Freshwater wetland plants respond nonlinearly to inundation over a sustained period.

A-Ci curve Cyperaceae Poaceae flooding fructose glucose light curve marsh sucrose

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:
10 2021
Historique:
revised: 25 05 2021
received: 19 01 2021
accepted: 25 05 2021
pubmed: 8 10 2021
medline: 18 11 2021
entrez: 7 10 2021
Statut: ppublish

Résumé

Wetland plants regularly experience physiological stresses resulting from inundation; however, plant responses to the interacting effects of water level and inundation duration are not fully understood. We conducted a mesocosm experiment on two wetland species, sawgrass (Cladium jamaicense) and muhly grass (Muhlenbergia filipes), that co-dominate many freshwater wetlands in the Florida Everglades. We tracked photosynthesis, respiration, and growth at water levels of -10 (control), 10 (shallow), and 35 cm (deep) with reference to soil surface over 6 months. The response of photosynthesis to inundation was nonlinear. Specifically, photosynthetic capacity (A Overall, the two species exhibited nonlinear and contrasting patterns of carbon uptake and use under inundation stress, which ultimately defines their strategies of surviving regularly flooded habitats. The results suggest that a future scenario with more intensive inundation, due to the water management and climate change, may weaken the dominance of muhly grass in many freshwater wetlands of the Everglades.

Identifiants

pubmed: 34617586
doi: 10.1002/ajb2.1746
doi:

Substances chimiques

Soil 0

Types de publication

Journal Article Research Support, U.S. Gov't, Non-P.H.S.

Langues

eng

Sous-ensembles de citation

IM

Pagination

1917-1931

Informations de copyright

© 2021 The Authors. American Journal of Botany published by Wiley Periodicals LLC on behalf of Botanical Society of America.

Références

Akman, M., A. V. Bhikharie, E. H. McLean, A. Boonman, E. J. W. Visser, M. E. Schranz, and P. H. Tienderen. 2012. Wait or escape? Contrasting submergence tolerance strategies of Rorippa amphibia, Rorippa sylvestris and their hybrid. Annals of Botany 109: 1263-1275.
Armentano, T. V., J. P. Sah, M. S. Ross, D. T. Jones, H. C. Cooley, and C. S. Smith. 2006. Rapid responses of vegetation to hydrological changes in Taylor Slough, Everglades National Park, Florida, USA. Hydrobiologia 569: 293-309.
Bates, D., M. Maechler, B. Bolker, and S. Walker. 2015. Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67: 1-48.
Bellasio, C., D. J. Beerling, and H. Griffiths. 2016. Deriving C4 photosynthetic parameters from combined gas exchange and chlorophyll fluorescence using an Excel tool: theory and practice. Plant Cell and Environment 39: 1164-1179.
Bernacchi, C. J., E. L. Singsaas, C. Pimentel, A. R. Portis, and S. P. Long. 2001. Improved temperature response functions for models of Rubisco-limited photosynthesis. Plant Cell and Environment 24: 253-259.
Blom, C. W. P. M., and L. A. C. J. Voesenek. 1996. Flooding: the survival strategies of plants. Trends in Ecology & Evolution 11: 290-295.
Bragina, T., I. Drozdova, Y. V. Ponomareva, V. Alekhin, and G. Grineva. 2002. Photosynthesis, respiration, and transpiration in maize seedlings under hypoxia induced by complete flooding. Doklady Biological Sciences 384: 274-277.
Chapin, F. S., M. S. Torn, and M. Tateno. 1996. Principles of ecosystem sustainability. American Naturalist 148: 1016-1037.
Chen, H. J., M. F. Zamorano, and D. Ivanoff. 2010. Effect of flooding depth on growth, biomass, photosynthesis, and chlorophyll fluorescence of Typha domingensis. Wetlands 30: 957-965.
von Caemmerer, S. 2000. Biochemical models of leaf photosynthesis. Techniques in plant sciences no. 2. CSIRO Publishing, Collingwood, Australia.
Das, K. K., R. K. Sarkar, and A. M. Ismail. 2005. Elongation ability and non-structural carbohydrate levels in relation to submergence tolerance in rice. Plant Science 168: 131-136.
Duursma, R. A. 2015. Plantecophys-An R package for analysing and modelling leaf gas exchange data. PLoS One 10: 1-13.
Else, M. A., D. Coupland, L. Dutton, and M. B. Jackson. 2001. Decreased root hydraulic conductivity reduces leaf water potential, initiates stomatal closure and slows leaf expansion in flooded plants of castor oil (Ricinus communis) despite diminished delivery of ABA from the roots to shoots in xylem sap. Physiologia Plantarum 111: 46-54.
Ewing, K. 1996. Tolerance of four wetland plant species to flooding and sediment deposition. Environmental and Experimental Botany 36: 131-146.
Farquhar, G. D., S. V. Caemmerer, and J. A. Berry. 1980. A biochemical-model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149: 78-90.
Ghannoum, O. 2009. C4 photosynthesis and water stress. Annals of Botany 103: 635-644.
Grassi, G., and F. Magnani. 2005. Stomatal, mesophyll conductance and biochemical limitations to photosynthesis as affected by drought and leaf ontogeny in ash and oak trees. Plant, Cell and Environment 28: 834-849.
Hartmann, H., and S. Trumbore. 2016. Understanding the roles of nonstructural carbohydrates in forest trees-from what we can measure to what we want to know. New Phytologist 211: 386-403.
Islam, M. A., and S. E. Macdonald. 2004. Ecophysiological adaptations of black spruce (Picea mariana) and tamarack (Larix laricina) seedlings to flooding. Trees-Structure and Function 18: 35-42.
Jackson, M. B. 2002. Long-distance signalling from roots to shoots assessed: the flooding story. Journal of Experimental Botany 53: 175-181.
Jackson, M. B., and W. Armstrong. 1999. Formation of aerenchyma and the processes of plant ventilation in relation to soil flooding and submergence. Plant Biology 1: 274-287.
Jones, S. F., C. L. Stagg, K. W. Krauss, and M. W. Hester. 2018. Flooding alters plant-mediated carbon cycling independently of elevated atmospheric CO2 concentrations. Journal of Geophysical Research: Biogeosciences 123: 1976-1987.
Kaiser, E., A. Morales, J. Harbinson, J. Kromdijk, E. Heuvelink, and L. F. M. Marcelis. 2015. Dynamic photosynthesis in different environmental conditions. Journal of Experimental Botany 66: 2415-2426.
Kayranli, B., M. Scholz, A. Mustafa, and Å. Hedmark. 2010. Carbon storage and fluxes within freshwater wetlands: a critical review. Wetlands 30: 111-124.
Kludze, H. K., and R. D. DeLaune. 1996. Soil redox intensity effects on oxygen exchange and growth of cattail and sawgrass. Soil Science Society of America Journal 60: 616-621.
Kromer, S. 1995. Respiration during photosynthesis. Annual Review of Plant Physiology and Plant Molecular Biology 46: 45-70.
Kuznetsova, A., P. Brockhoff, and R. Christensen. 2016. lmerTest: tests in linear mixed effects models. R package version 2.0-30. Website: https://CRAN.R-project.org/package=lmerTest
Kyei-Boahen, S., R. Lada, T. Astatkie, R. Gordon, and C. Caldwell. 2003. Photosynthetic response of carrots to varying irradiances. Photosynthetica 41: 301-305.
Lan, Z. C., H. Huang, Y. S. Chen, J. S. Liu, J. G. Chen, L. Li, L. Li, et al. 2019. Testing mechanisms underlying responses of plant functional traits to flooding duration gradient in a lakeshore meadow. Journal of Freshwater Ecology 34: 481-495.
Landhausser, S. M., P. S. Chow, L. T. Dickman, M. E. Furze, I. Kuhlman, S. Schmid, J. Wiesenbauer, et al. 2018. Standardized protocols and procedures can precisely and accurately quantify non-structural carbohydrates. Tree Physiology 38: 1764-1778.
Lenth, R. 2019. emmeans: estimated marginal means, aka least-squares means: R package version 1.3.4. Website: https://CRAN.R-project.org
Liao, C. T., and C. H. Lin. 1994. Effect of flooding stress on photosynthetic activities of Momordica charantia. Plant Physiology and Biochemistry 32: 479-485.
Loreti, E., H. van Veen, and P. Perata. 2016. Plant responses to flooding stress. Current Opinion in Plant Biology 33: 64-71.
Luo, Y. Q., D. F. Hui, W. X. Cheng, J. S. Coleman, D. W. Johnson, and D. A. Sims. 2000. Canopy quantum yield in a mesocosm study. Agricultural and Forest Meteorology 100: 35-48.
Miller, R. C., and J. B. Zedler. 2003. Responses of native and invasive wetland plants to hydroperiod and water depth. Plant Ecology 167: 57-69.
Moldau, H. 1973. Effects of various water regimes on stomatal and mesophyll conductances of bean leaves. Photosynthetica 7: 1-7.
Mommer, L., and E. J. W. Visser. 2005. Underwater photosynthesis in flooded terrestrial plants: a matter of leaf plasticity. Annals of Botany 96: 581-589.
Pan, Y., Y. H. Xie, X. S. Chen, and F. Li. 2012. Effects of flooding and sedimentation on the growth and physiology of two emergent macrophytes from Dongting Lake wetlands. Aquatic Botany 100: 35-40.
Perry, W. 2004. Elements of south Florida's comprehensive Everglades restoration plan. Ecotoxicology 13: 185-193.
Pezeshki, S. R. 1993. Differences in patterns of photosynthetic responses to hypoxia in flood-tolerant and flood-sensitive tree species. Photosynthetica 28: 423-430.
Pezeshki, S. R. 1994. Responses of baldcypress (Taxodium distichum) seedlings to hypoxia-leaf protein-content, ribulose-1,5-bisphosphate carboxylase oxygenase activity and photosynthesis. Photosynthetica 30: 59-68.
Pezeshki, S. R. 2001. Wetland plant responses to soil flooding. Environmental and Experimental Botany 46: 299-312.
Pezeshki, S. R., S. W. Matthews, and R. D. Delaune. 1991. Root cortex structure and metabolic responses of Spartina patens to soil redox conditions. Environmental and Experimental Botany 31: 91-97.
Pezeshki, S. R., R. D. DeLaune, H. K. Kludze, and H. S. Choi. 1996. Photosynthetic and growth responses of cattail (Typha domingensis) and sawgrass (Cladium jamaicense) to soil redox conditions. Aquatic Botany 54: 25-35.
Qin, X. Y., F. Li, X. S. Chen, and Y. H. Xie. 2013. Growth responses and non-structural carbohydrates in three wetland macrophyte species following submergence and de-submergence. Acta Physiologiae Plantarum 35: 2069-2074.
R Core Team. 2020. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Website: http://www.R-project.org/
Ram, P. C., B. B. Singh, A. K. Singh, P. Ram, P. N. Singh, H. P. Singh, I. Boamfa, et al. 2002. Submergence tolerance in rainfed lowland rice: physiological basis and prospects for cultivar improvement through marker-aided breeding. Field Crops Research 76: 131-152.
Richards, J. H., and P. C. Olivas. 2020. A common-mesocosm experiment recreates sawgrass (Cladium jamaicense) phenotypes from Everglades marl prairies and peat marshes. American Journal of Botany 107: 56-65.
Rose, C., and W. G. Crumpton. 1996. Effects of emergent macrophytes on dissolved oxygen dynamics in a prairie pothole wetland. Wetlands 16: 495-502.
Salmon, Y., A. Lintunen, A. Dayet, T. Chan, R. Dewar, T. Vesala, and T. Hooltta. 2020. Leaf carbon and water status control stomatal and nonstomatal limitations of photosynthesis in trees. New Phytologist 266: 690-703.
Schedlbauer, J. L., S. F. Oberbauer, G. Starr, and K. L. Jimenez. 2010. Seasonal differences in the CO2 exchange of a short-hydroperiod Florida Everglades marsh. Agricultural and Forest Meteorology 150: 994-1006.
Thornley, J. H. M. 1998. Dynamic model of leaf photosynthesis with acclimation to light and nitrogen. Annals of Botany 81: 421-430.
Todd, M. J., R. Muneepeerakul, D. Pumo, S. Azaele, F. Miralles-Wilhelm, A. Rinaldo, and I. Rodriguez-Iturbe. 2010. Hydrological drivers of wetland vegetation community distribution within Everglades National Park, Florida. Advances in Water Resources 33: 1279-1289.
Troxler, T. G., D. L. Childers, and C. J. Madden. 2014. Drivers of decadal-scale change in southern everglades wetland macrophyte communities of the coastal ecotone. Wetlands 34: S81-S90.
Voesenek, L. A. C. J., and J. Bailey-Serres. 2015. Flood adaptive traits and processes: an overview. New Phytologist 206: 57-73.
Vu, J. C. V., and G. Yelenosky. 1992. Photosynthetic responses of rough lemon and sour orange to soil flooding, chilling, and short-term temperature fluctuations during growth. Environmental and Experimental Botany 32: 471-477.
Wample, R. L., and R. W. Davis. 1983. Effect of flooding on starch accumulation in chloroplasts of sunflower (Helianthus annuus L). Plant Physiology 73: 195-198.
Wickham, H. 2016. ggplot2: elegant graphics for data analysis. Springer-Verlag, NY, NY, USA.
Zhao, J., S. L. Malone, S. F. Oberbauer, P. C. Olivas, J. L. Schedlbauer, C. L. Staudhammer, and G. Starr. 2019. Intensified inundation shifts a freshwater wetland from a CO2 sink to a source. Global Change Biology 25: 3319-3333.
Zhao, J., S. F. Oberbauer, P. C. Olivas, J. L. Schedlbauer, J. L. May, J. G. Moser, S. L. Malone, et al. 2018. Contrasting photosynthetic responses of two dominant macrophyte species to seasonal inundation in an Everglades freshwater prairie. Wetlands 38: 893-903.

Auteurs

Junbin Zhao (J)

Department of Biological Sciences and Southeast Environmental Research Center, Florida International University, Miami, FL, USA.
Department of Biogeochemistry and Soil Quality, Division of Environment and Natural Resources, Norwegian Institute of Bioeconomy Research, Ås, Norway.

Sparkle L Malone (SL)

Department of Biological Sciences and Southeast Environmental Research Center, Florida International University, Miami, FL, USA.

Christina L Staudhammer (CL)

Department of Biological Sciences, University of Alabama, Tuscaloosa, AL, USA.

Gregory Starr (G)

Department of Biological Sciences, University of Alabama, Tuscaloosa, AL, USA.

Henrik Hartmann (H)

Max Planck Institute for Biogeochemistry, Hans-Knöll-Str 10, Jena 07745, Germany.

Steven F Oberbauer (SF)

Department of Biological Sciences and Southeast Environmental Research Center, Florida International University, Miami, FL, USA.

Articles similaires

Populus Soil Microbiology Soil Microbiota Fungi
Humans Climate Change Health Personnel Surveys and Questionnaires Medical Oncology
Lakes Salinity Archaea Bacteria Microbiota
Rivers Turkey Biodiversity Environmental Monitoring Animals

Classifications MeSH