The invasive plant Solidago canadensis exhibits partial local adaptation to low salinity at germination but not at later life-history stages.
Asteraceae
ecotypic variation
genetic differentiation
habitat specialization
natural selection
ontogeny
optimal reaction norm
phenotypic plasticity
plant invasion
salt stress
Journal
American journal of botany
ISSN: 1537-2197
Titre abrégé: Am J Bot
Pays: United States
ID NLM: 0370467
Informations de publication
Date de publication:
04 2020
04 2020
Historique:
received:
04
09
2019
accepted:
23
01
2020
pubmed:
1
4
2020
medline:
6
5
2020
entrez:
1
4
2020
Statut:
ppublish
Résumé
Evolutionary adaptation may enable plants to inhabit a broad range of environments. However, germination and early life-history stages have seldom been considered in estimates of evolutionary adaptation. Moreover, whether soil microbial communities can influence evolutionary adaptation in plants remains little explored. We used reciprocal transplant experiments to investigate whether two populations of an invasive plant Solidago canadensis that occur in contrasting habitats of low versus high salinity expressed adaptation to the respective salinity levels. We germinated S. canadensis seeds collected from low-and high-salinity habitats under low- and high-salt treatments. We also raised S. canadensis seedlings from the two salinity habitats under low- and high-salt treatments and in the presence versus absence of microbial communities from the two habitats. Genotypes from a low-salinity habitat had higher germination rates under low-salt treatment than genotypes from a high-salinity habitat. However, both genotypes had similar germination rates under a high-salt treatment. The two genotypes also had similar seedling survival and biomass responses to low- and high-salt treatments. Nevertheless, seedling biomass was significantly higher under low salt treatment. Soil microbial communities did not influence biomass of S. canadensis under the two salt treatments. The results on germination rates suggest partial local adaptation to low salinity. However, there was no evidence of local adaptation to salinity at the seedling survival and growth stages. The finding that germination and seedling biomass responded to different salt treatments suggests that the two traits are important for salt tolerance.
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
599-606Subventions
Organisme : Ten Thousand Talent Program of Zhejiang Province
Pays : International
Organisme : National Key Research and Development Program
ID : 2016YFC1201100
Pays : International
Organisme : National Natural Science Foundation of China
ID : 31850410484
Pays : International
Informations de copyright
© 2020 Botanical Society of America.
Références
Anderson, J. T., D. W. Inouye, A. M. McKinney, R. I. Colautti, and T. Mitchell-Olds. 2012. Phenotypic plasticity and adaptive evolution contribute to advancing flowering phenology in response to climate change. Proceedings of the Royal Society, B, Biological Sciences 279: 3843-3852.
Baltruschat, H., J. Fodor, B. D. Harrach, E. Niemczyk, B. Barna, G. Gullner, A. Janeczko, et al. 2008. Salt tolerance of barley induced by the root endophyte Piriformospora indica is associated with a strong increase in antioxidants. New Phytologist 180: 501-510.
Bao, S. D. 1999. Soil and agricultural chemistry analysis, 3rd ed. China Agricultural Press, Beijing, China.
Baskin, C. C., and J. M. Baskin. 2014. Seeds: Ecology, biogeography, and evolution of dormancy and germination, 2nd ed. Academic Press, Cambridge, Massachusetts, USA.
Bothe, H., K. Turnau, and M. Regvar. 2010. The potential role of arbuscular mycorrhizal fungi in protecting endangered plants and habitats. Mycorrhiza 20: 445-457.
Burghardt, L., C. Metcalf, A. Wilczek, J. Schmitt, and K. Donohue. 2015. Modeling the influence of genetic and environmental variation on the expression of plant life cycles across landscapes. American Naturalist 185: 212-227.
Chojak-Koźniewska, J., E. Kuźniak, and J. Zimny. 2018. The effects of combined abiotic and pathogen stress in plants: Insights from salinity and Pseudomonas syringae pv. lachrymans interaction in Cucumber. Frontiers in Plant Science 9: 1691.
Dietz, H., and P. J. Edwards. 2006. Recognition that causal processes change during plant invasion helps explain conflicts in evidence. Ecology 87: 1359-1367.
Dong, M., J. Lu, W. Zhang, J. Chen, and B. Li. 2006. Canada goldenrod (Solidago canadensis): An invasive alien weed rapidly spreading in China. Acta Phytotaxonomica Sinica 44: 72-85.
Dong, L.-J., H.-W. Yu, and W.-M. He. 2015. What determines positive, neutral, and negative impacts of Solidago canadensis invasion on native plant species richness? Scientific Reports 5: 16804.
Donohue, K. 2014. Why ontogeny matters during adaptation: Developmental niche construction and pleiotropy across the life cycle in Arabidopsis thaliana. Evolution 68: 32-47.
Donohue, K., R. R. de Casas, L. Burghardt, K. Kovach, and C. G. Willis. 2010. Germination, postgermination adaptation, and species ecological ranges. Annual Review of Ecology, Evolution, and Systematics 41: 293-319.
Evelin, H., R. Kapoor, and B. Giri. 2009. Arbuscular mycorrhizal fungi in alleviation of salt stress: A review. Annals of Botany 104: 1263-1280.
Facon, B., B. J. Genton, J. Shykoff, P. Jarne, A. Estoup, and P. David. 2006. A general eco-evolutionary framework for understanding bioinvasions. Trends in Ecology & Evolution 21: 130-135.
Fileccia, V., P. Ruisi, R. Ingraffia, D. Giambalvo, A. Frenda, and F. Martinelli. 2017. Arbuscular mycorrhizal symbiosis mitigates the negative effects of salinity on durum wheat. PLoS ONE 12: e0184158.
Geber, M. A., and V. M. Eckhart. 2005. Experimental studies of adaptation in Clarkia xantiana. II. Fitness variation across a subspecies border. Evolution 59: 521-531.
Giménez-Benavides, L., A. Escudero, and J. M. Iriondo. 2007. Local adaptation enhances seedling recruitment along an altitudinal gradient in a high mountain mediterranean plant. Annals of Botany 99: 723-734.
Godoy, O., A. Saldaña, N. Fuentes, F. Valladares, and E. Gianoli. 2010. Forests are not immune to plant invasions: Phenotypic plasticity and local adaptation allow Prunella vulgaris to colonize a temperate evergreen rainforest. Biological Invasions 13: 1615-1625.
Hanin, M., C. Ebel, M. Ngom, L. Laplaze, and K. Masmoud. 2016. New insights on plant salt tolerance mechanisms and their potential use for breeding. Frontiers in Plant Science 7: 178.
Heinen, R., Q. Ye, and F. Chaumont. 2009. Role of aquaporins in leaf physiology. Journal of Experimental Botany 60: 2971-2985.
Huang, X., J. Schmitt, L. Dorn, C. Griffith, S. Effgen, S. Takao, M. Koornneef, and K. Donohue. 2010. The earliest stages of adaptation in an experimental plant population: Strong selection on QTLS for seed dormancy. Molecular Ecology 19: 1335-1351.
Jin, H., Y. Yuan, F. Gao, A. M. O. Oduor, and J. Li. 2020. Data from: The invasive plant Solidago canadensis exhibits partial local adaptation to low salinity at germination but not at later life-history stages. Dryad Digital Repository. https://doi.org/10.5061/dryad.18931zcsh.
Kawecki, T. J., and D. Ebert. 2004. Conceptual issues in local adaptation. Ecology Letters 7: 1225-1241.
Keller, M., and J. Kollmann. 1999. Effects of seed provenance on germination of herbs for agricultural compensation sites. Agriculture, Ecosystems and Environment 72: 87-99.
Kitajima, K., and M. Fenner. 2000. Ecology of seedling regeneration. In M. Fenner [ed.], Seeds: The ecology of regeneration in plant communities, 331-359. CABI Publishing, Wallingford, UK.
Lau, J. A., and J. T. Lennon. 2011. Evolutionary ecology of plant-microbe interactions: soil microbial structure alters selection on plant traits. New Phytologist 192: 215-224.
Li, J., H. Liu, M. Yan, and L. Du. 2017. No evidence for local adaptation to salt stress in the existing populations of invasive Solidago canadensis in China. PLoS ONE 12: 1-13.
Li, J., A. M. O. Oduor, F. Yu, and M. Dong. 2019. A native parasitic plant and soil microorganisms facilitate a native plant co-occurrence with an invasive plant. Ecology and Evolution 9: 8652-8663.
Logofet, D. O., N. G. Ulanova, and I. N. Belova. 2014. Adaptation on the ground and beneath: Does the local population maximize its λ1? Ecological Complexity 20: 176-184.
Mack, R., D. Simberloff, M. W. Lonsdale, H. Evans, M. Clout, and F. A. Bazzaz. 2000. Biotic invasions: Causes, epidemiology, global consequences, and control. Ecological Applications 10: 689-710.
Moles, A., M. Gruber, and S. Bonser. 2008. A new framework for predicting invasive plant species. Journal of Ecology 96: 13-17.
Moyers, B. T., and N. C. Kane. 2010. The genetics of adaptation to novel environments: Selection on germination timing in Arabidopsis thaliana. Molecular Ecology 19: 1270-1272.
Munns, R. 2005. Genes and salt tolerance: Bringing them together. New Phytologist 167: 645-663.
Munns, R., and M. Tester. 2008. Mechanisms of salinity tolerance. Annual Review of Plant Biology 59: 651-681.
Nagy, E. S., and K. J. Rice. 1997. Local adaptation in two subspecies of an annual plant: Implications for migration and gene flow. Evolution 51: 1079-1089.
Nicotra, A. B., O. K. Atkin, S. P. Bonser, A. M. Davidson, E. J. Finnegan, U. Mathesius, P. Poot, et al. 2010. Plant phenotypic plasticity in a changing climate. Trends in Plant Science 15: 684-692.
Norusis, M. J. 2009. SPSS 17.0 Guide to Data Analysis. Prentice Hall International Inc., Upper Saddle, River, NJ, USA.
Oduor, A. M. O. 2013. Evolutionary responses of native plant species to invasive plants: A review. New Phytologist 200: 986-992.
Oduor, A. M. O., R. Leimu, and M. van Kleunen. 2016. Invasive plant species are locally adapted just as frequently and at least as strongly as native plant species. Journal of Ecology 104: 957-968.
Poorter, L. 2007. Are species adapted to their regeneration niche, adult niche, or both? American Naturalist 169: 433-442.
Postma, F. M., and J. Ågren. 2016. Early life stages contribute strongly to local adaptation in Arabidopsis thaliana. Proceedings of the National Academy of Sciences, USA 113: 7590-7595.
Postma, F. M., and J. Ågren. 2018. Among-year variation in selection during early life stages and the genetic basis of fitness in Arabidopsis thaliana. Molecular Ecology 27: 2498-2511.
Pyšek, P., V. Jarošík, P. E. Hulme, J. Pergl, M. Hejda, U. Chaffner, and M. Vilà. 2012. A global assessment of invasive plant impacts on resident species, communities and ecosystems: The interaction of impact measures, invading species’ traits and environment. Global Change Biology 18: 1725-1737.
Redman, R. S., Y. O. Kim, C. J. D. A. Woodward, C. Greer, L. Espino, S. L. Doty, and R. J. Rodriguez. 2011. Increased fitness of rice plants to abiotic stress via habitat adapted symbiosis: A strategy for mitigating impacts of climate change. PLoS ONE 6: e14823.
Rice, K. J., and E. E. Knapp. 2008. Effects of competition and life history stage on the expression of local adaptation in two native bunchgrasses. Restoration Ecology 16: 12-23.
Richards, C. L., O. Bossdorf, N. Z. Muth, J. Gurevitch, and M. Pigliucci. 2006. Jack of all trades, master of some? On the role of phenotypic plasticity in plant invasions. Ecology Letters 9: 981-993.
Richards, C. L., R. L. Walls, J. P. Bailey, R. Parameswaran, T. George, and M. Pigliucci. 2008. Plasticity in salt tolerance traits allows for invasion of novel habitat by Japanese knotweed s. l. (Fallopia japonica and F. × bohemica, Polygonaceae). American Journal of Botany 95: 931-942.
Richards, C. L., S. N. White, M. A. McGuire, S. J. Franks, L. A. Donovan, and R. Mauricio. 2010. Plasticity, not adaptation to salt level, explains variation along a salinity gradient in a salt marsh perennial. Estuaries and Coasts 33: 840-852.
Roach, D. A., and R. Wulff. 1987. Maternal effects in plants. Annual Review of Ecology and Systematics 18: 209-235.
Rodriguez, R. J., J. Henson, E. van Volkenburgh, M. Hoy, L. Wright, F. Beckwith, Y. O. Kim, and R. S. Redman. 2008. Stress tolerance in plants via habitat-adapted symbiosis. ISME Journal 2: 404-416.
Ruíz-Lozano, J., R. Porcel, C. Azcón, and R. Aroca. 2012. Regulation by arbuscular mycorrhizae of the integrated physiological response to salinity in plants: New challenges in physiological and molecular studies. Journal of Experimental Botany 63: 4033-4044.
Sax, D., J. Stachowicz, J. Brown, J. Bruno, M. Dawson, S. Gaines, R. Grosberg, et al. 2007. Ecological and evolutionary insights from species invasions. Trends in Ecology and Evolution 22: 465-471.
Shearin, Z. R. C., M. Filipek, R. Desai, W. A. Bickford, K. P. Kowalski, and K. Clay. 2018. Fungal endophytes from seeds of invasive, non-native Phragmites australis and their potential role in germination and seedling growth. Plant and Soil 422: 183-194.
Si, C., Z. Dai, Y. Lin, S. Qi, P. Huang, S. Miao, and D. Du. 2014. Local adaptation and phenotypic plasticity both occurred in Wedelia trilobata invasion across a tropical island. Biological Invasions 16: 2323-2337.
Siepielski, A., J. DiBattista, and S. Carlson. 2009. It's about time: The temporal dynamics of phenotypic selection in the wild. Ecology Letters 12: 1261-1276.
Soares, M. A., H. Y. Li, K. P. Kowalski, M. Bergen, M. S. Torres, and J. F. White. 2016. Evaluation of the functional roles of fungal endophytes of Phragmites australis from high saline and low saline habitats. Biological Invasions 18: 1-14.
Talaat, N., and B. Shawky. 2013. 24-Epibrassinolide alleviates salt-induced inhibition of productivity by increasing nutrients and compatible solutes accumulation and enhancing antioxidant system in wheat (Triticum aestivum L.). Acta Physiologiae Plantarum 35: 729-740.
Vasquez, E., E. Glenn, G. Guntenspergen, J. Brown, and S. Nelson. 2006. Salt tolerance and osmotic adjustment of Spartina alterniflora (Poaceae) and the invasive M haplotype of Phragmites australis (Poaceae) along a salinity gradient. American Journal of Botany 93: 1784-1790.
Volis, S., S. Mendlinger, and D. Ward. 2002. Adaptive traits of wild barley plants of Mediterranean and desert origin. Oecologia 133: 131-138.
White, J. F., K. I. Kingsley, K. P. Kowalski, I. Irizarry, A. Micci, M. A. Soares, and M. S. Bergen. 2018. Disease protection and allelopathic interactions of seed-transmitted endophytic pseudomonads of invasive reed grass (Phragmites australis). Plant and Soil 422: 195-208.
Xu, X., Y. Wang, Q. Lu, Z. Lin, and H. Chen. 2011. Effect of Solidago canadensis invasions on soil nematode communities in Hangzhou Bay. Biodiversity Science 19: 519-527.
Xu, H., S. Qiang, P. Genovesi, H. Ding, J. Wu, L. Meng, Z. Han, et al. 2012. An inventory of invasive alien species in China. NeoBiota 15: 1-26.
Yadav, S., M. Irfan, A. Ahmad, and S. Hayat. 2011. Causes of salinity and plant manifestations to salt stress: A review. Journal of Environmental Biology 32: 667-685.
Yang, Q., B. Li, and E. Siemann. 2015. The effects of fertilization on plant-soil interactions and salinity tolerance of invasive Triadica sebifera. Plant and Soil 394: 99-107.
Yao, B. Q., C. M. Zhao, J. M. Deng, H. K. Zhou, X. Q. Zhao, and J. Q. Liu. 2013. Phenotypic plasticity of Thellungiella salsaginea in response to saline stress. Evolutionary Ecology Research 15: 829-846.
Yuan, Y., B. Wang, S. Zhang, J. Tang, C. Tu, S. Hu, J. W. H. Yong, and X. Chen. 2013. Enhanced allelopathy and competitive ability of invasive plant Solidago canadensis in its introduced range. Journal of Plant Ecology 6: 253-263.
Zenni, R. D., J. B. Lamy, L. Lamarque, and A. Porté. 2014. Adaptive evolution and phenotypic plasticity during naturalization and spread of invasive species: Implications for tree invasion biology. Biological Invasions 16: 635-644.
Zhao, S. Y., S. G. Sun, C. Dai, R. W. Gituru, J. M. Chen, and Q. F. Wang. 2015. Genetic variation and structure in native and invasive Solidago canadensis populations. Weed Research 55: 163-172.
Zhu, L. 2011. Distribution and ecological adaptation characteristics of Solidago canadensis to Jiuduansha, Shanghai. M.S. thesis. Shanghai Normal University, Shanghai, China.