Abstract
Sulfur deposition and eutrophication accelerated the production of hydrogen sulfide (H2S) in aquatic ecosystems. However, the understanding of how H2S affects the invasive potential of exotic aquatic plants is inadequate. Here, the exotic Elodea nuttallii (Planch.) H. St. John was exposed to five H2S concentrations (0–1.0 mM) and compared with the native Hydrilla verticillata (L. f.) Royle. Both plants grew well below 0.5 mM H2S, with E. nuttallii showing better performance. E. nuttallii and H. verticillata maintained their height growth rates by reducing the ramets number and the relative growth rate, respectively. This trade-off in morphological traits was for adequate light and oxygen. Furthermore, E. nuttallii exhibited higher chlorophyll and carotenoids content but lower chlorophyll a/b, indicating better utilization of low light in the water body. High concentrations of H2S induced oxidative stress in E. nuttallii, leading to higher superoxide dismutase (SOD), soluble sugars, and starch. The utilization strategies of C, N, P and S by E. nuttallii remained unchanged with varying H2S concentrations, demonstrating higher stoichiometric stability. In conclusion, E. nuttallii showed greater resistance to H2S compared to H. verticillata. The invasive potential of E. nuttallii in H2S-enriched aquatic environments was depending on the H2S concentration of native community.
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Data availability
The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Ahmad, R., S. Ali, M. Rizwan, M. Dawood, M. Farid, A. Hussain, L. Wijaya, M. N. Alyemeni & P. Ahmad, 2020. Hydrogen sulfide alleviates chromium stress on cauliflower by restricting its uptake and enhancing antioxidative system. Physiologia Plantarum 168(2): 289–300. https://doi.org/10.1111/ppl.13001.
Al Ubeed, H. M. S., R. B. H. Wills, M. C. Bowyer, Q. V. Vuong & J. B. Golding, 2017. Interaction of exogenous hydrogen sulphide and ethylene on senescence of green leafy vegetables. Postharvest Biology and Technology 133: 81–87. https://doi.org/10.1016/j.postharvbio.2017.07.010.
Angelstein, S. & H. Schubert, 2008. Elodea nuttallii: uptake, translocation and release of phosphorus. Aquatic Biology 3(3): 209–216. https://doi.org/10.3354/ab00080.
Apostolaki, E. T., M. Holmer, V. Santinelli & I. Karakassis, 2018. Species-specific response to sulfide intrusion in native and exotic Mediterranean seagrasses under stress. Marine Environmental Research 134: 85–95. https://doi.org/10.1016/j.marenvres.2017.12.006.
Arif, Y., S. Hayat, M. Yusuf & A. Bajguz, 2021. Hydrogen sulfide: A versatile gaseous molecule in plants. Plant Physiology and Biochemistry 158: 372–384. https://doi.org/10.1016/j.plaphy.2020.11.045.
Azzoni, R., C. Giordani, M. Bartoli, D. T. Welsh & P. Viaroli, 2001. Iron, sulphur and phosphorus cycling in the rhizosphere sediments of a eutrophic Ruppia cirrhosa meadow (Valle Smarlacca, Italy). Journal of Sea Research 45(1): 15–26. https://doi.org/10.1016/s1385-1101(00)00056-3.
Ba, Y., J. Zhai, J. Yan, K. Li & H. Xu, 2021. H2S improves growth of tomato seedlings involving the MAPK signaling. Scientia Horticulturae 288. https://doi.org/10.1016/j.scienta.2021.110366.
Bao, S., 2000. Agrochemical Analysis of Soil, China Agriculture Press, Bei**g:
Barrat-Segretain, M. H. & A. Elger, 2004. Experiments on growth interactions between two invasive macrophyte species. Journal of Vegetation Science 15(1): 109–114. https://doi.org/10.1111/j.1654-1103.2004.tb02243.x.
Bennett, S., J. Santana-Garcon, N. Marbà, G. Jorda, A. Anton, E. T. Apostolaki, J. Cebrian, N. R. Geraldi, D. Krause-Jensen, C. E. Lovelock, P. Martinetto, J. M. Pandolfi & C. M. Duarte, 2021. Climate-driven impacts of exotic species on marine ecosystems. Global Ecology and Biogeography 30(5): 1043–1055. https://doi.org/10.1111/geb.13283.
Boriboonkaset, T., C. Theerawitaya, N. Yamada, A. Pichakum, K. Supaibulwatana, S. Cha-um, T. Takabe & C. Kirdmanee, 2013. Regulation of some carbohydrate metabolism-related genes, starch and soluble sugar contents, photosynthetic activities and yield attributes of two contrasting rice genotypes subjected to salt stress. Protoplasma 250(5): 1157–1167. https://doi.org/10.1007/s00709-013-0496-9.
Brodersen, K. E., D. A. Nielsen, P. J. Ralph & M. Kühl, 2014. Oxic microshield and local pH enhancement protects Zostera muelleri from sediment derived hydrogen sulphide. New Phytologist 205(3): 1264–1276. https://doi.org/10.1111/nph.13124.
Brodersen, K. E., M. Lichtenberg, L.-C. Paz & M. Kuhl, 2015. Epiphyte-cover on seagrass (Zostera marina L.) leaves impedes plant performance and radial O2 loss from the below-ground tissue. Frontiers in Marine Science 2. https://doi.org/10.3389/fmars.2015.00058.
Brodersen, K. E., K. Koren, M. Lichtenberg & M. Kuhl, 2016. Nanoparticle-based measurements of pH and O2 dynamics in the rhizosphere of Zostera marina L.: effects of temperature elevation and light-dark transitions. Plant Cell and Environment 39(7): 1619–1630. https://doi.org/10.1111/pce.12740.
Bu, H.-Y., P. Jia, W. Qi, K. Liu, D.-H. Xu, W.-J. Ge & X.-J. Wang, 2018. The effects of phylogeny, life-history traits and altitude on the carbon, nitrogen, and phosphorus contents of seeds across 203 species from an alpine meadow. Plant Ecology 219(6): 737–748. https://doi.org/10.1007/s11258-018-0830-6.
Chen, J., W.-Y. Liu, W.-Q. Zhang, Y.-M. Zhang, Y.-W. Zhao & G.-H. Wei, 2022. Effects of sodium hydrosulfide and rhizobia on the growth rate, nutrient stoichiometry, and nutrient resorption of soybean (Glycine max L.). Journal of Plant Nutrition and Soil Science 185(1): 69–86. https://doi.org/10.1002/jpln.202100121.
Cook, C. D. K. & K. Urmi-König, 1985. A revision of the genus Elodea (Hydrocharitaceae). Aquatic Botany 21(2): 111–156. https://doi.org/10.1016/0304-3770(85)90084-1.
Da Silva, J. M. & M. C. Arrabaça, 2004. Contributions of soluble carbohydrates to the osmotic adjustment in the C4 grass Setaria sphacelata: a comparison between rapidly and slowly imposed water stress. Journal of Plant Physiology 161(5): 551–555. https://doi.org/10.1078/0176-1617-01109.
De Battisti, D., M. S. Fowler, S. R. Jenkins, M. W. Skov, T. J. Bouma, P. J. Neyland & J. N. Griffin, 2020. Multiple trait dimensions mediate stress gradient effects on plant biomass allocation, with implications for coastal ecosystem services. Journal of Ecology 108(4): 1227–1240. https://doi.org/10.1111/1365-2745.13393.
Demidchik, V., 2015. Mechanisms of oxidative stress in plants: from classical chemistry to cell biology. Environmental and Experimental Botany 109: 212–228. https://doi.org/10.1016/j.envexpbot.2014.06.021.
Ding, S., X. Yu, J. Zhang, Z. Yin, Y. Zou, G. Wang, L. Sheng & C. He, 2021. Bioconcentration and translocation of elements regulate plant responses to water-salt conditions in saline-alkaline wetlands. Environmental and Experimental Botany 183. https://doi.org/10.1016/j.envexpbot.2020.104360.
Dong, S. & D. M. Beckles, 2019. Dynamic changes in the starch-sugar interconversion within plant source and sink tissues promote a better abiotic stress response. Journal of Plant Physiology 234: 80–93. https://doi.org/10.1016/j.jplph.2019.01.007.
Dooley, F. D., S. Wyllie-Echeverria, E. Gupta & P. D. Ward, 2015. Tolerance of Phyllospadix scouleri seedlings to hydrogen sulfide. Aquatic Botany 123: 72–75. https://doi.org/10.1016/j.aquabot.2015.02.004.
Duan, B., Y. Ma, M. Jiang, F. Yang, L. Ni & W. Lu, 2015. Improvement of photosynthesis in rice (Oryza sativa L.) as a result of an increase in stomatal aperture and density by exogenous hydrogen sulfide treatment. Plant Growth Regulation 75(1): 33–44. https://doi.org/10.1007/s10725-014-9929-5.
ECFC, 1992. Flora Reipublicae Popularis Sinicae (in Chinese), Vol. 8. Science Press, Bei**g:
Eghbal, M. A., P. S. Pennefather & P. J. O’Brien, 2004. H2S cytotoxicity mechanism involves reactive oxygen species formation and mitochondrial depolarisation. Toxicology 203(1–3): 69–76. https://doi.org/10.1016/j.tox.2004.05.020.
Flores-Rojas, N. C., M. Esterhuizen-Londt & S. Pflugmacher, 2015. Antioxidative stress responses in the floating macrophyte Lemna minor L. with cylindrospermopsin exposure. Aquatic Toxicology 169: 188–195. https://doi.org/10.1016/j.aquatox.2015.11.002.
Gallego-Tevar, B., B. J. Grewell, C. J. Futrell, R. E. Drenovsky & J. M. Castillo, 2020. Interactive effects of salinity and inundation on native Spartina foliosa, invasive S. densiflora and their hybrid from San Francisco Estuary, California. Annals of Botany 125(2): 377–389. https://doi.org/10.1093/aob/mcz170.
Han, Y.-Q., L.-G. Wang, W.-H. You, H.-H. Yu, K.-Y. **ao & Z.-H. Wu, 2018. Flooding interacting with clonal fragmentation affects the survival and growth of a key floodplain submerged macrophyte. Hydrobiologia 806(1): 67–75. https://doi.org/10.1007/s10750-017-3356-3.
Han, H., H. Wu, Y. Zhi, J. Zhou, W. Li, L. Yuan & Y. Cao, 2023. Impacts of bisphenol A on growth and reproductive traits of submerged macrophyte Vallisneria natans. Environmental Science and Pollution Research 30(16): 46383–46393. https://doi.org/10.1007/s11356-023-25521-8.
Hancock, J. T., 2019. Hydrogen sulfide and environmental stresses. Environmental and Experimental Botany 161: 50–56. https://doi.org/10.1016/j.envexpbot.2018.08.034.
Hasanuzzaman, M., M. H. M. B. Bhuyan, J. A. Mahmud, K. Nahar, S. M. Mohsin, K. Parvin & M. Fujita, 2018. Interaction of sulfur with phytohormones and signaling molecules in conferring abiotic stress tolerance to plants. Plant Signaling & Behavior 13(5). https://doi.org/10.1080/15592324.2018.1477905.
Herbert, E. R., P. Boon, A. J. Burgin, S. C. Neubauer, R. B. Franklin, M. Ardón, K. N. Hopfensperger, L. P. M. Lamers & P. Gell, 2015. A global perspective on wetland salinization: ecological consequences of a growing threat to freshwater wetlands. Ecosphere 6(10). https://doi.org/10.1890/es14-00534.1.
Hinckley, E. L. S., J. T. Crawford, H. Fakhraei & C. T. Driscoll, 2020. A shift in sulfur-cycle manipulation from atmospheric emissions to agricultural additions. Nature Geoscience 13(9): 597–604. https://doi.org/10.1038/s41561-020-0620-3.
Holmer, M., N. Marba, M. Lamote & C. M. Duarte, 2009. Deterioration of sediment quality in seagrass meadows (Posidonia oceanica) invaded by macroalgae (Caulerpa sp.). Estuaries and Coasts 32(3): 456–466. https://doi.org/10.1007/s12237-009-9133-4.
Hossain, M. A., S. Bhattacharjee, S.-M. Armin, P. Qian, W. **n, H.-Y. Li, D. J. Burritt, M. Fujita & L.-S. P. Tran, 2015. Hydrogen peroxide priming modulates abiotic oxidative stress tolerance: insights from ROS detoxification and scavenging. Frontiers in Plant Science 6. https://doi.org/10.3389/fpls.2015.00420.
Karkonen, A. & K. Kuchitsu, 2015. Reactive oxygen species in cell wall metabolism and development in plants. Phytochemistry 112: 22–32. https://doi.org/10.1016/j.phytochem.2014.09.016.
LaFond-Hudson, S., N. W. Johnson, J. Pastor & B. Dewey, 2022. Sulfur geochemistry destabilizes population oscillations of wild rice (Zizania palustris). Journal of Geophysical Research-Biogeosciences 127(8). https://doi.org/10.1029/2022jg006809.
Lamers, L. P. M., L. L. Govers, I. Janssen, J. J. M. Geurts, M. E. W. Van der Welle, M. M. Van Katwijk, T. Van der Heide, J. G. M. Roelofs & A. J. P. Smolders, 2013. Sulfide as a soil phytotoxin-a review. Frontiers in Plant Science 4. https://doi.org/10.3389/fpls.2013.00268.
Li, H., 2000. Principles and Techniques of Plant Physiological Biochemical Experiment (in Chinese), Higher Education Press, Bei**g:
Lichtenthaler, H. K., 1987. Chlorophylls and Carotenoids: Pigments of Photosynthetic Biomembranes Methods in Enzymology, Vol. 148. Academic Press:, 350–382.
Lisjak, M., T. Teklic, I. D. Wilson, M. Whiteman & J. T. Hancock, 2013. Hydrogen sulfide: environmental factor or signalling molecule? Plant Cell and Environment 36(9): 1607–1616. https://doi.org/10.1111/pce.12073.
Liu, G.-H., J.-W. Xu, L.-J. Zhang, W. Li & W.-Z. Liu, 2007. Inter-specific competition between two submerged macrophytes, Elodea nuttallii and Hydrilla verticillata. J Chinese Journal of Plant Ecology 31(1): 83–92. https://doi.org/10.17521/cjpe.2007.0011.
Liu, X., Y. Zhang, W. Han, A. Tang, J. Shen, Z. Cui, P. Vitousek, J. W. Erisman, K. Goulding, P. Christie, A. Fangmeier & F. Zhang, 2013. Enhanced nitrogen deposition over China. Nature 494(7438): 459–462. https://doi.org/10.1038/nature11917.
Liu, B., X. Zhang, X. You, Y. Li, S. Long, S. Wen, Q. Liu, T. Liu, H. Guo & Y. Xu, 2022. Hydrogen sulfide improves tall fescue photosynthesis response to low-light stress by regulating chlorophyll and carotenoid metabolisms. Plant Physiology and Biochemistry 170: 133–145. https://doi.org/10.1016/j.plaphy.2021.12.002.
Liu, R., X. E. Ning, D. M. Li, L. Chen & Z. L. Ning, 2023a. The physiological responses of critically endangered species Ardisia gigantifolia Stapf (Primulaceae) to different light intensities. Photosynthetica 61(1): 115–123. https://doi.org/10.32615/ps.2023.011.
Liu, Y., M. Ma, Z. Ding, B. Liu, M. Jiang, X. Lu & Y. Lou, 2023b. Light-acquisition traits link aboveground biomass and environment in inner saline-alkaline herbaceous marshes. Science of the Total Environment 857. https://doi.org/10.1016/j.scitotenv.2022.159660.
Luan, J.-H., L. Zhang, Y.-C. Zou & X.-G. Lu, 2006. Ecological attributes of carex pseudocuraica over different water depth in the Sanjiang Plain (in Chinese). Wetland Science 2006(04): 258–263.
Lucero, J. E., A. Filazzola, R. M. Callaway, J. Braun, N. Ghazian, S. Haas, M. F. Miguel, M. Owen, M. Seifan, M. Zuliani & C. J. Lortie, 2022. Increasing global aridity destabilizes shrub facilitation of exotic but not native plant species. Global Ecology and Conservation 40. https://doi.org/10.1016/j.gecco.2022.e02345.
Lukács, B. A., A. E. Vojtkó, A. Mesterházy, V. A. Molnár, K. Süveges, Z. Végvári, G. Brusa & B. E. L. Cerabolini, 2017. Growth-form and spatiality driving the functional difference of native and alien aquatic plants in Europe. Ecology and Evolution 7(3): 950–963. https://doi.org/10.1002/ece3.2703.
Maoka, T., 2020. Carotenoids as natural functional pigments. Journal of Natural Medicines 74(1): 1–16. https://doi.org/10.1007/s11418-019-01364-x.
Martin, B. C., J. Bougoure, M. H. Ryan, W. W. Bennett, T. D. Colmer, N. K. Joyce, Y. S. Olsen & G. A. Kendrick, 2019. Oxygen loss from seagrass roots coincides with colonisation of sulphide-oxidising cable bacteria and reduces sulphide stress. Isme Journal 13(3): 707–719. https://doi.org/10.1038/s41396-018-0308-5.
Maxwell, K. & G. N. Johnson, 2000. Chlorophyll fluorescence – a practical guide. Journal of Experimental Botany 51(345): 659–668. https://doi.org/10.1093/jexbot/51.345.659.
Meisner, A., G. B. De Deyn, W. de Boer & W. H. van der Putten, 2013. Soil biotic legacy effects of extreme weather events influence plant invasiveness. Proceedings of the National Academy of Sciences of the United States of America 110(24): 9835–9838. https://doi.org/10.1073/pnas.1300922110.
Mikhailova, T. A., O. V. Kalugina, L. V. Afanas’eva & O. I. Nesterenko, 2010. Trends of chemical element content in needles of scots pine (Pinus sylvestris L.) under various natural conditions and emission load. Contemporary Problems of Ecology 3(2): 173–179. https://doi.org/10.1134/s1995425510020062.
Miller, H. L., III., C. Meile & A. B. Burd, 2007. A novel 2D model of internal O2 dynamics and H2S intrusion in seagrasses. Ecological Modelling 205(3–4): 365–380. https://doi.org/10.1016/j.ecolmodel.2007.03.004.
Minden, V. & M. Kleyer, 2015. Ecosystem multifunctionality of coastal marshes is determined by key plant traits. Journal of Vegetation Science 26(4): 651–662. https://doi.org/10.1111/jvs.12276.
Nazar, R., N. Iqbal, A. Masood, S. Syeed & N. A. Khan, 2011. Understanding the significance of sulfur in improving salinity tolerance in plants. Environmental and Experimental Botany 70(2–3): 80–87. https://doi.org/10.1016/j.envexpbot.2010.09.011.
Otieno, E. O., C. Shen, K. Zhang, J. Wan, M. He, Z. Tao, W. Huang & E. Siemann, 2023. Effects of nutrient pulses on exotic species shift from positive to neutral with decreasing water availability. Ecological Applications. https://doi.org/10.1002/eap.2805.
Pandey, A. K. & A. Gautam, 2020. Stress responsive gene regulation in relation to hydrogen sulfide in plants under abiotic stress. Physiologia Plantarum 168(2): 511–525. https://doi.org/10.1111/ppl.13064.
Parveen, M., T. Asaeda & M. H. Rashid, 2017a. Effect of hydrogen sulfide exposure on the growth, oxidative stress and carbohydrate metabolism of Elodea nuttallii and Egeria densa. Fundamental and Applied Limnology 191(1): 53–62. https://doi.org/10.1127/fal/2017/1046.
Parveen, M., T. Asaeda & M. H. Rashid, 2017b. Hydrogen sulfide induced growth, photosynthesis and biochemical responses in three submerged macrophytes. Flora 230: 1–11. https://doi.org/10.1016/j.flora.2017.03.005.
Parveen, M., T. Asaeda & M. H. Rashid, 2017c. Biochemical adaptations of four submerged macrophytes under combined exposure to hypoxia and hydrogen sulphide. Plos One 12(8). https://doi.org/10.1371/journal.pone.0182691.
Paul, B. D., S. H. Snyder & K. Kashfi, 2021. Effects of hydrogen sulfide on mitochondrial function and cellular bioenergetics. Redox Biology 38. https://doi.org/10.1016/j.redox.2020.101772.
Pérez-Harguindeguy, N., S. Díaz, E. Garnier, S. Lavorel, H. Poorter, P. Jaureguiberry, M. S. Bret-Harte, W. K. Cornwell, J. M. Craine, D. E. Gurvich, C. Urcelay, E. J. Veneklaas, P. B. Reich, L. Poorter, I. J. Wright, P. Ray, L. Enrico, J. G. Pausas, A. C. de Vos, N. Buchmann, G. Funes, F. Quétier, J. G. Hodgson, K. Thompson, H. D. Morgan, H. ter Steege, L. Sack, B. Blonder, P. Poschlod, M. V. Vaieretti, G. Conti, A. C. Staver, S. Aquino & J. H. C. Cornelissen, 2016. Corrigendum to: New handbook for standardised measurement of plant functional traits worldwide. Australian Journal of Botany 64(8). https://doi.org/10.1071/bt12225_co.
Pérez-Pérez, M. E., S. D. Lemaire & J. L. Crespo, 2012. Reactive oxygen species and autophagy in plants and algae. Plant Physiology 160(1): 156–164. https://doi.org/10.1104/pp.112.199992.
Petruzzella, A., C. H. A. van Leeuwen, E. van Donk & E. S. Bakker, 2020. Direct and indirect effects of native plants and herbivores on biotic resistance to alien aquatic plant invasions. Journal of Ecology 108(4): 1487–1496. https://doi.org/10.1111/1365-2745.13380.
Schmitz, R. A., S. H. Peeters, S. S. Mohammadi, T. Berben, T. van Erven, C. A. Iosif, T. van Alen, W. Versantvoort, M. S. M. Jetten, H. J. M. op den Camp & A. Pol, 2023. Simultaneous sulfide and methane oxidation by an extremophile. Nature Communications 14(1). https://doi.org/10.1038/s41467-023-38699-9.
Sharma, D. K., S. B. Andersen, C.-O. Ottosen & E. Rosenqvist, 2015. Wheat cultivars selected for high Fv/Fm under heat stress maintain high photosynthesis, total chlorophyll, stomatal conductance, transpiration and dry matter. Physiologia Plantarum 153(2): 284–298. https://doi.org/10.1111/ppl.12245.
Sharma, A., B. Shahzad, V. Kumar, S. K. Kohli, G. P. S. Sidhu, A. S. Bali, N. Handa, D. Kapoor, R. Bhardwaj & B. Zheng, 2019. Phytohormones regulate accumulation of osmolytes under abiotic stress. Biomolecules 9(7). https://doi.org/10.3390/biom9070285.
Silveira, M. J. & S. M. Thomaz, 2023. Effects of interactions between abiotic and biotic factors on growth of a non-native macrophyte. Biological Invasions 25(2): 431–440. https://doi.org/10.1007/s10530-022-02924-1.
Simkin, A. J., L. Kapoor, C. G. P. Doss, T. A. Hofmann, T. Lawson & S. Ramamoorthy, 2022. The role of photosynthesis related pigments in light harvesting, photoprotection and enhancement of photosynthetic yield in planta. Photosynthesis Research 152(1): 23–42. https://doi.org/10.1007/s11120-021-00892-6.
Tanaka, R. & A. Tanaka, 2005. Effects of chlorophyllide a oxygenase overexpression on light acclimation in Arabidopsis thaliana. Photosynthesis Research 85(3): 327–340. https://doi.org/10.1007/s11120-005-6807-z.
Tang, S. & C. Luo, 2012. Principles and Techniques of Plant Physiology Experiment (in Chinese), Southwest Normal University Press, Chongqing:
Tavanti, T. R., A. A. Rodrigues de Melo, L. D. Kaiber Moreira, D. E. Juarez Sanchez, R. dos Santos Silva, R. M. D. Silva & A. R. D. Reis, 2021. Micronutrient fertilization enhances ROS scavenging system for alleviation of abiotic stresses in plants. Plant Physiology and Biochemistry 160: 386–396. https://doi.org/10.1016/j.plaphy.2021.01.040.
Tounekti, T., A. M. Vadel, M. Onate, H. Khemira & S. Munne-Bosch, 2011. Salt-induced oxidative stress in rosemary plants: Damage or protection? Environmental and Experimental Botany 71(2): 298–305. https://doi.org/10.1016/j.envexpbot.2010.12.016.
van Kleunen, M., E. Weber & M. Fischer, 2010. A meta-analysis of trait differences between invasive and non-invasive plant species. Ecology Letters 13(2): 235–245. https://doi.org/10.1111/j.1461-0248.2009.01418.x.
Van Goethem, R. R., C. J. Huckins & A. M. Marcarelli, 2020. Effects of invasive watermilfoil on primary production in littoral zones of north-temperate lakes. Diversity-Basel 12(2). https://doi.org/10.3390/d12020082.
Wang, X. K. & Y. Y. **ng, 2017. Evaluation of the effects of irrigation and fertilization on tomato fruit yield and quality: a principal component analysis. Scientific Reports 7. https://doi.org/10.1038/s41598-017-00373-8.
Wei, B., D. Zhang, G. Wang, Y. Liu, Q. Li, Z. Zheng, G. Yang, Y. Peng, K. Niu & Y. Yang, 2023. Experimental warming altered plant functional traits and their coordination in a permafrost ecosystem. New Phytologist. https://doi.org/10.1111/nph.19115.
Wu, J., S. P. Cheng, W. Liang & Z. B. Wu, 2009. Effects of organic-rich sediment and below-ground sulfide exposure on submerged macrophyte, Hydrilla verticillata. Bulletin of Environmental Contamination and Toxicology 83(4): 497–501. https://doi.org/10.1007/s00128-009-9800-y.
**ao, K., D. Yu & Z. Wu, 2007. Differential effects of water depth and sediment type on clonal growth of the submersed macrophyte Vallisneria natans. Hydrobiologia 589: 265–272. https://doi.org/10.1007/s10750-007-0740-4.
**ao, Y., J. Tang, H. Qing, C. Zhou, W. Kong & S. An, 2011. Trade-offs among growth, clonal, and sexual reproduction in an invasive plant Spartina alterniflora responding to inundation and clonal integration. Hydrobiologia 658(1): 353–363. https://doi.org/10.1007/s10750-010-0505-3.
**ao, Y., J. Sun, F. Liu & T. Xu, 2016. Effects of salinity and sulphide on seed germination of three coastal plants. Flora 218: 86–91. https://doi.org/10.1016/j.flora.2015.12.002.
**e, D., D. Yu, L. F. Yu & C. H. Liu, 2010. Asexual propagations of introduced exotic macrophytes Elodea nuttallii, Myriophyllum aquaticum, and M. propinquum are improved by nutrient-rich sediments in China. Hydrobiologia 655(1): 37–47. https://doi.org/10.1007/s10750-010-0402-9.
Xu, X., L. Yang, X. Huang, Z. Li & D. Yu, 2018. Water brownification may not promote invasions of submerged non-native macrophytes. Hydrobiologia 817(1): 215–225. https://doi.org/10.1007/s10750-017-3387-9.
Yin, H. & Y. Wu, 2016. Factors affecting the production of volatile organic sulfur compounds (VOSCs) from algal-induced black water blooms in eutrophic freshwater lakes. Water Air and Soil Pollution 227(9). https://doi.org/10.1007/s11270-016-3061-2.
You, W., S. Fan, D. Yu, D. **e & C. Liu, 2014. An invasive clonal plant benefits from clonal integration more than a co-occurring native plant in nutrient-patchy and competitive environments. Plos One 9(5). https://doi.org/10.1371/journal.pone.0097246.
Yuan, G., L. Sun, P. Guo, J. **ao, W. Meng, B. Ren, A. Wu, Y. Li, H. Fu & E. Jeppesen, 2023. How eutrophication promotes exotic aquatic plant invasion in the lake littoral zone? Environmental Science & Technology 57(21): 8002–8014. https://doi.org/10.1021/acs.est.2c09486.
Zhang, J., T. Ren, J. Yang, L. Xu, M. Li, Y. Zhang, X. Han & N. He, 2021. Leaf multi-element network reveals the change of species dominance under nitrogen deposition. Frontiers in Plant Science 12. https://doi.org/10.3389/fpls.2021.580340.
Zhu, J., D. Yu & X. Xu, 2015. The phylogeographic structure of Hydrilla verticillata (Hydrocharitaceae) in China and its implications for the biogeographic history of this worldwide-distributed submerged macrophyte. Bmc Evolutionary Biology 15. https://doi.org/10.1186/s12862-015-0381-6.
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We sincerely appreciate the assistance from Dr. Tian Lv throughout the writing process.
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HL Conceptualization, Investigation, Methodology, Writing—review & editing. HH Formal analysis, Visualization, Writing—original draft, Writing—review & editing. HY and SF Funding acquisition, Resources, Writing—review & editing. CL Conceptualization, Writing—review & editing, Supervision.
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Liu, H., Huang, H., Yu, H. et al. Better growth and photosynthetic performance of Elodea nuttallii to short-term hydrogen sulfide than native Hydrilla verticillata. Hydrobiologia (2024). https://doi.org/10.1007/s10750-024-05592-5
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DOI: https://doi.org/10.1007/s10750-024-05592-5