Habitat-specific allocations of elements in Atriplex lentiformis seeds indicate adaptation to metal toxicity

Author:

Murawska-Wlodarczyk Kamila1ORCID,van der Ent Antony234ORCID,Wlodarczyk Tomasz1ORCID,Słomka Aneta5ORCID,Paterson David J6ORCID,Brueckner Dennis7ORCID,Przybyłowicz Wojciech J89ORCID,Mesjasz-Przybyłowicz Jolanta9ORCID,Ryan Chris C10ORCID,Maier Raina M1ORCID,Babst-Kostecka Alicja1ORCID

Affiliation:

1. Department of Environmental Science, The University of Arizona , Tucson, AZ , USA

2. Laboratory of Genetics, Wageningen University and Research , Wageningen , The Netherlands

3. Centre for Mined Land Rehabilitation, Sustainable Minerals Institute, The University of Queensland , St Lucia, Queensland , Australia

4. Laboratoire Sols et Environnement, INRAE, Université de Lorraine , Nancy , France

5. Department of Plant Cytology and Embryology, Institute of Botany, Faculty of Biology, Jagiellonian University , Krakow , Poland

6. Australian Synchrotron, ANSTO , Clayton, Victoria , Australia

7. Deutsches Elektronen-Synchrotron DESY , 22607 Hamburg , Germany

8. AGH University of Science and Technology, Faculty of Physics & Applied Computer Science , Krakow , Poland

9. Department of Botany and Zoology, Stellenbosch University , Stellenbosch , South Africa

10. CSIRO, Mineral Resources , Clayton, Victoria , Australia

Abstract

Abstract Self-sustaining vegetation in metal-contaminated areas is essential for rebuilding ecological resilience and community stability in degraded lands. Metal-tolerant plants originating from contaminated post-mining areas may hold the key to successful plant establishment and growth. Yet, little is known about the impact of metal toxicity on reproductive strategies, metal accumulation, and allocation patterns at the seed stage. Our research focused on the metal tolerant Atriplex lentiformis. Specifically, we examined the effects of toxic metal(loid) concentration in soils on variability in its reproductive strategies, including germination patterns, elemental uptake, and allocation within the seeds. We employed advanced imaging techniques like synchrotron X-ray fluorescence microscopy (2D scans and 3D tomograms) combined with inductively coupled plasma mass spectrometry to reveal significant differences in metal(loid) concentration and distribution within the seed structures of A. lentiformis from contrasting habitats. Exclusive Zn hotspots of high concentrations were found in the seeds of the metallicolous accession, primarily in the sensitive tissues of shoot apical meristems and root zones of the seed embryos. Our findings offer novel insights into phenotypic variability and metal tolerance and accumulation in plants from extreme environments. This knowledge can be applied to enhance plant survival and performance in land restoration efforts.

Funder

University of Arizona Center for Environmentally Sustainable Mining Industry-Academic Revegetation Research Cooperative

National Institute of Environmental and Health Sciences Superfund Research Program

Publisher

Oxford University Press (OUP)

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