Dryland soil salinity and seasonal effects on leaf and xylem sap ecophysiological characteristics of native plant species
E. Mapfumo
A *
+ Author Affiliations
- Author Affiliations
A Concordia University of Edmonton, 7128 Ada Boulevard, Edmonton, AB T5B 4E4, Canada.
Australian Journal of Botany 70(1) 42-55 https://doi.org/10.1071/BT21022
Submitted: 23 February 2021 Accepted: 27 October 2021 Published: 26 November 2021
© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing
Abstract
The objective of this 3-year study was to investigate the relationships between soil salinity and ecophysiological responses of C3 and C4 native plant species around Lake Altham and Lake Coyrecup (both are salt lakes in Western Australia), and to evaluate their potential for use in the remediation of salt-affected soils. Three shrubs (Atriplex vesicaria, Tecticornia lepidosperma and T. indica) that grew in highly saline soil of average Na concentration greater than 300 mM had higher leaf δ13C and δ15N ratios. These species also had higher Na-to-K and Na-to-Ca ratios in both their leaves and stem xylem sap, indicating that these species accumulate high amounts of sodium in their tissues. In contrast, tree species Eucalyptus loxophleba, Casuarina obesa and Acacia acuminata grew in soil of average Na concentration of less than 100 mM and had lower values of δ15N, δ13C, Na content, and Na-to-K ratio in their leaves. These species also had lower xylem Na-to-K and Na-to-Ca ratios. Seasonal effects were observed in leaf total N content, leaf Na, xylem sap Na-to-K ratio and xylem sap Na-to-Ca ratio. Strong and significant positive correlations (r > 0.75; P < 0.01) were observed between soil Na concentration and ecophysiological responses, such as leaf Na contents, leaf δ15N, xylem sap Na, xylem Na-to-K ratio and xylem Na-to-Ca ratio. Overall, Atr. vesicaria, T. lepidosperma, T. indica and Santalum acuminatum are good candidates for remediation of highly saline soils.
Keywords: ecophysiology, halophytes, ion ratios, plant adaptation, remediation, salinity, salt lakes, stable isotope ratios.
References
Asch F, Dingkuhn M, Dörffling K, Miezan K (2000) Leaf K/Na ratio predicts salinity induced yield loss in irrigated rice. Euphytica 113, 109–118.| Leaf K/Na ratio predicts salinity induced yield loss in irrigated rice.Crossref | GoogleScholarGoogle Scholar |
Assaha DVM, Ueda A, Saneoka H, Al-Yahyai R, Yaish MW (2017) The role of Na+ and K+ transporters in salt stress adaptation in glycophytes. Frontiers in Physiology 8, 509.
| The role of Na+ and K+ transporters in salt stress adaptation in glycophytes.Crossref | GoogleScholarGoogle Scholar | 28769821PubMed |
Barakat NAM, Cazzato E, Nedjimi B, Kabiel HF, Laudadio V, Tufarelli V (2013) Ecophysiological and species-specific responses to seasonal variations in halophytic species of the chenopodiaceae in a Mediterranean salt marsh. African Journal of Ecology 52, 163–172.
| Ecophysiological and species-specific responses to seasonal variations in halophytic species of the chenopodiaceae in a Mediterranean salt marsh.Crossref | GoogleScholarGoogle Scholar |
Barrett-Lennard EG (2002) Restoration of saline land through revegetation. Agricultural Water Management 53, 213–226.
| Restoration of saline land through revegetation.Crossref | GoogleScholarGoogle Scholar |
Barrett-Lennard EG (2003) The interaction between waterlogging and salinity in higher plants: causes, consequences and implications. Plant and Soil 253, 35–54.
| The interaction between waterlogging and salinity in higher plants: causes, consequences and implications.Crossref | GoogleScholarGoogle Scholar |
Bazihizina N, Barrett-Lennard EG, Colmer TD (2012) Plant responses to heterogeneous salinity: growth of the halophyte Atriplex nummularia is determined by the root-weighted mean salinity of the root zone. Journal of Experimental Botany 63, 6347–6358.
| Plant responses to heterogeneous salinity: growth of the halophyte Atriplex nummularia is determined by the root-weighted mean salinity of the root zone.Crossref | GoogleScholarGoogle Scholar | 23125356PubMed |
Bell DT (1999) Australia trees for the rehabilitation of waterlogged and salinity-damaged landscapes. Australian Journal of Botany 47, 697–716.
| Australia trees for the rehabilitation of waterlogged and salinity-damaged landscapes.Crossref | GoogleScholarGoogle Scholar |
Boutton TW, Liao JD (2010) Changes in soil nitrogen storage and δ15N with woody plant encroachment in a subtropical savanna parkland landscape. Journal of Geophysical Research 115, G03019.
| Changes in soil nitrogen storage and δ15N with woody plant encroachment in a subtropical savanna parkland landscape.Crossref | GoogleScholarGoogle Scholar |
Bustamante MMC, Martinelli LA, Silva DA, Camargo PB, Klink CA, Domingues TF, Santos RV (2004) 15N natural abundance in woody plants and soils of central Brazilian savannas (cerrado). Ecological Applications 14, 200–213.
| 15N natural abundance in woody plants and soils of central Brazilian savannas (cerrado).Crossref | GoogleScholarGoogle Scholar |
Carter JL, Colmer TD, Veneklaas EJ (2006) Variable tolerance of wetland tree species to combined salinity and waterlogging is related to regulation of ion uptake and production of organic solutes. New Phytologist 169, 123–134.
| Variable tolerance of wetland tree species to combined salinity and waterlogging is related to regulation of ion uptake and production of organic solutes.Crossref | GoogleScholarGoogle Scholar |
Casolo V, Tomasella M, De Col V, Braidot E, Savi T, Nardini A (2014) Water relations of an invasive halophyte (Spartina patens): osmoregulation and ionic effects on xylem hydraulics. Functional Plant Biology 42, 264–273.
| Water relations of an invasive halophyte (Spartina patens): osmoregulation and ionic effects on xylem hydraulics.Crossref | GoogleScholarGoogle Scholar |
Cernusak LA, Ubierna N, Winter K, Holtum JAM, Marshall JD, Farquhar GD (2013) Environmental and physiological determinants of carbon isotope discrimination in terrestrial plants. New Phytologist 200, 950–965.
| Environmental and physiological determinants of carbon isotope discrimination in terrestrial plants.Crossref | GoogleScholarGoogle Scholar |
de Araújo SAM, Silveira JAG, Almeida TD, Rocha IMA, Morais DL, Viégas RA (2006) Salinity tolerance of halophyte Atriplex nummularia L. grown under increasing NaCl levels. Revista Brasileira de Engenharia Agrícola e Ambiental 10, 848–854.
| Salinity tolerance of halophyte Atriplex nummularia L. grown under increasing NaCl levels.Crossref | GoogleScholarGoogle Scholar |
English JP, Colmer TD (2013) Tolerance of extreme salinity in two stem-succulent halophytes (Tecticornia species). Functional Plant Biology 40, 897–912.
| Tolerance of extreme salinity in two stem-succulent halophytes (Tecticornia species).Crossref | GoogleScholarGoogle Scholar | 32481159PubMed |
Farquhar GD, Ball MC, von Caemmerer S, Roksandic Z (1982) Effect of salinity and humidity on δ13C value of halophytes – evidence of diffusional isotope fractionation determined by the ratio of intercellular/atmospheric partial pressure of CO2 under different environmental conditions. Oecologia 52, 121–124.
| Effect of salinity and humidity on δ13C value of halophytes – evidence of diffusional isotope fractionation determined by the ratio of intercellular/atmospheric partial pressure of CO2 under different environmental conditions.Crossref | GoogleScholarGoogle Scholar | 28310117PubMed |
Flowers TJ (1985) Physiology of halophytes. Plant and Soil 89, 41–56.
| Physiology of halophytes.Crossref | GoogleScholarGoogle Scholar |
Flowers TJ, Colmer TD (2008) Salinity tolerance in halophytes. New Phytologist 179, 945–963.
| Salinity tolerance in halophytes.Crossref | GoogleScholarGoogle Scholar |
Flowers TJ, Hajibagheri MA, Clipson NJW (1986) Halophytes. The Quarterly Review of Biology 61, 313–337.
| Halophytes.Crossref | GoogleScholarGoogle Scholar |
Fowler J, Cohen L, Jarvis P (1998) ‘Practical statistics for field biology’, 2nd edn. (Wiley: New York, NY, USA)
Ghorbanalizadeh A, Akhani H, Bergmeier E (2020) Vegetation patterns of a rapidly drying up salt lake ecosystem: Lake Urmia, NW Iran. Phytocoenologia 50, 1–46.
| Vegetation patterns of a rapidly drying up salt lake ecosystem: Lake Urmia, NW Iran.Crossref | GoogleScholarGoogle Scholar |
Gil R, Bautista I, Boscaiu M, Lidón A, Wankhade S, Sánchez H, Llinares J, Vicente O (2014) Responses of five Mediterranean halophytes to seasonal changes in environmental conditions. AoB PLANTS 6, plu049
| Responses of five Mediterranean halophytes to seasonal changes in environmental conditions.Crossref | GoogleScholarGoogle Scholar | 25139768PubMed |
Gorham J (1996) Mechanisms of salt tolerance of halophytes. In ‘Halophytes and biosaline agriculture’. (Eds R Choukr-Allah, CV Malcolm, A Hamdy) pp. 31–53. (Marcel Dekker Inc.: New York, NY, USA)
Guy RD, Reid DM, Krouse HR (1986) Factors affecting 13C/12C ratios of inland halophytes. II. Ecophysiological interpretations of patterns in the field. Canadian Journal of Botany 64, 2700–2707.
| Factors affecting 13C/12C ratios of inland halophytes. II. Ecophysiological interpretations of patterns in the field.Crossref | GoogleScholarGoogle Scholar |
Hasanuzzaman M, Nahar K, Alam MM, Bhowmik PC, Hossain MA, Rahman MM, Prasad MNV, Ozturk M, Fujita M (2014) Potential use of halophytes to remediate saline soils. BioMed Research International 2014, 1–12.
| Potential use of halophytes to remediate saline soils.Crossref | GoogleScholarGoogle Scholar |
Hobbie EA, Werner RA (2004) Intramolecular, compound-specific, and bulk carbon isotope patterns in C3 and C4 plants: a review and synthesis. The New Phytologist 161, 371–385.
| Intramolecular, compound-specific, and bulk carbon isotope patterns in C3 and C4 plants: a review and synthesis.Crossref | GoogleScholarGoogle Scholar |
Hobbie EA, Macko SA, Williams M (2000) Correlations between foliar δ15N and nitrogen concentrations may indicate plant–mycorrhizal interactions. Oecologia 122, 273–283.
| Correlations between foliar δ15N and nitrogen concentrations may indicate plant–mycorrhizal interactions.Crossref | GoogleScholarGoogle Scholar | 28308382PubMed |
Högberg P (1997) 15N natural abundance in soil-plant systems. New Phytologist 137, 179–203.
| 15N natural abundance in soil-plant systems.Crossref | GoogleScholarGoogle Scholar |
Kozlowski TT (1997) Responses of woody plants to flooding and salinity. Tree Physiology Monograph 17, 490
| Responses of woody plants to flooding and salinity.Crossref | GoogleScholarGoogle Scholar |
Krauss KW, Lovelock CE, McKee KL, López-Hoffman L, Ewe SML, Sousa WP (2008) Environmental drivers in mangrove establishment and early development: a review. Aquatic Botany 89, 105–127.
| Environmental drivers in mangrove establishment and early development: a review.Crossref | GoogleScholarGoogle Scholar |
Ladd SN, Sachs JP (2013) Positive correlation between salinity and n-alkane δ13C values in the mangrove Avicennia marina. Organic Geochemistry 64, 1–8.
| Positive correlation between salinity and n-alkane δ13C values in the mangrove Avicennia marina.Crossref | GoogleScholarGoogle Scholar |
LoPresti EF (2014) Chenopod salt bladders deter insect herbivores. Oecologia 174, 921–930.
| Chenopod salt bladders deter insect herbivores.Crossref | GoogleScholarGoogle Scholar | 24241642PubMed |
Loveys BR, Loveys BR, Tyerman SD (2001) Water relations and gas exchange of the root hemiparasite Santalum acuminatum (Quandong). Australian Journal of Botany 49, 479–486.
| Water relations and gas exchange of the root hemiparasite Santalum acuminatum (Quandong).Crossref | GoogleScholarGoogle Scholar |
Ma S, He F, Tian D, Zou D, Yan Z, Yang Y, Zhou T, Huang K, Shen H, Fang J (2018) Variations and determinants of carbon content in plants: a global synthesis. Biogeosciences 15, 693–702.
| Variations and determinants of carbon content in plants: a global synthesis.Crossref | GoogleScholarGoogle Scholar |
Males J (2017) Secrets of succulence. Journal of Experimental Botany 68, 2121–2134.
| Secrets of succulence.Crossref | GoogleScholarGoogle Scholar | 28369497PubMed |
Muller O, Hirose T, Werger MJA, Hikosaka K (2011) Optimal use of leaf nitrogen explains seasonal changes in leaf nitrogen content of an understorey evergreen shrub. Annals of Botany 108, 529–536.
| Optimal use of leaf nitrogen explains seasonal changes in leaf nitrogen content of an understorey evergreen shrub.Crossref | GoogleScholarGoogle Scholar | 21757476PubMed |
Murakeözya EP, Nagya Z, Duhazé C, Bouchereau A, Tuba Z (2003) Seasonal changes in the levels of compatible osmolytes in three halophytic species of inland saline vegetation in Hungary. Journal of Plant Physiology 160, 395–401.
| Seasonal changes in the levels of compatible osmolytes in three halophytic species of inland saline vegetation in Hungary.Crossref | GoogleScholarGoogle Scholar |
Nedjimi B (2012) Seasonal variation in productivity, water relations and ion contents of Atriplex halimus spp. schweinfurthii grown in Chott Zehrez wetland, Algeria. Journal of the Saudi Society of Agricultural Sciences 11, 43–49.
| Seasonal variation in productivity, water relations and ion contents of Atriplex halimus spp. schweinfurthii grown in Chott Zehrez wetland, Algeria.Crossref | GoogleScholarGoogle Scholar |
Niknam SR, McComb J (2000) Salt tolerance screening of selected Australian woody species – a review. Forest Ecology and Management 139, 1–19.
| Salt tolerance screening of selected Australian woody species – a review.Crossref | GoogleScholarGoogle Scholar |
Pate JS, Dawson TE (1999) Assessing the performance of woody plants in uptake and utilization of carbon, water and nutrients: implications for designing agricultural mimic systems. Agroforestry Systems 45, 245–275.
| Assessing the performance of woody plants in uptake and utilization of carbon, water and nutrients: implications for designing agricultural mimic systems.Crossref | GoogleScholarGoogle Scholar |
Rayment GE, Higginson FR (1992) ‘Australian laboratory handbook of soil and water chemical methods’,(Inkata Press: Melbourne, Vic., Australia)
Short DC, Colmer TD (1999) Salt tolerance in the halophyte Halosarcia pergranulata subsp. pergranulata. Annals of Botany 83, 207–213.
| Salt tolerance in the halophyte Halosarcia pergranulata subsp. pergranulata.Crossref | GoogleScholarGoogle Scholar |
Suaire R, Durickovic I, Framont-Terrasse L, Leblain J-Y, De Rouck A-C, Simonnot M-O (2016) Phytoextraction of Na+ and Cl− by Atriplex halimus L. and Atriplex hortensis L.: a promising solution for remediation of road runoff contaminated with deicing salts. Ecological Engineering 94, 182–189.
| Phytoextraction of Na+ and Cl− by Atriplex halimus L. and Atriplex hortensis L.: a promising solution for remediation of road runoff contaminated with deicing salts.Crossref | GoogleScholarGoogle Scholar |
Tester M, Davenport R (2003) Na+ tolerance and Na+ transport in higher plants: a review article. Annals of Botany 91, 503–527.
| Na+ tolerance and Na+ transport in higher plants: a review article.Crossref | GoogleScholarGoogle Scholar | 12646496PubMed |
Tug GN, Ketenoglu O, Bilgin A (2012) The relationships between plant zonation and edaphic factors in halophytic vegetation around Lake Tuz, Central Anatolia, Turkey. Rendiconti Lincei 23, 355–363.
| The relationships between plant zonation and edaphic factors in halophytic vegetation around Lake Tuz, Central Anatolia, Turkey.Crossref | GoogleScholarGoogle Scholar |
Tyree MT, Salleo S, Nardini A, Assunta Lo Gullo M, Mosca R (1999) Refilling of embolized vessels in young stems of laurel. Do we need a new paradigm? Plant Physiology 120, 11–22.
| Refilling of embolized vessels in young stems of laurel. Do we need a new paradigm?Crossref | GoogleScholarGoogle Scholar |
USDA (1954) ‘Diagnosis and improvement of saline and alkali soils’, Handbook 60. (USDA)
van der Moezel PG, Bell DT (1990) Saltland reclamation: selection of superior Australian tree genotypes for discharge sites. Proceedings of the Ecological Society of Australia 16, 545–549.
van der Moezel PG, Walton CS, Pearce-Pinto GVN, Bell DT (1989) Screening for salinity and waterlogging tolerance in five Casuarina species. Landscape and Urban Planning 17, 331–337.
| Screening for salinity and waterlogging tolerance in five Casuarina species.Crossref | GoogleScholarGoogle Scholar |
van der Moezel PG, Pearce-Pinto GVN, Bell DT (1991) Screening for salt and waterlogging tolerance in Eucalyptus and Melaleuca species. Forest Ecology and Management 40, 27–37.
| Screening for salt and waterlogging tolerance in Eucalyptus and Melaleuca species.Crossref | GoogleScholarGoogle Scholar |
Wakeel A (2013) Potassium–sodium interactions in soil and plant under saline-sodic conditions. Journal of Plant Nutrition and Soil Science 176, 344–354.
| Potassium–sodium interactions in soil and plant under saline-sodic conditions.Crossref | GoogleScholarGoogle Scholar |
Walker RR (1989) Growth, photosynthesis and distribution of chloride, sodium and potassium ions in salt-affected Quandong (Santalum acuminatum. Australian Journal of Plant Physiology 16, 365–377.
| Growth, photosynthesis and distribution of chloride, sodium and potassium ions in salt-affected Quandong (Santalum acuminatum.Crossref | GoogleScholarGoogle Scholar |
Walker CD, Sinclair R (1992) Soil salinity is correlated with a decline in 13C discrimination in leaves of Atriplex species. Australian Journal of Ecology 17, 83–88.
| Soil salinity is correlated with a decline in 13C discrimination in leaves of Atriplex species.Crossref | GoogleScholarGoogle Scholar |
Wang X, Kong F, Kong W, Xu W (2018) Edaphic characterization and plant zonation in the Qaidam Basin, Tibetan Plateau. Scientific Reports 8, 1822
| Edaphic characterization and plant zonation in the Qaidam Basin, Tibetan Plateau.Crossref | GoogleScholarGoogle Scholar | 29379126PubMed |
Welker JM, Jónsdóttir IS, Fahnestock JT (2003) Leaf isotopic (δ13C and δ15N) and nitrogen contents of Carex plants along the Eurasian Coastal Arctic: results from the Northeast Passage expedition. Polar Biology 27, 29–37.
| Leaf isotopic (δ13C and δ15N) and nitrogen contents of Carex plants along the Eurasian Coastal Arctic: results from the Northeast Passage expedition.Crossref | GoogleScholarGoogle Scholar |
Werner C, Schnyder H, Cuntz M, Keitel C, Zeemans MJ, Dawson TE, Badeck F-W, Brugnoli E, Ghashghaie J, Grams TEE, Kayler ZE, Lakatos M, Lee X, Máguas C, Ogée J, Rascher KG, Siegwolf RTW, Unger S, Welker J, Wingate L, Gessler A (2012) Progress and challenges in using stable isotopes to trace plant carbon and water relations across scales. Biogeosciences 9, 3083–3111.
| Progress and challenges in using stable isotopes to trace plant carbon and water relations across scales.Crossref | GoogleScholarGoogle Scholar |
Zarei M, Shabala S, Zeng F, Chen X, Zhang S, Azizi M, Rahemi M, Davarpanah S, Yu M, Shabala L (2019) Comparing kinetics of xylem ion loading and its regulation in halophytes and glycophytes. Plant and Cell Physiology 61, 403–415.
| Comparing kinetics of xylem ion loading and its regulation in halophytes and glycophytes.Crossref | GoogleScholarGoogle Scholar |
