Xylem development, cadmium bioconcentration, and antioxidant defense in Populus × euramericana stems under combined conditions of nitrogen and cadmium

https://doi.org/10.1016/j.envexpbot.2019.04.014Get rights and content

Highlights

  • Xylem development was suppressed by combination of N deficiency and Cd exposure.

  • Phytohormones and antioxidants decreased due to poor N nutritional status in stem.

  • Adequate N application promoted antioxidant defense and Cd tolerance in stems.

  • The suppression on xylem development was partially alleviated by N application.

  • N icnreased stem Cd accumulation via promoting Cd tolerance and xylem development.

Abstract

Populus species feature remarkable phytoremediation of cadmium (Cd) contamination. The influence of nitrogen (N) availability on Cd accumulation and tolerance in stems was investigated in a clone of Populus × euramericana. Secondary xylem development in stems was dramatically suppressed by the combined conditions of N deficiency and Cd exposure, but such suppression was partially alleviated by N application. Under adequate N condition, the Cd bioconcentration factor (BCF) in stems at moderate and high Cd exposures reached 3.07 and 0.91, respectively, whereas the Cd content in stems at high Cd exposure reached 164 μg Cd plant−1. However, Cd bioconcentration and accumulation in stems were sharply decreased due to N deficiency. The levels of phytohormones (abscisic acid, jasmonic acid, and salicylic acid) and antioxidants (free proline and peroxidase) in stems decreased in low N treatment because of poor tissue N concentration, thereby attenuating antioxidant defense and Cd tolerance. The decreased Cd tolerance and inhibited xylem development under low N condition led to the dramatic decrement of Cd accumulation in stems. Adequate N application increased the phytohormone and antioxidant levels in stems, thereby promoting antioxidant defense, as indicated by the low malondialdehyde (MDA) level. Moreover, both the improved antioxidant defense and appropriate N nutrient status contributed to xylem development. Consequently, the capacity for Cd bioconcentration and accumulation in Populus stems was promoted by N application, thereby facilitating the phytoextraction of Cd from Cd-contaminated soils.

Introduction

Cadmium (Cd) is a toxic heavy metal that is harmful to humans and animals (He et al., 2013; Shi et al., 2015). The phytoremediation of Cd-contaminated soils has been proposed as a promising solution to this problem (Wu et al., 2010; Chen et al., 2011; He et al., 2015). For instance, plants can absorb and accumulate high amounts of Cd (hyperaccumulators) for the phytoremediation of Cd-contaminated soils (Shi et al., 2015). However, the ability of herbaceous hyperaccumulators to accumulate Cd is limited by their low biomass (Wu et al., 2010; He et al., 2011). Thus, fast-growing woody species, such as Populus and Salix, have been considered because of their feature huge biomass, rapid growth, high stem volume, and favorable tolerance to heavy metals (He et al., 2015). Furthermore, the use of woody species poses low risk of heavy metals entering the food chain (He et al., 2015).

Heavy metals can depress plant growth and consequently reduce biomass and crop yield (He et al., 2015; Shi et al., 2019). They can also affect the microstructure of plant tissues and organelles, thereby disrupting the organelle functions (Devi et al., 2007; Guo et al., 2009; Shi et al., 2018). In response to Cd stress, plants typically exhibit physiological and transcriptional responses to avoid or alleviate protein denaturation and oxidative damage caused by excessive reactive oxygen species (ROS) in their cells (Yang et al., 2011; Wang et al., 2013; Sofo et al., 2013). Enzymatic and nonenzymatic antioxidants play key roles in ROS scavenging and antioxidant defense (He et al., 2015, 2011; Sofo et al., 2013; Shi et al., 2018). The capacity for Cd uptake and translocation is related to the molecular and physiological regulation of Cd2+ detoxification and antioxidant defense in plants (He et al., 2015, 2011).

In most forest ecosystems, nutrient deficiency is a major constraint to woody plant growth (Li et al., 2012; Zhang et al., 2013; Luo et al., 2016). Nutrient-deficient soils may influence the adaptive responses of plants to environmental stresses, such as drought and heavy metal accumulation (Konotop et al., 2012; Malčovská et al., 2014; Xu et al., 2015; Khan et al., 2016). Nitrogen (N) is a major nutrient that is essential to plant development and stress tolerance (Luo et al., 2013a; Gan et al., 2016). N deficiency may substantially reduce photosynthesis and sugar metabolism, resulting in decreased biomass production (Luo et al., 2013b; Gan et al., 2016). N participates in biosynthesis and signal transduction of plant hormones related to stress tolerance (Luo et al., 2015; Shi et al., 2017; Luo et al., 2019). Moreover, N supply may positively or negatively affects plant metal uptake and metal translocation from roots to shoots (Zhang et al., 2014; Qasim et al., 2015; Zaid and Mohammad, 2018; Wu et al., 2018). In woody species, xylem is crucial to the mediation of Cd translocation from roots to shoots; thus, it determines Cd accumulation in the aerial organs of plants (Qin et al., 2013). Stem growth and xylem development in poplars are sensitive to N availability (Li et al., 2012). Poplar plantations are often on marginal lands with less N resources (Xu et al., 2015; Gan et al., 2016; Shi et al., 2017). Therefore, determining the influence of soil N availability on xylem development, Cd accumulation, and Cd tolerance in the stems of woody species is crucial for the phytoremediation of Cd-contaminated soils.

Populus × euramericana is a fast growing, highly tolerant and widely adaptive plant in the regions with high Cd contamination level (Wu et al., 2010; Di Baccio et al., 2011; Qasim et al., 2015, 2016). Considerable Cd accumulation without severe reduction in biomass accumulation has been demonstrated in P. × euramericana (Wu et al., 2010; Di Baccio et al., 2011; Qasim et al., 2016). In this study, a clone of Populus × euramericana was extensively investigated. The following hypotheses were addressed: (1) N availability may affect xylem development and levels of antioxidants and phytohormones in stems. (2) N availability may influence the capacity for Cd accumulation in stems via regulating xylem development and Cd tolerance. This study will provide guidelines for the phytoremediation of Cd-contaminated soil with limited N resources.

Section snippets

Plant material and experimental design

P. × euramericana clone (clone ID, “97″) derived from a cross-breeding program was used as the plant material. The clone shows favorable growth performance and wide adaptability in the northern parts of China. Plantlets were produced by micropropagation and then cultivated in a climate chamber (day temperature: 26 °C; night temperature: 20 °C; relative air humidity: 50%–60%; light per day: 14 h). After 25 days, the rooted plantlets were planted in 10 L pots filled with fine sand. Subsequently,

Growth traits and stem anatomy

N exerted remarkable effects on plant biomass and plant height (Fig. 1). The significant effects of Cd and the interaction effect of N and Cd (N × Cd) on the plant biomass were also detected (Fig. 1). Under adequate N condition, plant biomass and plant height were suppressed by high level of Cd exposure, whereas stem growth was unaffected by Cd under low N condition (Fig. 1). At low N condition, growth traits including plant biomass, plant height, and stem biomass decreased regardless of Cd

Influence of N deficiency and Cd exposure on secondary xylem development

In the present study, the secondary xylem development of poplar was suppressed by Cd exposure or N deficiency due to decreased cell layers in xylem. The inhibitory effect of N deficiency was more remarkable than that of Cd exposure (Fig. 1, Fig. 2). Considerable inhibitory effects of N deficiency on stem growth in Populus and other fast-growing plants may be explained as these species demands high amount of N (Luo et al., 2013a, 2015; Zheng et al., 2017). N addition enhances secondary xylem

Conclusions

The mechanisms of N-mediated Cd accumulation and Cd tolerance in poplar stems were demonstrated at anatomical and physiological levels, as summarized in a diagrammatic sketch (Fig. 5). As compared with N deficiency, Cd BCF and Cd content in stems were relatively high after adequate N supply (ca. 200 mg NH4NO3 kg−1 soil). Xylem development in stems was largely suppressed by the combined conditions of N deficiency and Cd exposure, but the suppression was alleviated by N application, facilitating

Acknowledgments

This project was financially supported by National Key R&D Program of China (Grant No. 2016YFD0600105), the Start-up Project for Introduced Recruit in Northwest A&F University (Z111021402), the China Scholarship Council (CSC NO. 201706305011), and the Fundamental Research Funds for the Central Universities (No. 2452016056).

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