Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE (Open Access)

Introducing the halophyte Salicornia europaea to investigate combined impact of salt and tidal submergence conditions

Angelina Jordine https://orcid.org/0009-0001-2121-2454 A * , Julia Retzlaff https://orcid.org/0009-0000-2773-0773 A , Lina Gens A , Brigitta Ehrt A , Lisa Fürtauer https://orcid.org/0000-0001-5248-4105 B and Joost T. van Dongen https://orcid.org/0000-0001-7944-9289 A *
+ Author Affiliations
- Author Affiliations

A Institute of Biology I, Aachen Biology and Biotechnology, RWTH Aachen University, Aachen 52074, Germany.

B Institute of Biology III, Aachen Biology and Biotechnology, RWTH Aachen University, Aachen 52074, Germany.


Handling Editor: Ole Pedersen

Functional Plant Biology 51, FP23228 https://doi.org/10.1071/FP23228
Submitted: 30 September 2023  Accepted: 6 February 2024  Published: 23 February 2024

© 2024 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND)

Abstract

Tolerance mechanisms to single abiotic stress events are being investigated in different plant species, but how plants deal with multiple stress factors occurring simultaneously is still poorly understood. Here, we introduce Salicornia europaea as a species with an extraordinary tolerance level to both flooding and high salt concentrations. Plants exposed to 0.5 M NaCl (mimicking sea water concentrations) grew larger than plants not exposed to salt. Adding more salt reduced growth, but concentrations up to 2.5 M NaCl were not lethal. Regular tidal flooding with salt water (0.5 M NaCl) did not affect growth or chlorophyll fluorescence, whereas continuous flooding stopped growth while plants survived. Quantitative polymerase chain reaction (qPCR) analysis of plants exposed to 1% oxygen in air revealed induction of selected hypoxia responsive genes, but these genes were not induced during tidal flooding, suggesting that S. europaea did not experience hypoxic stress. Indeed, plants were able to transport oxygen into waterlogged soil. Interestingly, sequential exposure to salt and hypoxic air changed the expression of several but not all genes as compared to their expression upon hypoxia only, demonstrating the potential to use S. europaea to investigate signalling-crosstalk between tolerance reactions to multiple environmental perturbations.

Keywords: extremophile, flooding, halophyte, hypoxia, Salicornia europaea, salt, stress response, tolerance.

References

Acosta-Motos JR, Ortuño MF, Bernal-Vicente A, Diaz-Vivancos P, Sanchez-Blanco MJ, Hernandez JA (2017) Plant responses to salt stress: adaptive mechanisms. Agronomy 7, 18.
| Crossref | Google Scholar |

Alef K (1991) ‘Methodenhandbuch Bodenmikrobiologie: Aktivitäten, Biomasse, Differenzierung.’ pp. 85–95. (Ecomed)

Andrews S (2010) FastQC: A Quality Control tool for High Throughput Sequence Data. Available at https://www.bioinformatics.babraham.ac.uk/projects/fastqc/

Armstrong W, Armstrong J, Beckett PM (1990) Measurement and modelling of oxygen release from roots of Phragmites australis. In ‘Constructed wetlands in water pollution control’. (Eds PF Cooper, BC Findlater) pp. 41–51. (Pergamon: Oxford, UK)

Bailey-Serres J, Voesenek LACJ (2008) Flooding stress: acclimations and genetic diversity. Annual Review of Plant Biology 59, 313-339.
| Crossref | Google Scholar | PubMed |

Bailey-Serres J, Lee SC, Brinton E (2012) Waterproofing crops: effective flooding survival strategies. Plant Physiology 160, 1698-1709.
| Crossref | Google Scholar | PubMed |

Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annual Review of Plant Biology 59, 89-113.
| Crossref | Google Scholar | PubMed |

Billings WD, Mooney HA (1968) The ecology of arctic and alpine plants. Biological Reviews 43, 481-529.
| Crossref | Google Scholar |

Biswal B, Joshi PN, Raval MK, Biswal UC (2011) Photosynthesis, a global sensor of environmental stress in green plants: stress signalling and adaptation. Current Science 101, 47-56.
| Google Scholar |

Bliss LC (1971) Arctic and alpine plant life cycles. Annual Review of Ecology and Systematics 2, 405-438.
| Crossref | Google Scholar |

Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114-2120.
| Crossref | Google Scholar | PubMed |

Bray EA, Bailey-Serres J, Weretilnyk E (2000) Responses to abiotic stress. In ‘Biochemistry & molecular biology of plants’. (Eds B Buchanan, W Gruissem, RL Jones) pp. 1158–1203. (American Society of Plant Physiologists)

Breckle SW (2002) Salinity, halophytes and salt affected natural ecosystems. In ‘Salinity: environment-plants-molecules’. (Eds A Läuchli, U Lüttge) pp. 53–77. (Springer: Dordrecht, Netherlands)

Chapman VJ (1974) Salt marshes and salt deserts of the world. In ‘Ecology of halophytes’. (Eds RJ Reimold, WH Queen) pp. 3–19. (Academic Press: London, UK)

Cooper A (1982) The effects of salinity and waterlogging on the growth and cation uptake of salt marsh plants. New Phytologist 90, 263-275.
| Crossref | Google Scholar |

de Fraine E (1913) The anatomy of the genus Salicornia. Botanical Journal of the Linnean Society 41, 317-348.
| Crossref | Google Scholar |

Fan P, Nie L, Jiang P, Feng J, Lv S, Chen X, Bao H, Guo J, Tai F, Wang J, Jia W, Li Y (2013) Transcriptome analysis of Salicornia europaea under saline conditions revealed the adaptive primary metabolic pathways as early events to facilitate salt adaptation. PLoS ONE 8, e80595.
| Crossref | Google Scholar |

Furtado BU, Gołębiewski M, Skorupa M, Hulisz P, Hrynkiewicz K (2019) Bacterial and fungal endophytic microbiomes of Salicornia europaea. Applied and Environmental Microbiology 85, e00305-19.
| Crossref | Google Scholar |

Garg R, Verma M, Agrawal S, Shankar R, Majee M, Jain M (2014) Deep transcriptome sequencing of wild halophyte rice, Porteresia coarctata, provides novel insights into the salinity and submergence tolerance factors. DNA Research 21, 69-84.
| Crossref | Google Scholar | PubMed |

Glup G (1985) ‘Dünen, Watt und Salzwiesen – Schutz und Erhaltung von Küste und Inseln, Tier- und Pflanzenwelt.’ (Niedersächsischer Minister für Ernährung, Landwirtschaft und Forsten) [In German]

Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q (2011) Full-Length transcriptome assembly from RNA-Seq data without a reference genome. Nature biotechnology 29, 644-652.
| Crossref | Google Scholar |

Gutterman Y (2012) ‘Seed germination in desert plants.’ (Springer Science & Business Media)

Haas BJ, Papanicolaou A, Yassour M, Grabherr M, Blood PD, Bowden J, Couger MB, Eccles D, Li B, Lieber M, MacManes MD, Ott M, Orvis J, Pochet N, Strozzi F, Weeks N, Westerman R, William T, Dewey CN, Henschel R, LeDuc RD, Friedman N, Regev A (2013) De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nature Protocols 8, 1494-1512.
| Crossref | Google Scholar | PubMed |

Hattori Y, Nagai K, Ashikari M (2011) Rice growth adapting to deepwater. Current Opinion in Plant Biology 14, 100-105.
| Crossref | Google Scholar | PubMed |

Hirabayashi Y, Mahendran R, Koirala S, Konoshima L, Yamazaki D, Watanabe S, Kim H, Kanae S (2013) Global flood risk under climate change. Nature Climate Change 3, 816-821.
| Crossref | Google Scholar |

Holt RD (2009) Bringing the Hutchinsonian niche into the 21st century: ecological and evolutionary perspectives. Proceedings of the National Academy of Sciences 106, 19659-19665.
| Crossref | Google Scholar |

Huang X, Madan A (1999) CAP3: a DNA sequence assembly program. Genome Research 9, 868-877.
| Crossref | Google Scholar | PubMed |

Isermeyer H (1952) Eine einfache Methode zur Bestimmung der Bodenatmung und der Karbonate im Boden. Zeitschrift für Pflanzenernährung, Düngung, Bodenkunde 56, 26-38 [In German].
| Crossref | Google Scholar |

Jacoby RP, Taylor NL, Millar AH (2011) The role of mitochondrial respiration in salinity tolerance. Trends in Plant Science 16, 614-623.
| Crossref | Google Scholar | PubMed |

Jäggi W (1976) Die Bestimmung der CO2-Bildung als Maß der bodenbiologischen Aktivität. Schweizer Landwirtschaftliche Forschung 15, 371-380 [In German].
| Google Scholar |

Kadereit G, Ball P, Beer S, Mucina L, Sokoloff D, Teege P, Yaprak AE, Freitag H (2007) A taxonomic nightmare comes true: phylogeny and biogeography of glassworts (Salicornia L., Chenopodiaceae). Taxon 56, 1143-1170.
| Crossref | Google Scholar |

Kalaji HM, Jajoo A, Oukarroum A, Brestic M, Zivcak M, Samborska IA, Cetner MD, Łukasik I, Goltsev V, Ladle RJ (2016) Chlorophyll a fluorescence as a tool to monitor physiological status of plants under abiotic stress conditions. Acta Physiologiae Plantarum 38, 102.
| Crossref | Google Scholar |

Keiffer CH, McCarthy BC, Ungar IA (1994) Effect of salinity and waterlogging on growth and survival of Salicornia europaea L., and inland halophyte. Ohio Journal of Science 94, 70-73.
| Google Scholar |

Kenrick P, Crane PR (1997) The origin and early evolution of plants on land. Nature 389, 33-39.
| Crossref | Google Scholar |

Koyro H-W (2002) Ultrastructural effects of salinity in higher plants. In ‘Salinity: environment-plants-molecules’. (Eds A Läuchli, U Lüttge) pp. 139–157. (Springer: Dordrecht, Netherlands)

Lamichhane S, Alpuerto JB, Han A, Fukao T (2020) The central negative regulator of flooding tolerance, the PROTEOLYSIS 6 branch of the N-degron pathway, adversely modulates salinity tolerance in Arabidopsis. Plants 9, 1415.
| Crossref | Google Scholar |

Liang W, Ma X, Wan P, Liu L (2018) Plant salt-tolerance mechanism: a review. Biochemical and Biophysical Research Communications 495, 286-291.
| Crossref | Google Scholar | PubMed |

Licausi F, Kosmacz M, Weits DA, Giuntoli B, Giorgi FM, Voesenek LACJ, Perata P, van Dongen JT (2011) Oxygen sensing in plants is mediated by an N-end rule pathway for protein destabilization. Nature 479, 419-422.
| Crossref | Google Scholar | PubMed |

Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25, 402-408.
| Crossref | Google Scholar | PubMed |

Loreti E, Perata P (2020) The many facets of hypoxia in plants. Plants 9, 745.
| Crossref | Google Scholar | PubMed |

Loreti E, Striker GG (2020) Plant responses to hypoxia: signaling and adaptation. Plants 9, 1704.
| Crossref | Google Scholar | PubMed |

Lv S, Jiang P, Chen X, Fan P, Wang X, Li Y (2012) Multiple compartmentalization of sodium conferred salt tolerance in Salicornia europaea. Plant Physiology and Biochemistry 51, 47-52.
| Crossref | Google Scholar | PubMed |

Ma J, Zhang M, Xiao X, You J, Wang J, Wang T, Yao Y, Tian C (2013) Global transcriptome profiling of Salicornia europaea L. shoots under NaCl treatment. PLoS ONE 8, e65877.
| Crossref | Google Scholar | PubMed |

Mahalingam R (2015) Consideration of combined stress: a crucial paradigm for improving multiple stress tolerance in plants. In ‘Combined stress in plants: physiological, molecular and biochemical aspects’. (Ed. R Mahalingam) pp. 1–26. (Springer)

Mahalingam R, Pandey P, Senthil-Kumar M (2021) Progress and prospects of concurrent or combined stress studies in plants. In ‘Annual plant reviews online, Vol. 4’. (Ed. JA Roberts) pp. 813–868. (John Wiley & Sons)

Manzur ME, Grimoldi AA, Insausti P, Striker GG (2009) Escape from water or remain quiescent? Lotus tenuis changes its strategy depending on depth of submergence. Annals of Botany 104, 1163-1169.
| Crossref | Google Scholar | PubMed |

Martins TS, Da-Silva CJ, Shabala S, Striker GG, Carvalho IR, de Oliveira ACB, do Amarante L (2024) Understanding plant responses to saline waterlogging: insights from halophytes and implications for crop tolerance. Planta 259, 24.
| Crossref | Google Scholar |

Maxwell K, Johnson GN (2000) Chlorophyll fluorescence – a practical guide. Journal of Experimental Botany 51, 659-668.
| Crossref | Google Scholar | PubMed |

Mazhar S, Pellegrini E, Contin M, Bravo C, De Nobili M (2022) Impacts of salinization caused by sea level rise on the biological processes of coastal soils – a review. Frontiers in Environmental Science 10, 909415.
| Crossref | Google Scholar |

McGraw DC, Ungar IA (1981) Growth and survival of the halophyte Salicornia europaera L. under saline field conditions. The Ohio Journal of Science 81, 109-113.
| Google Scholar |

Mishra A, Tanna B (2017) Halophytes: potential resources for salt stress tolerance genes and promoters. Frontiers in Plant Science 8, 829.
| Crossref | Google Scholar | PubMed |

Moatabarniya S, Chehregani Rad A, Khoshkholgh Sima NA, Askari H, Zeinalabedini M, Hesarkhani Z, Ghaffari MR (2022) Morphological and anatomical changes of Salicornia roots are associated with different salinity and nutrients conditions in contrasting genotypes. Rhizosphere 24, 100629.
| Crossref | Google Scholar |

Mommer L, Pons TL, Wolters-Arts M, Venema JH, Visser EJW (2005) Submergence-induced morphological, anatomical, and biochemical responses in a terrestrial species affect gas diffusion resistance and photosynthetic performance. Plant Physiology 139, 497-508.
| Crossref | Google Scholar | PubMed |

Nagai K, Hattori Y, Ashikari M (2010) Stunt or elongate? Two opposite strategies by which rice adapts to floods. Journal of Plant Research 123, 303-309.
| Crossref | Google Scholar | PubMed |

Patel MK, Kumar M, Li W, Luo Y, Burritt DJ, Alkan N, Tran L-SP (2020) Enhancing salt tolerance of plants: from metabolic reprogramming to exogenous chemical treatments and molecular approaches. Cells 9, 2492.
| Crossref | Google Scholar | PubMed |

Pellegrini E, Konnerup D, Winkel A, Casolo V, Pedersen O (2017) Contrasting oxygen dynamics in Limonium narbonense and Sarcocornia fruticosa during partial and complete submergence. Functional Plant Biology 44, 867-876.
| Crossref | Google Scholar | PubMed |

Pellegrini E, Forlani G, Boscutti F, Casolo V (2020) Evidence of non-structural carbohydrates-mediated response to flooding and salinity in Limonium narbonense and Salicornia fruticosa. Aquatic Botany 166, 103265.
| Crossref | Google Scholar |

Prihatini NS, Soemarno (2023) Role of plant-bacteria association in constructed wetlands for the removal of iron (Fe) from contaminated water. In ‘Aquatic macrophytes: ecology, functions and services’. (Eds S Kumar, K Bauddh, R Singh, N Kumar, R Kumar) pp. 297–311. (Springer)

Proetel H (1921) Das Meer - Tidebewegung. In ‘III. Teil. Wasserbau. 2. Band: See-und Seehafenbau. Handbibliothek für Bauingenieure’. (Ed. R Otzen) pp. 31–38. (Springer) [In German]

Razzaghi Komaresofla B, Alikhani HA, Etesami H, Khoshkholgh-Sima NA (2019) Improved growth and salinity tolerance of the halophyte Salicornia sp. by co–inoculation with endophytic and rhizosphere bacteria. Applied Soil Ecology 138, 160-170.
| Crossref | Google Scholar |

Redelstein R, Zotz G, Balke T (2018) Seedling stability in waterlogged sediments: an experiment with saltmarsh plants. Marine Ecology Progress Series 590, 95-108.
| Crossref | Google Scholar |

Rengasamy P, Olsson KA (1993) Irrigation and sodicity. Australian Journal of Soil Research 31, 821-837.
| Crossref | Google Scholar |

Rijkwaterstaat (2021) Terschelling Noordzee, Hoog- en laagwaterstanden en -tijdstippen. Ministerie van Infrastructur en Waterstaat, Netherlands. Available at https://getij.rws.nl/ [In Dutch]

Rizhsky L, Liang H, Shuman J, Shulaev V, Davletova S, Mittler R (2004) When defense pathways collide. The response of Arabidopsis to a combination of drought and heat stress. Plant Physiology 134, 1683-1696.
| Crossref | Google Scholar | PubMed |

Salazar OR, Chen K, Melino VJ, Reddy MP, Hřibová E, Čížková J, Beránková D, Aranda M, Jaremko L, Jaremko M, Fedoroff NV, Tester M, Schmöckel SM (2023) Learning from the expert: studying Salicornia to understand salinity tolerance [Preprint]. BioRxiv 2023–2004. doi:10.1101/2023.04.21.537482

Sarkar RK, Chakraborty K, Chattopadhyay K, Ray S, Panda D, Ismail AM (2019) Responses of rice to individual and combined stresses of flooding and salinity. In ‘Advances in rice research for abiotic stress tolerance’. (Eds M Hasanuzzaman, M Fujita, K Nahar, JK Biswas) pp. 281–297. (Woodhead Publishing)

Saviozzi A, Cardelli R, Di Puccio R (2011) Impact of salinity on soil biological activities: a laboratory experiment. Communications in Soil Science and Plant Analysis 42, 358-367.
| Crossref | Google Scholar |

Steffen S, Ball P, Mucina L, Kadereit G (2015) Phylogeny, biogeography and ecological diversification of Sarcocornia (Salicornioideae, Amaranthaceae). Annals of Botany 115, 353-368.
| Crossref | Google Scholar | PubMed |

Turnbull LA, Isbell F, Purves DW, Loreau M, Hector A (2016) Understanding the value of plant diversity for ecosystem functioning through niche theory. Proceedings of the Royal Society B: Biological Sciences 283, 20160536.
| Crossref | Google Scholar |

Ungar IA, Benner DK, McGraw DC (1979) The distribution and growth of Salicornia europaea on an inland salt pan. Ecology 60, 329-336.
| Crossref | Google Scholar |

van Aken HM (2008) Variability of the salinity in the western Wadden Sea on tidal to centennial time scales. Journal of Sea Research 59, 121-132.
| Crossref | Google Scholar |

van Dongen JT, Licausi F (2015) Oxygen sensing and signaling. Annual Review of Plant Biology 66, 345-367.
| Crossref | Google Scholar | PubMed |

van Regteren M, Amptmeijer D, de Groot AV, Baptist MJ, Elschot K (2020) Where does the salt marsh start? Field-based evidence for the lack of a transitional area between a gradually sloping intertidal flat and salt marsh. Estuarine, Coastal and Shelf Science 243, 106909.
| Crossref | Google Scholar |

Voegele RT, Schmid A (2011) RT real-time PCR-based quantification of Uromyces fabae in planta. FEMS Microbiology Letters 322, 131-137.
| Crossref | Google Scholar | PubMed |

Waters ER (2003) Molecular adaptation and the origin of land plants. Molecular Phylogenetics and Evolution 29, 456-463.
| Crossref | Google Scholar | PubMed |

Yang Y, Guo Y (2018) Elucidating the molecular mechanisms mediating plant salt-stress responses. New Phytologist 217, 523-539.
| Crossref | Google Scholar | PubMed |

Zabalza A, van Dongen JT, Froehlich A, Oliver SN, Faix B, Gupta KJ, Schmalzlin E, Igal M, Orcaray L, Royuela M, Geigenberger P (2009) Regulation of respiration and fermentation to control the plant internal oxygen concentration. Plant Physiology 149, 1087-1098.
| Crossref | Google Scholar | PubMed |

Zedler JB, Bonin CL, Larkin DJ, Varty A (2008) Salt marshes. In ‘Encyclopedia of ecology, Vol. 29’. (Eds SE Jørgensen, BD Fath) pp. 3132–3141. (Elsevier)