Paspalum urvillei and Setaria parviflora, two grasses naturally adapted to extreme iron-rich environments Talita Oliveira de Araujo, Marie-Pierre Isaure, Ghaya Alchoubassi, Katarzyna Bierla, Joanna Szpunar, Nicolas Trcera, Sandrine Chay, Carine Alcon, Luzimar Campos da Silva, Catherine Curie, et al. To cite this version: Talita Oliveira de Araujo, Marie-Pierre Isaure, Ghaya Alchoubassi, Katarzyna Bierla, Joanna Szpunar, et al.. Paspalum urvillei and Setaria parviflora, two grasses naturally adapted to ex- treme iron-rich environments. Plant Physiology and Biochemistry, Elsevier, 2020, 151, pp.144-156. 10.1016/j.plaphy.2020.03.014. hal-02518238 HAL Id: hal-02518238 https://hal.inrae.fr/hal-02518238 Submitted on 25 Aug 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Plant Physiology and Biochemistry 151 (2020) 144–156 Contents lists available at ScienceDirect Plant Physiology and Biochemistry journal homepage: www.elsevier.com/locate/plaphy Research article Paspalum urvillei and Setaria parviflora, two grasses naturally adapted to extreme iron-rich environments T Talita Oliveira de Araujoa,d, Marie-Pierre Isaureb, Ghaya Alchoubassib, Katarzyna Bierlab, Joanna Szpunarb, Nicolas Trcerac, Sandrine Chayd, Carine Alcond, Luzimar Campos da Silvaa, ∗ Catherine Curied, Stephane Marid, a Universidade Federal de Viçosa, Laboratório de Anatomia Vegetal, Viçosa, 36570-900, Brazil b Universite de Pau et des Pays de l'Adour, E2S UPPA, CNRS, IPREM UMR 5254, Hélioparc, 64053 Pau, France c Synchrotron SOLEIL, l’Orme des Merisiers Saint Aubin BP48, 91192, Gif-sur-Yvette Cedex, France d BPMP, Univ Montpellier, CNRS, INRAE, Institut Agro, Montpellier, France ARTICLE INFO ABSTRACT Keywords: Paspalum urvillei and Setaria parviflora are two plant species naturally adapted to iron-rich environments such as Paspalum urvillei around iron mines wastes. The aim of our work was to characterize how these two species cope with these Setaria parviflora extreme conditions by comparing them with related model species, Oryza sativa and Setaria viridis, that appeared Setaria viridis to be much less tolerant to Fe excess. Both Paspalum urvillei and Setaria parviflora were able to limit the amount of Oryza sativa Fe accumulated within roots and shoots, compared to the less tolerant species. Perls/DAB staining of Fe in root Perls-DAB method cross sections indicated that Paspalum urvillei and Setaria parviflora responded through the build-up of the iron μXRF μ μXANES plaque (IP), suggesting a role of this structure in the limitation of Fe uptake. Synchrotron XRF analyses showed Iron plaque the presence of phosphorus, calcium, silicon and sulfur on IP of Paspalum urvillei roots and μXANES analyses Vacuole identified Fe oxyhydroxide (ferrihydrite) as the main Fe form. Once within roots, high concentrations of Fe were Chloroplast localized in the cell walls and vacuoles of Paspalum urvillei, Setaria parviflora and O. sativa whereas Setaria viridis Ferritin accumulated Fe in ferritins. The Fe forms translocated to the shoots of Setaria parviflora were identified as tri-iron Citrate complexes with citrate and malate. In leaves, all species accumulated Fe in the vacuoles of bundle sheath cells Malate and as ferritin complexes in plastids. Taken together, our results strongly suggest that Paspalum urvillei and Setaria parviflora set up mechanisms of Fe exclusion in roots and shoots to limit the toxicity induced by Fe excess. 1. Introduction Cd, As, Cu, Co, Mn, Pb, Se, Tl and rare earth elements (REE) has been reported (van der Ent et al., 2013; Reeves et al., 2018). Iron hyper- Iron (Fe) is an essential micronutrient that is absorbed by roots of accumulation has been much less reported, probably because Fe has a grasses as Fe3+-phytosiderophores complexes and follows the tran- low bioavailability caused by the low solubility of iron oxyhydroxides spiration stream to the shoot along with other nutrients and minerals in natural environments and instead, acts as a limiting factor for plant (Nozoye et al., 2011). Despite being required in chloroplasts and mi- growth. Therefore the identification of true Fe hyperaccumulators is tochondria to be used as an enzymatic cofactor in a wide range of less clearly established than for other trace elements. Nevertheless, metabolic processes (Balk and Schaedler, 2014), when in excess, ferrous there are some studies reporting Fe tolerance and hyperaccumulation in ions can promote the generation of reactive oxygen species and oxi- Imperata cylindrica (grass family, Poacae) from the acidic mining area of dative stress (Dinakar et al., 2010). Nevertheless, some species are the Tinto River banks in the Iberian Pyritic Belt in Spain (Rodriguez naturally adapted to tolerate extremely high concentrations of metals in et al., 2005; de la Fuente et al., 2017). Contrary to hyperaccumulators, their environment, using two distinct strategies: some species will avoid true “excluder” plants have received much less attention (Bothe and the built up of metals in the organs, particularly in leaves, they are Slomka, 2017). termed “excluders” whereas other species will promote the storage of To deal with Fe excess, plants employ mechanisms such as induction metals in above-ground organs, these plants are known as “hyper- of antioxidant system (Stein et al., 2014), reorganization of the pho- accumulators” (van der Ent et al., 2013). Hyperaccumulation of Ni, Zn, tosynthetic apparatus (Pereira et al., 2014; Muller et al., 2015) and ∗ Corresponding author. E-mail address: [email protected] (S. Mari). https://doi.org/10.1016/j.plaphy.2020.03.014 Received 20 November 2019; Received in revised form 17 February 2020; Accepted 12 March 2020 Available online 18 March 2020 0981-9428/ © 2020 The Authors. Published by Elsevier Masson SAS. This is an open access article under the CC BY license (http://creativecommons.org/licenses/BY/4.0/). T. Oliveira de Araujo, et al. Plant Physiology and Biochemistry 151 (2020) 144–156 detoxification and/or sequestration in sites where Fe will not cause et al., 2012). Citrate was identified as the main Fe ligand in xylem sap damage to cell, i.e. vacuoles and apoplastic space (Briat et al., 2010a; of tomato plants (Rellan-Alvarez et al., 2010). Besides citrate, some Zhang et al., 2012). The presence of an iron plaque (IP) can be con- studies have indicated malate and nicotianamine as organic molecules, sidered as a mechanism of resistance, since it is due to Fe precipitation which form a complex with iron (Takahashi et al., 2003; Grillet et al., on the root surface, avoiding the over-accumulation of iron in leaf tis- 2014). Nothing is known about the long-distance Fe transport in Fe sues (Green and Etherington, 1977). The IP formation occurs in roots of hyperaccumulator and hypertolerant plants, and therefore the identi- wetland plant where Fe is spontaneously precipitated due to oxidizing fication, speciation and quantification of Fe transport forms in xylem microenvironments normally created around roots of aquatic plants (Xu sap are crucial to understand this long-distance transport. This knowl- et al., 2009). Thus, Fe2+ is oxidized into Fe3+, which precipitates on edge is the basis to understand how the metal is transported across the root surface, thereby creating a smooth regular reddish precipitate membranes and delivered to its final target. or irregular plaque coating on root surfaces (Pereira et al., 2014; The perennial grasses Paspalum urvillei Steudel and Setaria parvi- Tripathi et al., 2014). flora, native species from South America, were identified among the few The adsorption of trace metals and nutrients is the most important species able to grow spontaneously at the margins of decantation ponds characteristic of IP. A significant amount of metals bind to IP through of an Fe ore pelletizing industry located in Brazil, in the Ubu district the formation of complexes thanks to the high affinity of Fe hydroxide (municipality of Anchieta, state of Espìrito Santo, South-Eastern Brazil) for different metals (Batty et al., 2000; Liu et al., 2011). Extensive ef- (de Araujo et al., 2014). These ponds are supplied with water from the forts to understand the role of IP in metal sequestration and translo- mining system and plumbing of the iron ore pelletizing industry, cation have yielded contrasting results. Some authors agree that IP acts therefore creating an environment rich in iron particles. Paspalum ur- as a resistance barrier for metal(loids) translocation, and this barrier villei and Setaria parviflora were further described as highly tolerant to can function by either acting as an adsorbent of toxic elements or by Fe excess (de Araujo et al., 2014; Santana et al., 2014) and the for- simply being a physical obstacle (Pi et al., 2011; Huang et al., 2012). As mation of IP was observed around the roots (de Araujo et al., 2015). an illustration, iron plaques have been demonstrated to sequester ar- In this study, by combining Perls/DAB histochemistry, μXRF, senic in the wetland plants Typha latifolia (Hansel et al., 2002; Blute μXANES and chromatography coupled to mass spectrometry, we shed et al., 2004), Phragmites australis (Pardo et al., 2016), Phalaris ar- some light on the responses of Paspalum urvillei and Setaria parviflora to undinacea (Hansel et al., 2002), and rice Oryza sativa L (Liu et al., 2006). excess Fe and uncover new cellular Fe accumulation sites in response to Other metals such as Cu, Mn, Pb and Zn were also detected in IP from excess. Spartina alterniflora (Feng et al., 2015; Xu et al., 2018) and Phalaris arundinacea (Hansel et al., 2001). 2. Materials and methods Alternatively, IP may act as a buffer and reservoir in nutrient up- take, particularly during the time of diminished supply of nutrients (Hu 2.1.