Growth, physiology, and stomatal parameters of plant polyploids grown under ice age, present-day, and future CO2 concentrations

. 2023 Jul ; 239 (1) : 399-414. [epub] 20230511

Jazyk angličtina Země Anglie, Velká Británie Médium print-electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid37167007

Polyploidy plays an important role in plant evolution, but knowledge of its eco-physiological consequences, such as of the putatively enlarged stomata of polyploid plants, remains limited. Enlarged stomata should disadvantage polyploids at low CO2 concentrations (namely during the Quaternary glacial periods) because larger stomata are viewed as less effective at CO2 uptake. We observed the growth, physiology, and epidermal cell features of 15 diploids and their polyploid relatives cultivated under glacial, present-day, and potential future atmospheric CO2 concentrations (200, 400, and 800 ppm respectively). We demonstrated some well-known polyploidy effects, such as faster growth and larger leaves, seeds, stomata, and other epidermal cells. The stomata of polyploids, however, tended to be more elongated than those of diploids, and contrary to common belief, they had no negative effect on the CO2 uptake capacity of polyploids. Moreover, polyploids grew comparatively better than diploids even at low, glacial CO2 concentrations. Higher polyploids with large genomes also showed increased operational stomatal conductance and consequently, a lower water-use efficiency. Our results point to a possible decrease in growth superiority of polyploids over diploids in a current and future high CO2 climatic scenarios, as well as the possible water and/or nutrient dependency of higher polyploids.

Zobrazit více v PubMed

Ainsworth EA, Rogers A. 2007. The response of photosynthesis and stomatal conductance to rising [CO2]: mechanisms and environmental interactions. Plant, Cell & Environment 30: 258-270.

Annenberg TJ, Segraves KA. 2020. Nutrient enrichment and neopolyploidy interact to increase lifetime fitness of Arabidopsis thaliana. Plant and Soil 456: 439-453.

Baresch A, Crifò C, Boyce CK. 2019. Competition for epidermal space in the evolution of leaves with high physiological rates. New Phytologist 221: 628-639.

Beaulieu JM, Leitch IJ, Patel S, Pendharkar A, Knight CA. 2008. Genome size is a strong predictor of cell size and stomatal density in angiosperms. New Phytologist 174: 975-986.

te Beest M, Le Roux JJ, Richardson DM, Brysting AK, Suda J, Kubešová M, Pyšek P. 2012. The more the better? The role of polyploidy in facilitating plant invasions. Annals of Botany 109: 19-45.

Begon M, Townsend CR, Harper JL. 2006. Ecology. From individuals to ecosystems, 4th edn. Oxford, UK: Blackwell.

Bennett MD. 1987. Variation in genomic form in plants and its ecological implications. New Phytologist 106(Suppl): 177-200.

Bomblies K. 2020. When everything changes at once: finding a new normal after genome duplication. Proceedings of the Royal Society B: Biological Sciences 287: 20202154.

Castro M, Castro S, Loureiro J. 2018. Production of synthetic tetraploids as a tool for polyploid research. Web Ecology 18: 129-141.

Cavalier-Smith T. 2005. Economy, speed and size matter: evolutionary forces driving nuclear genome miniaturization and expansion. Annals of Botany 95: 147-175.

Chapin FS III, Matson PA, Vitousek PM. 2012. Principles of terrestrial ecosystem ecology, 2nd edn. New York, NY, USA: Springer.

Comai L. 2005. The advantages and disadvantages of being polyploid. Nature Reviews Genetics 6: 836-846.

DeMalach N, Kadmon R. 2018. Seed mass diversity along resource gradients: the role of allometric growth rate and size-asymmetric competition. Ecology 99: 2196-2206.

Doyle JJ, Coate JE. 2019. Polyploidy, the nucleotype, and novelty: the impact of genome doubling on the biology of the cell. International Journal of Plant Sciences 180: 1-52.

Drake PL, de Boer HJ, Schymanski SS, Veneklaas EJ. 2019. Two sides to every leaf: water and CO2 transport in hypostomatous and amphistomatous leaves. New Phytologist 222: 1179-1187.

Faizullah L, Morton JA, Hersch-Green EI, Walczyk AM, Leitch AR, Leitch IJ. 2021. Exploring environmental selection on genome size in angiosperms. Trends in Plant Science 26: 1039-1049.

Farquhar GD, Sharkey TD. 1982. Stomatal conductance and photosynthesis. Annual Review of Plant Physiology 11: 191-210.

Fowler NL, Levin DA. 1984. Ecological constraint on the establishment of a novel polyploid in competition with its diploid progenitor. American Naturalist 124: 703-711.

Fox DT, Soltis DE, Soltis PS, Ashman TL, Van de Peer Y. 2020. Polyploidy: a biological force from cells to ecosystems. Trends in Cell Biology 30: 688-694.

Francis D, Davies MS, Barlow PW. 2008. A strong nucleotypic effect on the cell cycle regardless of ploidy level. Annals of Botany 101: 747-757.

Franks PJ, Beerling DJ. 2009. Maximum leaf conductance driven by CO2 effects on stomatal size and density over geologic time. Proceedings of the National Academy of Sciences, USA 106: 10343-10347.

Gerhart LM, Ward JK. 2010. Plant responses to low [CO2] of the past. New Phytologist 188: 674-695.

Gonzalez N, Vanhaeren H, Inzé D. 2012. Leaf size control: complex coordination of cell division and expansion. Trends in Plant Science 17: 332-340.

Gottschalk W. 1976. Die Bedeutung der Polyploidie für die Evolution der Pflanzen. Stuttgart, Germany: Gustaf Fischer.

Grant V. 1981. Plant speciation, 2nd edn. New York, NY, USA: Columbia University Press.

Guignard MS, Nichols RA, Knell RJ, Macdonald A, Trimmer M, Romila CA, Leitch IJ, Leitch AR. 2016. Genome size and ploidy influence angiosperm species' biomass under nitrogen and phosphorus limitation. New Phytologist 210: 1195-1206.

Hegarty M, Coate J, Sherman-Broyles S, Abbott R, Hiscock S, Doyle J. 2013. Lessons from natural and artificial polyploids in higher plants. Cytogenetic and Genome Research 140: 204-225.

Hessen DO, Jeyasingh PD, Neiman M, Weider LJ. 2009. Genome streamlining and the elemental costs of growth. Trends in Ecology and Evolution 25: 75-80.

Hetherington AM, Woodward FI. 2003. The role of stomata in sensing and driving environmental change. Nature 424: 901-908.

Hodgson JG, Sharafi M, Jalili A, Díaz S, Montserrat-Martí G, Palmer C, Cerabolini B, Pierce S, Hamzehee B, Asri Y et al. 2010. Stomatal vs. genome size in angiosperms: the somatic tail wagging the genomic dog? Annals of Botany 105: 573-584.

Intergovernmental Panel on Climate Change. 2014. Summary for policymakers. In: Stocker TF, Qin D, Plattner G-K, Tignor MMB, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM, eds. Climate change 2013: the physical science basis. Contribution of working group I to the fifth assessment report of the Intergovernmental Panel on Climate Change. Cambridge, UK: Cambridge University Press, 3-29.

Jiao Y, Wickett NJ, Ayyampalayam S, Chanderbali AS, Landherr L, Ralph PE, Tomsho LP, Hu Y, Liang H, Soltis PS et al. 2011. Ancestral polyploidy in seed plants and angiosperms. Nature 473: 97-100.

Kirschbaum MUF. 2011. Does enhanced photosynthesis enhance growth? Lessons learned from CO2 enrichment studies. Plant Physiology 155: 117-124.

Körner C. 2006. Plant CO2 responses: an issue of definition, time and resource supply. New Phytologist 172: 393-411.

Körner C. 2015. Paradigm shift in plant growth control. Current Opinion in Plant Biology 25: 107-114.

Lake JA, Woodward FI. 2008. Response of stomatal numbers to CO2 and humidity: control by transpiration rate and abscisic acid. New Phytologist 179: 397-404.

Lambers H, Oliveira RS. 2019. Plant physiological ecology, 3rd edn. Cham, Switzerland: Springer Nature.

Leitch AR, Leitch IJ. 2008. Genomic plasticity and the diversity of polyploid plants. Science 320: 481-483.

Leitch IJ, Johnston E, Pellicer J, Hidalgo O, Bennett MD. 2019. Plant DNA C-values database (release 7.1, April 2019). [WWW document] URL https://cvalues.science.kew.org/ [accessed 22 September 2021].

Levin DA. 1975. Minority cytotype exclusion in local plant populations. Taxon 24: 35-43.

Levin DA. 1983. Polyploidy and novelty in flowering plants. American Naturalist 122: 1-25.

Levin DA. 2002. The role of chromosomal change in plant evolution. New York, NY, USA: Oxford University Press.

Lomax BH, Hilton J, Bateman RM, Upchurch GR, Lake JA, Leitch IJ, Cromwell A, Knight CA. 2014. Reconstructing relative genome size of vascular plants through geological time. New Phytologist 201: 636-644.

Long SP, Ainsworth EA, Rogers A, Ort DR. 2004. Rising atmospheric carbon dioxide: plants FACE the future. Annual Review of Plant Biology 55: 591-628.

Lüthi D, Le Floch M, Bereiter B, Blunier T, Barnola JM, Siegenthaler U, Raynaud D, Jouzel J, Fischer H, Kawamura K et al. 2008. High-resolution carbon dioxide concentration record 650,000-800,000 years before present. Nature 453: 379-382.

Mason AS, ed. 2017. Polyploidy and hybridization for crop improvement. Boca Raton, FL, USA: CRC Press.

Masterson J. 1994. Stomatal size in fossil plants: evidence for polyploidy in majority of angiosperms. Science 264: 421-424.

Mayrose I, Zhan ZH, Rothfels CJ, Magnuson-Ford K, Barker MS, Rieseberg LH, Otto SP. 2011. Recently formed polyploid plants diversify at lower rates. Science 333: 1257.

McElwain JC, Steinthorsdottir M. 2017. Paleoecology, ploidy, paleoatmospheric composition, and developmental biology: a review of the multiple uses of fossil stomata. Plant Physiology 174: 650-664.

Muir CD. 2018. Light and growth form interact to shape stomatal ratio among British angiosperms. New Phytologist 218: 242-252.

Müntzing A. 1936. The evolutionary significance of autopolyploidy. Hereditas 21: 363-378.

Novikova PY, Hohmann N, Van de Peer Y. 2018. Polyploid Arabidopsis species originated around recent glaciation maxima. Current Opinion in Plant Biology 42: 8-15.

Pacey EK, Maherali H, Husband BC. 2022. Polyploidy increases storage whilst decreasing structural stability in Arabidopssis thaliana. Current Biology 32: 4057-4063.

Poorter H, Fiorani F, Pieruschka R, Wojciechowski T, van der Putten WH, Kleyer M, Schurr U, Postma J. 2016. Pampered inside, pestered outside? Differences and similarities between plants growing in controlled conditions and in the field. New Phytologist 212: 838-855.

Poorter H, Knopf O, Wright IJ, Temme AA, Hogewoning SW, Graf A, Cernusak LA, Pons TL. 2022. A meta-analysis of response of C3 plants to atmospheric CO2: dose-response curves for 85 traits ranging from the molecular to the whole-plant level. New Phytologist 233: 1560-1596.

Poorter H, Navas ML. 2003. Plant growth and competition at elevated CO2: on winners, losers and functional groups. New Phytologist 157: 175-198.

Poorter H, Niinemets Ü, Ntagkas N, Siebenkäs A, Mäenpää M, Matsubara S, Pons T. 2019. A meta-analysis of plant responses to light intensity for 70 traits ranging from molecules to whole plant performance. New Phytologist 223: 1073-1105.

Poorter H, Remkes C, Lambers H. 1990. Carbon and nitrogen economy of 24 wild species differing in relative growth rate. Plant Physiology 94: 621-627.

Pritchard SG, Rogers HH, Prior SA, Peterson CM. 1999. Elevated CO2 and plant structure: a review. Global Change Biology 5: 807-837.

R Core Team. 2019. R: a language and environment for statistical computing. [WWW document] URL https://www.R-project.org/ [accessed 7 December 2020].

Ramsey J, Ramsey TS. 2014. Ecological studies of polyploidy in the 100 years following its discovery. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences 369: 20130352.

Ramsey J, Schemske DW. 1998. Pathways, mechanisms, and rates of polyploid formation in flowering plants. Annual Review of Ecology and Systematics 29: 467-501.

Ramsey J, Schemske DW. 2002. Neopolyploidy in flowering plants. Annual Review of Ecology and Systematics 33: 589-639.

Reddy AR, Rasineni GK, Raghavendra AS. 2010. The impact of global elevated CO2 concentration on photosynthesis and plant productivity. Current Science 99: 46-57.

Ren R, Wang H, Guo C, Zhang N, Zeng L, Chen Y, Ma H, Qi J. 2018. Widespread whole genome duplications contribute to genome complexity and species diversity in angiosperms. Molecular Plant 11: 414-428.

Rice A, Šmarda P, Novoslov M, Drori M, Glick L, Sabath N, Meiri S, Belmaker J, Mayrose I. 2019. The global biogeography of polyploid plants. Nature Ecology and Evolution 3: 265-273.

Rieseberg LH, Willis JH. 2007. Plant speciation. Nature 317: 910-914.

Roddy AB, Théroux-Rancourt G, Abbo T, Benedetti JW, Brodersen CR, Castro M, Castro S, Gilbride AB, Jensen B, Jiang GF et al. 2020. The scaling of genome size and cell size limits maximum rates of photosynthesis with implications for ecological strategies. International Journal of Plant Sciences 181: 75-87.

Royer DL. 2001. Stomatal density and stomatal index as indicators of paleoatmospheric CO2 concentration. Review of Palaeobotany and Palynology 114: 1-28.

Ruiz M, Oustric J, Santini J, Morillon R. 2020. Synthetic polyploidy in grafted crops. Frontiers in Plant Science 11: 540894.

Sage RF, Coleman JR. 2001. Effects of low atmospheric CO2 on plants: more than a thing of the past. Trends in Plant Science 6: 18-24.

Salman-Minkov A, Sabath N, Mayrose I. 2016. Whole-genome duplication as a key factor in crop domestication. Nature Plants 2: 16115.

Sattler MC, Carvalho CR, Clarindo WR. 2016. The polyploidy and its key role in plant breeding. Planta 243: 281-296.

Šmarda P, Hejcman M, Březinová A, Horová L, Steigerová H, Zedek F, Bureš P, Hejcmanová 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 Phytologist 200: 911-921.

Šmarda P, Horová L, Knápek O, Dieck H, Dieck M, Ražná K, Hrubík P, Orlóci L, Papp L, Veselá K et al. 2018. Multiple haploids, triploids, and tetraploids found in modern-day “living fossil” Ginkgo biloba. Horticulture Research 5: 55.

Šmarda P, Knápek O, Březinová A, Horová L, Grulich V, Danihelka J, Veselý P, Šmerda J, Rotreklová O, Bureš P. 2019. Genome sizes and genomic guanine+cytosine (GC) contents of the Czech vascular flora with new estimates for 1700 species. Preslia 91: 117-142.

Soltis D, Buggs RJA, Doyle JJ, Soltis PS. 2010. What we still don't know about polyploidy. Taxon 59: 1387-1403.

Soltis DE, Albert VA, Leebens-Mack J, Bell CD, Paterson AH, Zheng C, Sankoff D, Depamphilis CW, Wall PK, Soltis PS. 2009. Polyploidy and angiosperm diversification. American Journal of Botany 96: 336-348.

Soltis DE, Visger CJ, Soltis PS. 2014. The polyploidy revolution then…and now: Stebbins revisited. American Journal of Botany 101: 1057-1078.

Stebbins GL. 1950. Variation and evolution in plants. New York, NY, USA: Oxford University Press.

Stebbins GL. 1971. Chromosomal evolution in higher plants. London, UK: Edward Arnold.

Tal M. 1980. Physiology of polyploids. In: Lewis WH, ed. Polyploidy - biological relevance. New York, NY, USA: Plenum Press, 61-75.

Théroux-Rancourt G, Roddy AB, Earles JM, Gilbert ME, Zwieniecki MA, Boyce CK, Tholen D, McElrone AJ, Simonin KA, Brodersen CR. 2021. Maximum CO2 diffusion inside leaves is limited by the scaling of cell size and genome size. Proceedings of the Royal Society B: Biological Sciences 288: 20203145.

Valladares F, Niinemets Ü. 2008. Shade tolerance, a key plant feature of complex nature and consequences. Annual Review of Ecology, Evolution, and Systematics 39: 237-257.

Van de Peer Y, Mizrachi E, Marchal K. 2017. The evolutionary significance of polyploidy. Nature Reviews Genetics 18: 411-424.

Vanneste K, Baele G, Maere S, Van de Peer Y. 2014. Analysis of 41 plant genomes supports a wave of successful genome duplications in association with the Cretaceous-Paleogene boundary. Genome Research 24: 1334-1347.

Veselý P, Bureš P, Šmarda P, Pavlíček T. 2012. Genome size and DNA base composition of geophytes: the mirror of phenology and ecology? Annals of Botany 109: 65-75.

Wang X, Morton JA, Pellicer J, Leitch IJ, Leitch AR. 2021. Genome downsizing after polyploidy: mechanisms, rates and selection pressures. The Plant Journal 2021: 1003-1015.

Willmer C, Fricker M. 1996. Stomata, 2nd edn. London, UK: Chapman & Hall.

Woodward FI. 1987. Stomatal numbers are sensitive to increases in CO2 from pre-industrial levels. Nature 327: 617-618.

Zwieniecki MA, Haaning KS, Boyce CK, Jensen KH. 2016. Stomatal design principles in synthetic and real leaves. Journal of the Royal Society Interface 13: 20160535.

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...