Elsevier

Chemosphere

Volume 198, May 2018, Pages 425-431
Chemosphere

Arsenic-induced nutrient uptake in As-hyperaccumulator Pteris vittata and their potential role to enhance plant growth

https://doi.org/10.1016/j.chemosphere.2018.01.077Get rights and content

Highlights

  • Studied As on growth and nutrient uptake of three Pteris ferns under sterile media.

  • As-hyperaccumulators (P. vittata and P. multifida) were included.

  • Non-hyperaccumulator (P. ensiformis) was used as control.

  • Arsenic, Fe and P increased hyperaccumulator biomass.

  • As-induced K and Zn uptake may help promote growth of hyperaccumulators.

Abstract

It is known that arsenic (As) promotes growth of As-hyperaccumulator Pteris vittata (PV), however, the associated mechanisms are unclear. Here we examined As-induced nutrient uptake in P. vittata and their potential role to enhance plant growth in sterile agar by excluding microbial effects. As-hyperaccumulator P. multifida (PM) and non-hyperaccumulator P. ensiformis (PE) belonging to the Pteris genus were used as comparisons. The results showed that, after 40 d of growth, As induced biomass increase in hyperaccumulators PV and PM by 5.2–9.4 fold whereas it caused 63% decline in PE. The data suggested that As played a beneficial role in promoting hyperaccumulator growth. In addition, hyperaccumulators PV and PM accumulated 7.5–13, 1.4–3.6, and 1.8–4.4 fold more As, Fe, and P than the non-hyperaccumulator PE. In addition, nutrient contents such as K and Zn were also increased while Ca, Mg, and Mn decreased or unaffected under As treatment. This study demonstrated that As promoted growth in hyperaccumulators and enhanced Fe, P, K, and Zn uptake. Different plant growth responses to As among hyperaccumulators PV and PM and non-hyperaccumulator PE may help to better understand why hyperaccumulators grow better under As-stress.

Introduction

Arsenic (As) is of environmental concern due to its toxicity and carcinogenicity (Mass et al., 2001). In soils, As is often present in its oxidized form arsenate (AsV), which is a chemical analogue for phosphate (P) (Meharg and Hartley–Whitaker, 2002). Pteris vittata (PV; Chinese Brake fern) is the first-known As-hyperaccumulator (Ma et al., 2001). It tolerates soil As concentrations up to 1500 mg kg−1 and accumulates up to 23 g kg−1 As in the fronds, making it useful in phytoremediation of As-contaminated soils (Tu et al., 2002, Kertulis-Tartar et al., 2006).

The success of phytoremediation depends on many factors including plant biomass, and soil As concentration and availability to plants (Fitz and Wenzel, 2002, Cattani et al., 2009). However, high biomass production of hyperaccumulators is a key factor (Shelmerdine et al., 2009). Similar to other hyperaccumulators, the yield of P. vittata at 1.03–1.3 t ha−1 yr−1 is lower than crop maize at 2.4–5.2 t ha−1 yr−1 (Kertulis-Tartar et al., 2006, Shelmerdine et al., 2009, Ray et al., 2013). Therefore, it is important to explore ways to increase plant biomass to improve its phytoremediation efficiency.

Our previous studies observed that As, Fe, and P promoted PV growth (Liu et al., 2015, Liu et al., 2016). It is understandable that Fe and P promote plant growth since they are essential elements, however, it is unclear how As promotes plant growth. Arsenic, a main ingredient of pesticide, is toxic to plants. Literature showed that As is positively correlated to K, Na, La, and Sm, but negatively correlated to Ca, suggesting that As affects element accumulation by PV (Wei et al., 2006, Wei and Zhang, 2007). Thus, it would be interesting to study the effects of toxicant As and nutrients Fe and P on plant growth of hyperaccumulator and non-hyperaccumulator plants.

In this study, besides P. vittata, hyperaccumulator P. multifida (PM) and non-hyperaccumulator P. ensiformis (PE) were included to examine the impacts of As, Fe, and P on plant growth in sterile system to exclude microbial effects. In addition, we emphasized the effects of As on nutrient uptake to better understand the mechanisms of As-induced plant growth in hyperaccumulators. The specific objectives were to: 1) compare the growth responses of three plants to As, Fe, and P; 2) examine the accumulation of As, Fe, and P; and 3) assess the influence of As on plant uptake of other nutrients (Ca, K, Mg, Mn, Zn, and Ni). Information obtained from the study helps to remove more As from contaminated sites by optimizing nutrient status to enhance plant growth.

Section snippets

Spore sterilization and gametophyte culture

Spores of three ferns were surface-sterilized by immersion in 10% sodium hypochlorite and 75% ethanol for 30 min, followed by several rinses in sterile DI water (Zhu et al., 2011, Lessl et al., 2013). Sterilized spores were grown in Petri dishes with Murashige and Skoog (MS) solid media. The MS media were autoclaved, containing (mg L−1): KNO3, 1900; NH4NO3, 1650; KH2PO4, 170; MgSO4·7H2O, 370; CaCl2·2H2O, 440; KI, 0.83; H3BO3, 6.2; MnSO4·4H2O, 22.3; ZnSO4·7H2O, 8.6; Na2MoO4·2H2O, 0.25; CuSO4·5H2

Effects of As, Fe, and P on plant growth

After growing in sterile media for 40 d, all three plants showed little toxicity symptom. Compared to the control, addition of As, Fe or P induced greater plant growth in hyperaccumulators (PV and PM), but As decreased plant growth in non-hyperaccumulator PE (Fig. 1; p < 0.05). In addition, hyperaccumulators PV and PM gained much more growth than PE in all treatments.

Among treatments, the best plant growth was observed in PV in Fe-treatment, 27.1 compared to 3.56 g plant−1 in the control (Fig. 1

Conclusions

Previous studies observed that As, Fe, and P enhanced growth of As-hyperaccumulator PV, however, the associated mechanisms are unclear. Therefore, in present study, a sterile system was introduced to investigate their effects on plant growth of two hyperaccumulators PV and PM and non-hyperaccumulator PE. The results showed that their growth responded differently to As, Fe, and P treatment. Hyperaccumulators PV and PM gained the largest biomass in Fe and P treatment (27.1 and 17.1 g plant−1),

Acknowledgements

This work was supported in part by the National Key Research and Development Program of China (Grant No. 2016YFD0800801), the State Key Program of National Natural Science Foundation of China (Grant No. 21637002) and the Jiangsu Provincial Innovation Fund and program B for Outstanding PhD candidate of Nanjing University (Grant No. 201602B052).

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