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Australian Journal of Botany Australian Journal of Botany Society
Southern hemisphere botanical ecosystems
RESEARCH ARTICLE (Open Access)

Foliar elemental microprobe data and leaf anatomical traits consistent with drought tolerance in Eucalyptus largiflorens (Myrtaceae)

Denise R. Fernando https://orcid.org/0000-0002-0565-0534 A C , Jonathan P. Lynch B , Meredith T. Hanlon B and Alan T. Marshall A
+ Author Affiliations
- Author Affiliations

A Department of Ecology, Environment and Evolution, La Trobe University, Bundoora, Vic. 3086, Australia.

B Department of Plant Science, The Pennsylvania State University, University Park, PA 16802, USA.

C Corresponding author. Email: d.fernando@latrobe.edu.au

Australian Journal of Botany 69(4) 215-224 https://doi.org/10.1071/BT20170
Submitted: 22 December 2020  Accepted: 3 May 2021   Published: 3 June 2021

Journal Compilation © CSIRO 2021 Open Access CC BY

Abstract

In food-productive river basins, ecosystems reliant on natural flows are affected by climate change and water removal. One such example is Australia’s Murray–Darling Basin (MDB), to which the ecologically important black box tree Eucalyptus largiflorens (Myrtaceae) is unique. Little is known about its mineral nutrition and response to flooding. A field study conducted at Hattah Kulkyne National Park on the MDB examined nutrient and Al distribution in mature and young foliage of trees whose status varied with respect to the presence of surface floodwaters. Black box is also of interest due to emerging evidence of its capacity to accumulate high foliar salt concentrations. Here, cryo scanning electron microscopy alone (SEM), combined with energy dispersive spectroscopy (SEM-EDS) and X-ray fluorescence (XRF) spectroscopy were applied to evaluate leaf anatomy and elemental patterns at the cellular and whole-leaf levels. Variation in whole-leaf elemental levels across flooded and dry trees aligned with known nutritional fluctuations in this drought-tolerant species reliant on occasional infrequent flooding. The microprobe data provide evidence of drought tolerance by demonstrating that extended conditions of lack of water to trees do not elicit leaf anatomical changes nor changes to leaf cellular storage of these elements. Foliar Na concentrations of ~2000–6000 mg kg–1 DW were found co-localised with Cl in mesophyll and dermal cells of young and mature leaves, suggesting vacuolar salt disposal as a detoxification strategy.

Keywords: Eucalyptus largiflorens, black box tree, eucalypt, flooding, watercourses, salinity, Murray–Darling Basin, drought tolerance, foliar microprobe data, riverine ecosystems, river basin system.


References

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

Blamey FP, Hernandez-Soriano MC, Cheng M, Tang C, Paterson DJ, Lombi E, Wang WH, Scheckel KG, Kopittke PM (2015) Synchrotron-based techniques shed light on mechanisms of plant sensitivity and tolerance to high manganese in the root environment. Plant Physiology 169, 2006–2020.
Synchrotron-based techniques shed light on mechanisms of plant sensitivity and tolerance to high manganese in the root environment.Crossref | GoogleScholarGoogle Scholar | 26395840PubMed |

Bramley H, Hutson J, Tyerman SD (2003) Floodwater infiltration through root channels on a sodic clay floodplain and the influence on a local tree species Eucalyptus largiflorens. Plant and Soil 253, 275–286.
Floodwater infiltration through root channels on a sodic clay floodplain and the influence on a local tree species Eucalyptus largiflorens.Crossref | GoogleScholarGoogle Scholar |

Brooks RR (1998) ‘Plants that Hyperaccumulate Heavy Metals.’ (CAB International: Oxon, UK)

Capon S, James CS, George AK (2016) Riverine trees and shrubs. In ‘Vegetation of Australian Riverine Landscapes: Biology, Ecology and Management’. (Eds CJS Capon, M Reid) pp. 119–142. (CSIRO Publishing: Melbourne, Vic., Australia)

Cunningham S, MacNally R, Griffioen P, White M (2009) Mapping the condition of river red gum and black box stands in The Living Murray icon sites. MDBA. Report book number 51/10, Murray–Darling Basin Authority, Canberra, ACT, Australia.

Doody TM, Colloff MJ, Davies M, Koul V, Benyon RG, Nagler PL (2015) Quantifying water requirements of riparian river red gum (Eucalyptus camaldulensis) in the Murray–Darling Basin, Australia – implications for the management of environmental flows. Ecohydrology 8, 1471–1487.
Quantifying water requirements of riparian river red gum (Eucalyptus camaldulensis) in the Murray–Darling Basin, Australia – implications for the management of environmental flows.Crossref | GoogleScholarGoogle Scholar |

Eltahir AS, Elkamali HH, Abdallah SA, Hamad SF (2018) Comparative study of anatomy of Eucalyptus Microtheca and Eucalyptus camaldulensis leaves. Journal of Faculty of Sciences 5, 84–94.

Esau K (1965) ‘Plant Anatomy.’ (Wiley: New York, NY, USA)

Evans JR, Vogelmann TC (2006) Photosynthesis within isobilateral Eucalyptus pauciflora leaves. New Phytologist 171, 771–782.
Photosynthesis within isobilateral Eucalyptus pauciflora leaves.Crossref | GoogleScholarGoogle Scholar |

Fernando DR, Marshall A, Baker AJM, Mizuno T (2013) Microbeam methodologies as powerful tools in manganese hyperaccumulation research: present status and future directions. Frontiers in Plant Science 4, 319
Microbeam methodologies as powerful tools in manganese hyperaccumulation research: present status and future directions.Crossref | GoogleScholarGoogle Scholar | 23970891PubMed |

Fernando DR, Moroni SJ, Scott BJ, Conyers MK, Lynch JP, Marshall AT (2016a) Temperature and light drive manganese accumulation and stress in crops across three major plant families. Environmental and Experimental Botany 132, 66–79.
Temperature and light drive manganese accumulation and stress in crops across three major plant families.Crossref | GoogleScholarGoogle Scholar |

Fernando DR, Marshall AT, Lynch JP (2016b) Foliar nutrient distribution patterns in sympatric maple species reflect contrasting sensitivity to excess manganese. PLoS One 11, e0157702
Foliar nutrient distribution patterns in sympatric maple species reflect contrasting sensitivity to excess manganese.Crossref | GoogleScholarGoogle Scholar | 27391424PubMed |

Fernando DR, Lynch JP, Reichman S, Clark G, Miller R, Doody T (2018a) Inundation of a floodplain lake woodlands system: nutritional profiling and benefit to mature Eucalyptus largiflorens (Black Box) trees. Wetlands Ecology and Management 26, 961–975.
Inundation of a floodplain lake woodlands system: nutritional profiling and benefit to mature Eucalyptus largiflorens (Black Box) trees.Crossref | GoogleScholarGoogle Scholar |

Fernando DR, Marshall AT, Green PT (2018b) Cellular ion interactions in two endemic tropical rainforest species of a novel metallophytic tree genus. Tree Physiology 38, 119–128.
Cellular ion interactions in two endemic tropical rainforest species of a novel metallophytic tree genus.Crossref | GoogleScholarGoogle Scholar | 28981909PubMed |

Fernando DR, Fernando AE, Koerber GR, Doody TM (2021) Tree-soil interactions through water release to a floodplain ecosystem: a case study of Black Box (Eucalyptus largiflorens) on loamy sands. Wetlands
Tree-soil interactions through water release to a floodplain ecosystem: a case study of Black Box (Eucalyptus largiflorens) on loamy sands.Crossref | GoogleScholarGoogle Scholar |

Gallardo A (2003) Effect of tree canopy on the spatial distribution of soil nutrients in a Mediterranean Dehesa. Pedobiologia 47, 117–125.
Effect of tree canopy on the spatial distribution of soil nutrients in a Mediterranean Dehesa.Crossref | GoogleScholarGoogle Scholar |

Grafton RQ, Williams J, Perry CJ, Molle F, Ringler C, Steduto P, Udall B, Wheeler SA, Wang Y, Garrick D, Allen RG (2018) The paradox of irrigation efficiency: higher efficiency rarely reduces water consumption. Science 361, 748–750.
The paradox of irrigation efficiency: higher efficiency rarely reduces water consumption.Crossref | GoogleScholarGoogle Scholar | 30139857PubMed |

Grove TS, Malajczuk N (1985) Nutrient accumulation by trees and understorey shrubs in an age-series of Eucalyptus diversicolor F.Muell. stands. Forest Ecology and Management 11, 75–95.
Nutrient accumulation by trees and understorey shrubs in an age-series of Eucalyptus diversicolor F.Muell. stands.Crossref | GoogleScholarGoogle Scholar |

He M, Dijkstra FA (2014) Drought effect on plant nitrogen and phosphorus: a meta analysis. New Phytologist 204, 924–931.
Drought effect on plant nitrogen and phosphorus: a meta analysis.Crossref | GoogleScholarGoogle Scholar |

Huang CX, Steveninck RFMV (1988) Effect of moderate salinity on patterns of potassium, sodium and chloride accumulation in cells near the root tip of barley: Role of differentiating metaxylem vessels. Physiologia Plantarum 73, 525–533.
Effect of moderate salinity on patterns of potassium, sodium and chloride accumulation in cells near the root tip of barley: Role of differentiating metaxylem vessels.Crossref | GoogleScholarGoogle Scholar |

Hulme K, Hill S (2005) Mineralisation discovery through transported cover using River Redgums (Eucalyptus camaldulensis). In ‘Minerals Exploration Seminar’, 25 May 2005, Perth, WA, Australia. (Ed. RAD Gee) pp. 31–33. (CRC LEME: Perth, WA, Australia) Available at http://crcleme.org.au/NewsEvents/Events/Minex%20Seminar%20May%2005/Abstract_Volume_Minex%20May05.pdf

IPCC (2014) ‘IPCC, 2014: Summary for Policymakers.’ (Cambridge University Press: Cambridge, UK, and New York, NY, USA)

James SA, Bell DT (1995) Morphology and anatomy of leaves of Eucalyptus camaldulensis clones: variation between geographically separated locations. Australian Journal of Botany 43, 415–433.
Morphology and anatomy of leaves of Eucalyptus camaldulensis clones: variation between geographically separated locations.Crossref | GoogleScholarGoogle Scholar |

James SA, Bell DT (2000) Leaf orientation, light interception and stomatal conductance of Eucalyptus globulus ssp. globulus leaves. Tree Physiology 20, 815–823.
Leaf orientation, light interception and stomatal conductance of Eucalyptus globulus ssp. globulus leaves.Crossref | GoogleScholarGoogle Scholar | 12651502PubMed |

James SA, Bell DT (2001) Leaf morphological and anatomical characteristics of heteroblastic Eucalyptus globulus ssp. globulus (Myrtaceae). Australian Journal of Botany 49, 259–269.
Leaf morphological and anatomical characteristics of heteroblastic Eucalyptus globulus ssp. globulus (Myrtaceae).Crossref | GoogleScholarGoogle Scholar |

Jensen AE, Walker KF, Paton DC (2008) The role of seedbanks in restoration of floodplain woodlands. River Research and Applications 24, 632–649.
The role of seedbanks in restoration of floodplain woodlands.Crossref | GoogleScholarGoogle Scholar |

Johns C, Reid CJ, Roberts J, Sims N, Doody T, Overton I, McGinness HM, Rogers K, Campbell C, Gawne B (2009) Native trees of the River Murray floodplain: literature review and experimental designs to examine effects of flow enhancement and floodwater retention. Final report for the MDBA, Murray–Darling Freshwater Research Centre, Wodonga, Vic., Australia.

Judd TS, Attiwill PM, Adams MA (1996) Nutrient concentrations in Eucalyptus: a synthesis in relation to differences between taxa, sites and components. In ‘Nutrition of Eucalypts’. (Eds PM Attiwill, MA Adams) pp. 123–153. (CSIRO Publishing: Melbourne, Vic., Australia)

Leigh RA, Jones RG (1984) A hypothesis relating critical potassium concentrations for growth to the distribution and functions of this ion in the plant cell. New Phytologist 97, 1–13.
A hypothesis relating critical potassium concentrations for growth to the distribution and functions of this ion in the plant cell.Crossref | GoogleScholarGoogle Scholar |

Lugo AE, Cuevas E, Sanchez MJ (1990) Nutrients and mass in litter and top soil of ten tropical tree plantations. Plant and Soil 125, 263–280.
Nutrients and mass in litter and top soil of ten tropical tree plantations.Crossref | GoogleScholarGoogle Scholar |

Lynch JP, St Clair SB (2004) Mineral stress: the missing link in understanding how global climate change will affect plants in real world soils. Field Crops Research 90, 101–115.
Mineral stress: the missing link in understanding how global climate change will affect plants in real world soils.Crossref | GoogleScholarGoogle Scholar |

Marschner H (2002) ‘Mineral Nutrition of Higher Plants.’ (Academic Press: London, UK)

Marshall AT (2017) Quantitative X-ray microanalysis of model biological samples in the SEM using remote standards and the XPP analytical model. Journal of Microscopy 266, 231–238.
Quantitative X-ray microanalysis of model biological samples in the SEM using remote standards and the XPP analytical model.Crossref | GoogleScholarGoogle Scholar | 28181671PubMed |

McEvoy PK (1992) Ecophysiological comparisons between Eucalyptus camaldulensis Denh., E. largiflorens F.Muell. and E. microcarpa (Maiden) Maiden on the River Murray Floodplain. University of Melbourne, Melbourne, Vic., Australia.

McLean EH, Prober SM, Stock WD, Steane DA, Potts BW, Vaillancourt RE, Byrne M (2014) Plasticity of functional traits varies clinally along a rainfall gradient in Eucalyptus tricarpa. Plant, Cell & Environment 37, 1440–1451.
Plasticity of functional traits varies clinally along a rainfall gradient in Eucalyptus tricarpa.Crossref | GoogleScholarGoogle Scholar |

Migacz IP, Raeski PA, Almeida VP, Raman V, Nisgoski S, Muniz GI, Farago PV, Khan IA, Budel JM (2018) Comparative leaf morpho-anatomy of six species of Eucalyptus cultivated in Brazil. Brazillian Journal of Pharmacognosy 28, 273–281.
Comparative leaf morpho-anatomy of six species of Eucalyptus cultivated in Brazil.Crossref | GoogleScholarGoogle Scholar |

Millikan CR (1951) Radio-autographs of manganese in plants. Australian Journal of Biological Sciences 4, 28–41.
Radio-autographs of manganese in plants.Crossref | GoogleScholarGoogle Scholar |

Moxham C, Duncan M, Moloney P (2018) Tree health and regeneration response of Black Box (Eucalyptus largiflorens) to recent flooding. Ecological Management & Restoration 19, 58–65.
Tree health and regeneration response of Black Box (Eucalyptus largiflorens) to recent flooding.Crossref | GoogleScholarGoogle Scholar |

Munns R, Gilliham M (2015) Salinity tolerance of crops – what is the cost? New Phytologist 208, 668–673.
Salinity tolerance of crops – what is the cost?Crossref | GoogleScholarGoogle Scholar |

NPWS (2002) Biodiversity survey. Technical report, Dubbo, NSW, Australia.

O’Malley C, Sheldon F (1990) ‘Chowilla Floodplain Biological Study.’ (Nature Conservation Society of South Australia: Adelaide, SA, Australia)

Oi T, Hirunagi K, Taniguchi M, Miyake H (2013) Salt excretion from the salt glands in Rhodes grass (Chloris gayana Kunth) as evidenced by low-vacuum scanning electron microscopy. Flora 208, 52–57.
Salt excretion from the salt glands in Rhodes grass (Chloris gayana Kunth) as evidenced by low-vacuum scanning electron microscopy.Crossref | GoogleScholarGoogle Scholar |

Pittock J, Finlayson CM (2011) Australia’s Murray–Darling Basin: freshwater ecosystem conservation options in an era of climate change. Marine and Freshwater Research 62, 232–243.
Australia’s Murray–Darling Basin: freshwater ecosystem conservation options in an era of climate change.Crossref | GoogleScholarGoogle Scholar |

Poff NL, Allen JD, Palmer MA, Hart DD, Richter BD, Arthrington AH, Rogers KH, Meyer JL, Stanford JA (2003) River flows and water wars: emerging science for environmental decision making. Frontiers in Ecology and the Environment 1, 298–306.
River flows and water wars: emerging science for environmental decision making.Crossref | GoogleScholarGoogle Scholar |

Pouchou JL, Pichoir F (1991) Quantitative analysis of homogeneous or stratified microvolumes applying the model ‘PAP’. In ‘Electron Probe Quantitation’. (Eds KFJ Heinrich, DE Newbury) pp. 31–75. (Plenum Press: New York, NY, USA)

Pouchou JL, Pichoir F (1992) Advanced quantitative procedures for analytical SEM and EPMA: X-ray microanalysis of light elements and layered specimens. In ‘Electron Microscopy, EUREM 92’, 7–11 September 1992, Granada, Spain. Vol. 1, pp. 293–297. (European Congress on Electron Microscopy: Granada, Spain)

Roberts J, Marston F (2011) ‘Water Regime of Wetland & Floodplain Plants in the Murray–Darling Basin.’ (National Water Commission: Canberra, ACT, Australia)

Rodrigues ES, Gomes MHF, Duran NM, Cassanji JGB, daCruz TNM, Neto ASA, Savassa SM, DeAlmeida E, Carvalho HWP (2018) Laboratory microprobe X-ray fluorescence in plant science: emerging applications and case studies. Frontiers in Plant Science 9, 1588
Laboratory microprobe X-ray fluorescence in plant science: emerging applications and case studies.Crossref | GoogleScholarGoogle Scholar | 30487802PubMed |

Smith P, Smith J (2014) Floodplain vegetation of the River Murray in 1987–1988: an important pre-drought benchmark for subsequent studies. Cunninghamia 14, 97–151.
Floodplain vegetation of the River Murray in 1987–1988: an important pre-drought benchmark for subsequent studies.Crossref | GoogleScholarGoogle Scholar |

Taiz L, Zeiger E (2002) ‘Plant Physiology’, 3rd edn. (Sinauer Associates Inc.: Sunderland, MA, USA)

Van Steveninck RFM, Fernando DR, Anderson CA, Edwards LB, Van Steveninck ME (1988) Chloride and sulphur concentrations in chloroplasts of spinach. Physiologia Plantarum 74, 651–658.
Chloride and sulphur concentrations in chloroplasts of spinach.Crossref | GoogleScholarGoogle Scholar |

Wassens S, Car C, Jansen A (2005) ‘Murrumbidgee Irrigation Area Invertebrate Biodiversity Benchmark.’ (Murrumbidgee Irrigation Ltd: Griffith, NSW, Australia)

White RE (1997) ‘Principles and Practices of Soil Science – the Soil as a Natural Resource.’ (Blackwell Science: Melbourne, Vic., Australia)