Does slow and steady win the race? Root growth dynamics of Arabidopsis halleri ecotypes in soils with varying trace metal element contamination

https://doi.org/10.1016/j.envexpbot.2019.103862Get rights and content

Highlights

  • Arabidopsis halleri plants adjust their root architecture in response to metal content in soil.

  • Two different development strategies were observed: dampened root growth in metalliferous and TME foraging in non-metalliferous soil.

  • Emplacing a thin capping layer of non-polluted substrate promotes root penetration of underlying polluted soil.

Abstract

Hyperaccumulating plants possess complex traits, allowing them to thrive in soils with high concentrations of trace metal elements (TME). Accordingly, their TME hypertolerance and hyperaccumulation capacities have been intensely studied from physiological, evolutionary, and ecological perspectives. Little is known, however, about their root system development in TME enriched vs natural soils. We assessed temporal and quantitative changes in root systems of the model species Arabidopsis halleri, using a novel combination of root phenotyping in rhizoboxes and multitemporal digital imaging. We continuously monitored root growth of two non-metallicolous and two metallicolous populations in different substrate treatments, including homogeneous and horizontal layer applications of metalliferous and non-metalliferous soils. Non-metallicolous plants on non-metalliferous soils produced deep-reaching and wide roots, whereas metallicolous plants on metalliferous soil had smaller roots. This pattern was reversed when transplanting seedlings to foreign substrates, indicating that environment rather than ecotype determines root growth in A. halleri. Dampened root development in metalliferous and favored root proliferation in non-metalliferous soils indicate cost of tolerance and TME foraging, respectively. Importantly, root propagation into metalliferous soil was strongly promoted by a non-metalliferous “capping” layer that facilitated initial plant development. Hence, growing on non-polluted substrate in the early stage provides plants with a robust and optimal root system that facilitates seedling establishment and subsequent development under TME enriched conditions. These findings improve our understanding of plant performance in metalliferous environments and can help refine management practices for the sustainable reclamation of degraded lands.

Introduction

Only a limited number of vascular plant species possess physiological properties that allow them to cope with very high concentrations of trace metal elements (TMEs) in metalliferous soils. Some of these “hypertolerant” species additionally allocate large amounts of TMEs to shoots without showing any toxicity symptoms (Reeves and Baker, 2000). The latter are called “hyperaccumulators” and are exceptional model organisms to study plant adaptation to extreme environments (Pollard et al., 2002). Their unique characteristics are also of practical importance in applications like phytoremediation, phytomining and biofortification of essential elements (Chaney et al., 2007; Clemens, 2017). Importantly, evidence is mounting that these rare and unusual plants are acutely threatened by habitat loss from mining, forestry development, improper phytoremediation practices, or urban expansion (Whiting et al., 2004; Baker et al., 2010; Jaffré et al., 2018; Reeves et al., 2018). Hence, the time is now to conduct detailed investigations of hyperaccumulator species, to further advance our knowledge on TME tolerance and hyperaccumulation, and to take advantage of these complex traits.

To date, most studies on TME tolerance in plants have focused on above-ground growth, whereas roots have received much less attention. This is mostly due to technical difficulties in assessing root growth in soil medium. However, the development of root systems is an important trait that should not be neglected. As the first plant organ that comes in contact with TMEs, roots are likely to manifest symptoms of metal toxicity (Bradshaw, 1952; Meyer et al., 2009; Babst-Kostecka et al., 2016). Their growth, morphology and physiology are governed by the plant genotype and modulated by soil properties. Ultimately, the abiotic stress experienced by the root system strongly affects plant growth and productivity (Werner et al., 2010; Downie et al., 2015). Better knowledge of plant responses to particular soil conditions is thus crucial for the selection of populations or genotypes that are pre-adapted to elevated TME concentrations. This knowledge can then help optimize plant performance in metalliferous environments and translate into urgently needed new strategies for sustainable phytoremediation.

Inhibition of root growth due to exposure to high TME concentrations has often been reported in non-hyperaccumulating species (e.g. Ivanov et al., 2003; El Kassis et al., 2007; Moradi et al., 2009; Lux et al., 2010; Gallego et al., 2012; Khare et al., 2017; Sofo et al., 2017). By contrast, the root system behavior in hyperaccumulators remains insufficiently studied. Some investigations of Nocceae caerulescens and Sedum alfredii reported preferential root proliferation into soil patches with high concentration of the target TME (Schwartz et al., 1999; Whiting et al., 2000a; Haines, 2002; Dechamps et al., 2008; Liu et al., 2010), whereas other hyperaccumulators did not exhibit such a pattern (e.g. Berkheya coddii; Moradi et al., 2009). To date, little information is available on the root system architecture and development of one of the most prominent plant model species for the study of TME hypertolerance and hyperaccumulation – Arabidopsis halleri. Arabidopsis halleri (Brassicaceae) hypertolerates and hyperaccumulates zinc (Zn) and cadmium (Cd). It also tolerates high concentrations of lead (Pb) and uranium in the soil, but does not hyperaccumulate the latter two elements (Bert et al., 2002; Viehweger and Geipel, 2010). Importantly, A. halleri represents a group of species called pseudometallophytes, which include both metallicolous populations on metalliferous (M) soils, and non-metallicolous populations on non-metalliferous (NM) soils. Accordingly, species-wide quantitative variation in TME hyperaccumulation and hypertolerance have been frequently reported (Macnair, 2002; Pauwels et al., 2006; Meyer et al., 2010; Frérot et al., 2017; Stein et al., 2017; Babst‐Kostecka et al., 2018) and the unique traits of A. halleri could be explored to improve the phytoremediation of post-mining sites. Yet, possibilities to do so are currently hampered by a lack of information on the capacity of A. halleri root systems to penetrate and exploit contaminated soils with different TME concentrations.

In this greenhouse study, we employed a non-invasive root phenotyping approach based on rhizoboxes to assess the root development of A. halleri in response to TMEs. In contrast to the majority of previously used TME tolerance tests that involved artificial hydroponic environments or agar-solidified media, we characterized root systems that developed in actual soil. Furthermore, this approach enabled the visualization of root growth throughout the experiment, which is not possible when plants are cultivated e.g. in pots. In a novel approach, we combined our phenotyping with digital imaging and image analysis to assess and quantify changes in the root system. This combination allowed us to not only record the size and shape of A. halleri root systems at specific points in time, but to continuously monitor root growth dynamics and speed. Based on this setup, we addressed the following questions: (1) Do root system morphology and architecture differ between non-metallicolous and metallicolous A. halleri when plants grow in their corresponding (hereafter called “native”) soils? (2) Do non-metallicolous and metallicolous populations of A. halleri perform better in soil with TME excess or in uncontaminated soil? (3) Does the emplacement of an NM soil layer over M soil (“capping”) have an effect on root propagation into the M soil beneath?

Section snippets

Plant material and chemical analyses of soil

The sampling included two non-metalliferous (NM_PL14 and NM_PL35) and two metalliferous (M_PL22 and M_PL27) locations of A. halleri in southern Poland (Fig. 1; see Meyer et al., 2010 for site descriptions). The NM_PL14 site is located at low elevation in Niepołomice Forest, where the observed total soil Zn, Pb and Cd levels were 169 ± 20 mg kg−1, 28 ± 3 mg kg−1, 0.5 ± 0.1 mg kg−1, respectively (Babst‐Kostecka et al., 2018). The NM_PL35 is a sub-alpine location in the foothills of the Tatra Mts,

Population effects

Differences between populations within the two ecotypes were negligible in both NM and M substrate (Supplementary Table S2). The only exception was found in the trait root lengthbottom, which in NM substrate was significantly higher for NM_PL14 than NM_PL35 (non-metallicolous populations) and significantly higher for M_PL27 than M_PL22 (metallicolous populations). Due to this lack of population-specificity in 8 out of 9 parameters in NM substrate and 9 out of 9 parameters in M substrate,

Discussion

This study investigated the root architecture of metallicolous and non-metallicolous populations of A. halleri in response to M and NM soil. Overall, we observed pronounced differences between A. halleri ecotypes when grown in their native soils: non-metallicolous plants on NM soil developed deep-reaching and wide root systems; metallicolous plants on M soil developed shorter and narrower root systems. Importantly, these trends were reversed when seedlings were transplanted to foreign

Author contributions

CD and ABK planned and designed the research. ABK and KB performed the experiment. CD, CB and UK processed the root images. KN planned and designed the phenotyping platform GROWSCREEN Rhizo. CD analysed the data. CD and ABK led the writing of the manuscript. All authors contributed critically to the drafts and gave final approval for publication.

Acknowledgements

We thank M. Tatrzańska-Matuła, B. Pawłowska, A. Pitek, N. Porada, B. Łopata, G. Szarek-Łukaszewska, for collecting seeds, and F. Babst for editorial comments. This research was supported by the POWROTY/REINTEGRATION programme of the Foundation for Polish Science cofinanced by the European Union under the European Regional Development Fund (POIR.04.04.00-00-1D79/16-00), and statutory fund from the W. Szafer Institute of Botany PAS.

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