Abstract
Aims
Nascent polyploids, or neopolyploids, frequently arise within diploid plant lineages and are expected to experience increased requirements for growth-limiting nutrients because of building a larger genome. Because this may have important consequences for the ecology of neopolyploids, we need studies that track the lifetime fitness effects of whole genome duplication. Here we investigated how multiple origins of neopolyploidy and nutrient supply rate affected fitness-related traits of Arabidopsis thaliana.
Methods
We investigated the interaction between cytotype, independent neopolyploid origins, and soil fertility by conducting a greenhouse experiment with five nutrient treatments that varied nitrogen and phosphorus supply. We compared biomass, flowering phenology, fecundity, average mass per seed, and offspring germination rates of diploids and their descendent neotetraploids from four independent origins.
Results
The results supported the hypothesis that neopolyploidy increases nutrient limitation. Diploids outpaced their neotetraploid descendants in growth and composite fitness in all nutrient treatments except with high supply of nitrogen and phosphorus, where neotetraploid growth and composite fitness exceeded diploids. In contrast, we did not detect an interaction between cytotype and nutrient treatment for flowering phenology, but neotetraploids flowered later, and low nutrient supply caused earlier flowering. We additionally found that the trait responses of neotetraploids were strongly contingent on their independent, maternal origin.
Conclusions
Polyploidy has myriad effects on plant physiology, but few studies have tested how neopolyploid-induced physiological changes can affect plant environmental interactions. By showing that neopolyploid fitness is more constrained by nutrient supply, we conclude that neotetraploidy increases nutrient limitation in A. thaliana.
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References
Abbott RJ, Gomes MF (1989) Population genetic structure and outcrossing rate of Arabidopsis thaliana (L) Heynh. Heredity 62:411–418. https://doi.org/10.1038/hdy.1989.56
Arrigo N, Barker MS (2012) Rarely successful polyploids and their legacy in plant genomes. Curr Opin Plant Biol 15:140–146. https://doi.org/10.1016/j.pbi.2012.03.010
Bates D, Machler M, Bolker BM, Walker SC (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48. https://doi.org/10.18637/jss.v067.i01
Beaulieu JM, Leitch IJ, Knight CA (2007) Genome size evolution in relation to leaf strategy and metabolic rates revisited. Ann Bot 99:495–505. https://doi.org/10.1093/aob/mcl271
Birchler JA, Veitia RA (2010) The gene balance hypothesis: implications for gene regulation, quantitative traits and evolution. New Phytol 186:54–62. https://doi.org/10.1111/j.1469-8137.2009.03087.x
Bretagnolle F, Thompson JD (1996) An experimental study of ecological differences in winter growth between sympatric diploid and autotetraploid Dactylis glomerata. J Ecol 84:343–351. https://doi.org/10.2307/2261197
Cacco G, Ferrari G, Lucci GC (1976) Uptake efficiency of roots in plants at different ploidy levels. J Agric Sci 87:585–589. https://doi.org/10.1017/s0021859600033219
Caceres ME, De Pace C, Mugnozza GTS, Kotsonis P, Ceccarelli M, Cionini PG (1998) Genome size variations within Dasypyrum villosum: correlations with chromosomal traits, environmental factors and plant phenotypic characteristics and behaviour in reproduction. Theor Appl Genet 96:559–567. https://doi.org/10.1007/s001220050774
Cai Q, Ji CJ, Yan ZB, Jiang XX, Fang JY (2017) Anatomical responses of leaf and stem of Arabidopsis thaliana to nitrogen and phosphorus addition. J Plant Res 130:1035–1045. https://doi.org/10.1007/s10265-017-0960-2
Campbell DR (1991) Effects of floral traits on sequential components of fitness in Ipomopsis aggregata. Am Nat 137:713–737. https://doi.org/10.1086/285190
Chung J, Lee JH, Arumuganathan K, Graef GL, Specht JE (1998) Relationships between nuclear DNA content and seed and leaf size in soybean. Theor Appl Genet 96:1064–1068. https://doi.org/10.1007/s001220050840
Dhooghe E, Van Laere K, Eeckhaut T, Leus L, Van Huylenbroeck J (2011) Mitotic chromosome doubling of plant tissues in vitro. Plant Cell Tissue Org Cult 104:359–373. https://doi.org/10.1007/s11240-010-9786-5
Fowler NL, Levin DA (2016) Critical factors in the establishment of allopolyploids. Am J Bot 103:1236–1251. https://doi.org/10.3732/ajb.1500407
Guignard MS, Nichols RA, Knell RJ, Macdonald A, Romila CA, Trimmer M, Leitch IJ, Leitch AR (2016) Genome size and ploidy influence angiosperm species' biomass under nitrogen and phosphorus limitation. New Phytol 210:1195–1206. https://doi.org/10.1111/nph.13881
Guignard MS, Leitch AR, Acquisti C, Eizaguirre C, Elser J, Hessen DO, Jeyasingh PD (2017) Impacts of nitrogen and phosphorus: from genomes to natural ecosystems and agriculture. Front Ecol Evol 5:70
Gusewell S (2004) N : P ratios in terrestrial plants: variation and functional significance. New Phytol 164:243–266. https://doi.org/10.1111/j.1469-8137.2004.01192.x
Hessen DO, Jeyasingh PD, Neiman M, Weider LJ (2010) Genome streamlining and the elemental costs of growth. Trends Ecol Evol 25:75–80. https://doi.org/10.1016/j.tree.2009.08.004
Hoffmann MH, Bremer M, Schneider K, Burger F, Stolle E, Moritz G (2003) Flower visitors in a natural population of Arabidopsis thaliana. Plant Biol 5:491–494. https://doi.org/10.1055/s-2003-44784
Husband BC, Sabara HA (2004) Reproductive isolation between autotetraploids and their diploid progenitors in fireweed, Chamerion angustifolium (Onagraceae). New Phytol 161:703–713. https://doi.org/10.1046/j.1469-8137.2004.00998.x
Husband BC, Baldwin SJ, Sabara HA (2016) Direct vs. indirect effects of whole-genome duplication on prezygotic isolation in Chamerion angustifolium: implications for rapid speciation. Am J Bot 103:1259–1271. https://doi.org/10.3732/ajb.1600097
Koerselman W, Meuleman AFM (1996) The vegetation N:P ratio: a new tool to detect the nature of nutrient limitation. J Appl Ecol 33:1441–1450. https://doi.org/10.2307/2404783
Leitch AR, Leitch IJ (2008) Perspective - genomic plasticity and the diversity of polyploid plants. Science 320:481–483. https://doi.org/10.1126/science.1153585
Levin DA (1983) Polyploidy and novelty in flowering plants. Am Nat 122:1–25. https://doi.org/10.1086/284115
Levin DA (2019) Why polyploid exceptionalism is not accompanied by reduced extinction rates. Plant Syst Evol 305:1–11. https://doi.org/10.1007/s00606-018-1552-x
Levin DA, Soltis DE (2018) Factors promoting polyploid persistence and diversification and limiting diploid speciation during the K-Pg interlude. Curr Opin Plant Biol 42:1–7. https://doi.org/10.1016/j.pbi.2017.09.010
Lewis WM (1985) Nutrient scarcity as an evolutionary cause of haploidy. Am Nat 125:692–701
Mayrose I, Zhan SH, Rothfels CJ, Arrigo N, Barker MS, Rieseberg LH, Otto SP (2015) Methods for studying polyploid diversification and the dead end hypothesis: a reply to Soltis et al. (2014). New Phytol 206:27–35. https://doi.org/10.1111/nph.13192
Munguia-Rosas MA, Ollerton J, Parra-Tabla V, De-Nova JA (2011) Meta-analysis of phenotypic selection on flowering phenology suggests that early flowering plants are favoured. Ecol Lett 14:511–521. https://doi.org/10.1111/j.1461-0248.2011.01601.x
Muntzing A, Tometorp G, Mundt-Petersen K (1936) Tetraploid barley produced by heat treatment. Hereditas 22:401–406
Osborn TC, Pires JC, Birchler JA, Auger DL, Chen ZJ, Lee HS, Comai L, Madlung A, Doerge RW, Colot V, Martienssen RA (2003) Understanding mechanisms of novel gene expression in polyploids. Trends Genet 19:141–147. https://doi.org/10.1016/s0168-9525(03)00015-5
Oswald BP, Nuismer SL (2011) Neopolyploidy and diversification in Heuchera grossulariifolia. Evolution 65:1667–1679. https://doi.org/10.1111/j.1558-5646.2010.01208.x
Otto SP, Whitton J (2000) Polyploid incidence and evolution. Annu Rev Genet 34:401–437. https://doi.org/10.1146/annurev.genet.34.1.401
Pacey EK, Maherali H, Husband BC (2020) The influence of experimentally induced polyploidy on the relationships between endopolyploidy and plant function in Arabidopsis thaliana. Ecol Evol 10:198–216. https://doi.org/10.1002/ece3.5886
Parisod C, Holderegger R, Brochmann C (2010) Evolutionary consequences of autopolyploidy. New Phytol 186:5–17. https://doi.org/10.1111/j.1469-8137.2009.03142.x
Petit C, Lesbros P, Ge XJ, 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. https://doi.org/10.1038/sj.hdy.6881850
Platt A, Horton M, Huang YS, Li Y, Anastasio AE, Mulyati NW, Agren J, Bossdorf O, Byers D, Donohue K, Dunning M, Holub EB, Hudson A, Le Corre V, Loudet O, Roux F, Warthmann N, Weigel D, Rivero L, Scholl R, Nordborg M, Bergelson J, Borevitz JO (2010) The scale of population structure in Arabidopsis thaliana. PLoS Genet 6:8. https://doi.org/10.1371/journal.pgen.1000843
Porturas LD, Anneberg TJ, Cure AE, Wang SP, Althoff DM, Segraves KA (2019) A meta-analysis of whole genome duplication and theeffects on flowering traits in plants. Am J Bot 106:469–476. https://doi.org/10.1002/ajb2.1258
R Core Team (2019) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Ramsey J, Schemske DW (1998) Pathways, mechanisms, and rates of polyploid formation in flowering plants. Annu Rev Ecol Syst 29:467–501. https://doi.org/10.1146/annurev.ecolsys.29.1.467
Richardson BA, Ortiz HG, Carlson SL, Jaeger DM, Shaw NL (2015) Genetic and environmental effects on seed weight in subspecies of big sagebrush: applications for restoration. Ecosphere 6:13. https://doi.org/10.1890/es15-00249.1
Rodriguez DJ (1996) A model for the establishment of polyploidy in plants. Am Nat 147:33–46. https://doi.org/10.1086/285838
Segraves KA, Thompson JN (1999) Plant polyploidy and pollination: floral traits and insect visits to diploid and tetraploid Heuchera grossulariifolia. Evolution 53:1114–1127. https://doi.org/10.2307/2640816
Simon-Porcar VI, Silva JL, Meeus S, Higgins JD, Vallejo-Marin M (2017) Recent autopolyploidization in a naturalized population of Mimulus guttatus (Phrymaceae). Bot J Linn Soc 185:189–207. https://doi.org/10.1093/botlinnean/box052
Šmarda P, Hejcman M, Brezinova A, Horova L, Steigerova H, Zedek F, Bures P, Hejcmanova P, Schellberg J (2013) Effect of phosphorus availability on the selection of species with different ploidy levels and genome sizes in a long-term grassland fertilization experiment. New Phytol 200:911–921. https://doi.org/10.1111/nph.12399
Solhaug EM, Ihinger J, Jost M, Gamboa V, Marchant B, Bradford D, Doerge RW, Tyagi A, Replogle A, Madlung A (2016) Environmental regulation of Heterosis in the allopolyploid Arabidopsis suecica. Plant Physiol 170:2251–2263. https://doi.org/10.1104/pp.16.00052
Soltis DE, Soltis PS (1999) Polyploidy: recurrent formation and genome evolution. Trends Ecol Evol 14:348–352. https://doi.org/10.1016/s0169-5347(99)01638-9
Sperfeld E, Raubenheimer D, Wacker A (2016) Bridging factorial and gradient concepts of resource co-limitation: towards a general framework applied to consumers. Ecol Lett 19:201–215. https://doi.org/10.1111/ele.12554
Stebbins GL (1971) Chromosomal evolution in higher plants. Edward Arnold Ltd., London
Vitousek PM, Porder S, Houlton BZ, Chadwick OA (2010) Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen-phosphorus interactions. Ecol Appl 20:5–15. https://doi.org/10.1890/08-0127.1
Walczyk AM, Hersch-Green EI (2019) Impacts of soil nitrogen and phosphorus levels on cytotype performance of the circumboreal herb Chamerion angustifolium: implications for polyploid establishment. Am J Bot 106:906–921. https://doi.org/10.1002/ajb2.1321
Wei N, Du ZK, Liston A, Ashman TL (2020) Genome duplication effects on functional traits and fitness are genetic context and species dependent: studies of synthetic polyploid Fragaria. Am J Bot 107:262–272. https://doi.org/10.1002/ajb2.1377
Acknowledgements
We thank D. Althoff and S. Wang for assisting in the experimental design, and D. Althoff and A. Curé for help harvesting the plants. The authors thank D. Althoff, D. Frank, M. Ritchie, and M. Vidal for providing technical advice, and D. Althoff, S. Wang, A. Curé, P. Šmarda, M. Vidal, and an anonymous reviewer provided comments on earlier versions of the manuscript. This research was supported by a Sigma Xi Grants-In-Aid of Research to TJA, and NSF DEB 1556568 and 1655544 to KAS.
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Anneberg, T.J., Segraves, K.A. Nutrient enrichment and neopolyploidy interact to increase lifetime fitness of Arabidopsis thaliana. Plant Soil 456, 439–453 (2020). https://doi.org/10.1007/s11104-020-04727-6
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DOI: https://doi.org/10.1007/s11104-020-04727-6