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Bimodality of stable and plastic traits in plants

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Abstract

Key message

We discovered an unexpected mode of bimodal distribution of stable and plastic traits, which was consistent for homologous traits of 32 varieties of seven species both in well-irrigated fields and dry conditions.

Abstract

We challenged archived genetic mapping data for 36 fruit, seed, flower and yield traits in tomato and found an unexpected bimodal distribution in one measure of trait variability, the mean coefficient of variation, with some traits being consistently more variable than others. To determine the degree of conservation of this distribution among higher plants, we compared 18 homologous phenotypes, including yield and seed production, across different crop species grown in a common ‘crop garden’ experiment. The set included 32 varieties of tomato, eggplant, pepper, melon, watermelon, sunflower and maize. Estimates of canalization were obtained using a ‘canalization replication’ experimental design that generated multiple estimates of the coefficient of variation of traits, as well as their reaction norms in optimal and water-stressed field plots. A common pattern of bimodal distribution of stable and plastic traits was observed for all the varieties and for a wild weed (Solanum nigrum). We propose that canalization profiles of traits in a variety of taxa were ancestrally selected to maximize adaptation and reproductive success.

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References

  • Allard RW, Bradshaw AD (1964) Implications of genotype-environmental interactions in applied plant breeding. Crop Sci 4:503–508

    Article  Google Scholar 

  • Becker HC, Leon J (1988) Stability analysis in plant breeding. Plant Breed 101:1–23

    Article  Google Scholar 

  • Bradshaw AD (1965) Evolutionary significance of phenotypic plasticity in plants. Adv Genet 13:115–155

    Google Scholar 

  • Debat V, David P (2001) Mapping phenotypes: canalization, plasticity and developmental stability. Trends Ecol Evol 16:555–561

    Article  Google Scholar 

  • Dworkin I (2005) Canalization, cryptic variation, and developmental buffering: a critical examination and analytical perspective. Var A Cent Concept Biol. doi:10.1093/jxb/erl301

    Google Scholar 

  • Eshed Y, Zamir D (1995) An introgression line population of Lycopersicon pennellii in the cultivated tomato enables the identification and fine mapping of yield-associated QTL. Genetics 141:1147–1162

    CAS  PubMed  PubMed Central  Google Scholar 

  • Félix MA, Barkoulas M (2015) Pervasive robustness in biological systems. Nat Rev Genet 16:483–496

    Article  PubMed  Google Scholar 

  • Flint-Garcia SA, Buckler ES, Tiffin P, Ersoz E, Springer NM (2009) Heterosis is prevalent for multiple traits in diverse maize germplasm. PLoS One. doi:10.1371/journal.pone.0007433

    PubMed  PubMed Central  Google Scholar 

  • Fridman E (2015) Consequences of hybridization and heterozygosity on plant vigor and phenotypic stability. Plant Sci 232:35–40

    Article  CAS  PubMed  Google Scholar 

  • Geiler-Samerotte KA, Zhu YO, Goulet BE, Hall DW, Siegal ML (2016) Selection transforms the landscape of genetic variation interacting with Hsp90. PLoS Biol 14:e2000465

    Article  PubMed  PubMed Central  Google Scholar 

  • Hall MC, Dworkin I, Ungerer MC, Purugganan M (2007) Genetics of microenvironmental canalization in Arabidopsis thaliana. Proc Natl Acad Sci USA 104:13717–13722

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jimenez-Gomez JM, Corwin JA, Joseph B, Maloof JN, Kliebenstein DJ (2011) Genomic analysis of QTLs and genes altering natural variation in stochastic noise. PLoS Genet 7:e1002295

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Klebs G (1909) The influence of environment on the form of plants. Darwin and modern science. Cambridge University Press, London and New York, pp 223–246

    Google Scholar 

  • Lacaze X, Hayes PM, Korol A (2009) Genetics of phenotypic plasticity: QTL analysis in barley, Hordeum vulgare. Heredity 102:163–173

    Article  CAS  PubMed  Google Scholar 

  • Lempe J, Lachowiec J, Sullivan AM, Queitsch C (2013) Molecular mechanisms of robustness in plants. Curr Opin Plant Biol 16:62–69

    Article  CAS  PubMed  Google Scholar 

  • Lerner IM (1954) Genetic homeostasis. Oliver and Boyd, Edinburgh

    Google Scholar 

  • Lippman ZB, Zamir D (2007) Heterosis: revisiting the magic. Trends Genet 23:60–66

    Article  CAS  PubMed  Google Scholar 

  • Mühleisen J, Piepho HP, Maurer HP, Longin CFH, Reif JC (2014) Yield stability of hybrids versus lines in wheat, barley, and triticale. Theor Appl Genet 127:309–316

    Article  PubMed  Google Scholar 

  • Nilsson-Ehle H (1914) Vilka erfarenheter hava hittills vunnits rorande mojligheten av vaxters acklimatisering. Kgl Landtbruks-Akad Handl Tidskr 63:537–572

    Google Scholar 

  • Polly PD (1998) Variability in mammalian dentitions: size-related bias in the coefficient of variation. Biol J Linn Soc 64:83–99

    Article  Google Scholar 

  • Rendel JM (1967) Canalization and gene control. Logos Press, London

    Google Scholar 

  • Rutherford SL, Lindquist S (1998) Hsp90 as a capacitor for morphological evolution. Nature 396:336–342

    Article  CAS  PubMed  Google Scholar 

  • Schauer N, Semel Y, Balbo I, Steinfath M, Repsilber D, Selbig J, Pleban T, Zamir D, Fernie AR (2008) Mode of inheritance of primary metabolic traits in tomato. Plant Cell 20:509–523

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Semel Y, Nissenbaum J, Menda N, Zinder M, Krieger U, Issman N, Pleban T, Lippman Z, Gur A, Zamir D (2006) Overdominant quantitative trait loci for yield and fitness in tomato. Proc Natl Acad Sci USA 103:12981–12986

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shen X, Pettersson M, Rönnegård L, Carlborg Ö (2012) Inheritance beyond plain heritability: variance-controlling genes in arabidopsis thaliana. PLoS Genet 8:e1002839

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Turnbull LA, Santamaria L, Martorell T, Rallo J, Hector A (2006) Seed size variability: from carob to carats. Biol Lett 2:397–400

    Article  PubMed  PubMed Central  Google Scholar 

  • Waddington CH (1942) Canalization of development and the inheritance of acquired characters. Nature 150:563–565

    Article  Google Scholar 

  • Waddington CH (1961) Genetic assimilation. Adv Genet 10:257–293

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This research was supported by a grant from the European Research Council—Advanced Grant entitled YIELD (ERC 294691) the German-Israeli Project Cooperation program (DFG DIP project number FE552/12-1 and by the Israel Science Foundation (ISF; 653/15). We dedicate this paper to the memory of Mr. Gabi Gara who designed and managed our field trials, and much more.

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Authors and Affiliations

  1. The Institute of Plant Sciences and Genetics in Agriculture, Faculty of Agriculture, The Hebrew University of Jerusalem, PO Box 12, 76100, Rehovot, Israel

    Josef Fisher, Elad Bensal & Dani Zamir

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  1. Josef Fisher
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  2. Elad Bensal
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  3. Dani Zamir
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Correspondence to Dani Zamir.

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The authors declare that they have no conflict of interest.

Additional information

Communicated by Heiko C. Becker.

Raw data is available from the Dryad Digital Repository.

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Fisher, J., Bensal, E. & Zamir, D. Bimodality of stable and plastic traits in plants. Theor Appl Genet 130, 1915–1926 (2017). https://doi.org/10.1007/s00122-017-2933-1

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  • DOI: https://doi.org/10.1007/s00122-017-2933-1

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