1168

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We would like to thank H. Block, V. Katzorke and L. Börner for technical assistance. We furthermore extend our gratitude to Tom Mitchell-Olds for providing seed material, to Marcus Koch for help with genotype identification, and to Johann Greilhuber for his assistance in DNA content terminology. MP was partly supported by scholarship DAAD/IAESTE and by a grant for short visits of young researchers from Nicolaus Copernicus University, Poland

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The authors declare that they have no conflict of interest.

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Correspondence to Marie-Luise Voigt-Zielinski.

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Voigt-Zielinski, ML., Piwczyński, M. & Sharbel, T.F. Differential effects of polyploidy and diploidy on fitness of apomictic Boechera . Sex Plant Reprod 25, 97–109 (2012). https://doi.org/10.1007/s00497-012-0181-8

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