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Morphological and Physiological Changes of Broussonetia Papyrifera Seedlings in Cadmium Contaminated Soil

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Morphological and Physiological Changes of Broussonetia Papyrifera Seedlings in Cadmium Contaminated Soil plants Article Morphological and Physiological Changes of Broussonetia papyrifera Seedlings in Cadmium Contaminated Soil Wan Zhang 1, Yunlin Zhao 1, Zhenggang Xu 1,2,* , Huimin Huang 1, Jiakang Zhou 1 and Guiyan Yang 2 1 Hunan Research Center of Engineering Technology for Utilization of Environmental and Resources Plant, Central South University of Forestry and Technology, Changsha 410004, China; [email protected] (W.Z.); [email protected] (Y.Z.); [email protected] (H.H.); [email protected] (J.Z.) 2 College of Forestry, Northwest A & F University, Yangling 712100, China; [email protected] * Correspondence: [email protected]; Tel.: +86-186-8494-5647 Received: 23 September 2020; Accepted: 1 December 2020; Published: 3 December 2020 Abstract: Broussonetia papyrifera is a widely distributed economic tree species, and it is also a pioneer species in adverse environments. In order to investigate the growth and adaptation mechanism of B. papyrifera under cadmium (Cd) contaminated soil, potted experiments were used with six-month treatments to study Cd enrichment and the transportation, morphological and physiological characteristics of B. papyrifera tissues. The results showed that Cd mainly accumulated in the root when the Cd concentration was high (14.71 mg/kg), and the root biomass was significantly reduced by Cd stress although Cd promoted the growth of seedlings. The bioconcentration factors (BCF) increased with the increase in Cd concentration, and reached the maximum value of 0.21 at 14.71 mg/kg. On the contrary, translocation factor (TF) decreased significantly at 8.28–14.71 mg/kg Cd concentration. Cd not only led to the loose arrangement of the xylem vessels of leaves, but also changed the chlorophyll content. However, B. papyrifera could synthesize organic solutes such as soluble protein, soluble sugar and proline to reduce the intracellular osmotic potential. Our study proved that B. papyrifera has good tolerance to Cd stress and is a pioneer tree species for soil and ecological environment restoration. Keywords: Broussonetia papyrifera; cadmium contaminated soil; antioxidant enzyme; anatomic structure 1. Introduction Due to the impact of industrialization and geochemical activities, heavy metal pollution in soil has become a serious environmental problem that limits crop production and even threatens human health through the food chain [1,2]. Cadmium (Cd) is a natural element in the earth’s crust and is usually combined with other elements (such as oxygen, chlorine or sulfur) to form minerals. Over the past two centuries, a large amount of Cd has been released and accumulated in the soil environment [3,4]. The traditional method of reducing the toxicity by replacing the soil contaminated with heavy metals is highly expensive, and the placement of contaminated soil might become an urgent problem to be solved, which could even cause secondary pollution [5]. At present, phytoremediation has become a more promising method of environmental restoration based on biological extraction and filtration [6–9]. Hyperaccumulators have good application prospects in the remediation of contaminated soil, such as the first known arsenic (As) hyperaccumulation plant Pteris vittata [10–12], the manganese (Mn) hyperaccumulation plant Phytolacca acinosa [13,14], Sedum [15,16] with super enrichment ability to Cd, etc. However, most of the hyperaccumulators are dwarf and the accumulation of heavy metals Plants 2020, 9, 1698; doi:10.3390/plants9121698 www.mdpi.com/journal/plants Plants 2020, 9, 1698 2 of 17 will also make the plants grow slowly, which brings great difficulties to their practical application. Woody plants have large biomass and a long growth cycle. Besides the developed root system, the area of stems, branches, and leaves form a larger green space. Moreover, most pollutants would not endanger people’s health by food. Thus, woody plants are considered to be a candidate vegetation source for heavy metal pollution remediation. In order to cope with different environmental conditions, plants would produce dynamic responses and positive adjustment in their biological characteristics, such as morphological structures, physiological mechanisms and even genetic characteristics [17–19]. Changes in plants’ morphologies are the most intuitive response to abiotic stress. Plants could adapt to water stress by reducing stomata frequency, stomata length and reducing leaf thickness, as well as increasing the thickness of the palisade parenchyma [20]. Under the lead stress, the Artemisia Sacrorum var. Messerschmidtiana in the mineral area showed stronger tolerance than that in the non-mineral area, which was mainly reflected in the thickening of the stem epidermis, cell wall and xylem tube wall [21]. Under the condition of low Mn concentration (1 mmol/L), the biomass, surface area and root volume of B. papyrifera were increased [22]. Of course, the physiological response would not be absent in the process of coping with environmental stress. Plants could resist the toxicity of Cd and Mn by promoting the synthesis of soluble protein and increasing the activities of antioxidant enzyme, while high concentrations of Cd and Mn led to the increase in malondialdehyde (MDA), proline and H2O2 content, causing membrane lipid peroxidation and severe membrane damage [22,23]. Studies have also shown that Cd could inhibit the photochemical reaction of plant photosynthesis and destroy the metabolism of chlorophyll, and is an effective inhibitor of photosynthesis [6,24,25]. Broussonetia papyrifera, also known as paper mulberry, is a deciduous tree or shrub. It is widely distributed around the world, providing possibilities for extensive ecological restoration [26,27]. The B. papyrifera also has high economic benefits, its bast cellulose content can be as high as 63.76% [28], which can be blended with cotton [29], and the earliest high quality bark cloth was made of B. papyrifera bast [30,31]. The leaves are rich in amino acids, proteins, fats and trace elements, which makes them a good source of feed. In addition, the leaves are covered with fine pubescence and can be used to monitor the air pollution in their growing areas [32]. As a medicinal resource, B. papyrifera’s flowers are natural antioxidants and can treat impotence and ophthalmic diseases [33,34]. The fruit extract is not only a traditional medicine for treating cardiovascular diseases, but also contains alkaloids as a drug candidate for treating cancer [35]. Stem bark has a high content of phenolic compounds and is a potential resource for medical pharmaceuticals and anti-inflammatory drugs [36,37]. The root system of the B. papyrifera is very developed. Under natural conditions, it is mainly propagated by root sprout, and it is an environmental tree species that prevents soil erosion. Because of its fast-growing and adaptable ability, the tree is a pioneer species in desertification areas, mines, rivers, valleys, droughts and other extreme environments [38,39]. Based on the good economic potentiality and environmental effects, B. papyrifera is an important candidate plant for phytoremediation [22]. At present, the research on the adversity of B. papyrifera mostly focuses on drought and saline–alkali stresses [40–42]. There are few studies on the tolerance mechanism under heavy metal pollution. Among them, Zhao et al. [43] investigated the heavy metal enrichment of heavy metal polluted plants and found that B. papyrifera had higher enrichment ability for Pb and Zn, especially the leaf part, and the Cd enrichment ability was also higher than in other species. The manner in which B. papyrifera responds to heavy metal stress requires a detailed analysis. In order to explore more details about the response of B. papyrifera to Cd stress, the seedling growth, leaf anatomical structure and related physiological indexes of B. papyrifera were determined under different Cd stress conditions. The research can not only help understand the mechanism of B. papyrifera adaptation to poor environments, but also help to establish a technical ecology restoration system based on the tree. Plants 2020, 9, x FOR PEER REVIEW 3 of 17 papyrifera adaptation to poor environments, but also help to establish a technical ecology restoration system based on the tree. Plants 2020, 9, 1698 3 of 17 2. Results 2.2.1. Results Height Changes and the Characteristics of Leaf Phenotype 2.1. HeightWithin Changes 180 d and of Cd the Characteristicsstress, the height of Leaf of PhenotypeB. papyrifera seedlings in the soil without Cd solution irrigation (non-irrigated soil) did not change significantly (p > 0.05) (Figure 1). The initial height of all B. papyriferaWithin 180 seedlings d of Cd averaged stress, the about height 40 of cm.B. papyriferaIn order toseedlings adapt to in the the seasonal soil without changes, Cd solutionthe plant irrigationentered (non-irrigatedthe wintering soil)period did and not stopped change significantlygrowing at (90p > d.0.05) At this (Figure stage,1). Thethe growth initial height change of of all B. B.papyrifera papyrifera underseedlings 5.71 averaged mg/kg Cd about concentration 40 cm. In order was tothe adapt largest, to the with seasonal an increase changes, of 38.34 the plant ± 5.31 entered cm. At the180 wintering d, the periodheight andof seedlings stopped growingincreased at 90significantly d. At this stage, at 11.49 the growthmg/kg changeand 14.71 of B. papyriferamg/kg Cd under 5.71 mg/kg Cd concentration was the largest, with an increase of 38.34 5.31 cm. At 180 d, concentrations, indicating that Cd stress can stimulate the growth of B. papyrifera± seedlings. After 20 thed, heightthe leaf of phenotype seedlings of increased B. papyrifera significantly seedlings atchanged 11.49 mg (Fi/gurekg and S1: 14.71The photo mg/kg shows Cd concentrations, the second fully indicatingexpanded that leaf Cdof the stress seedling can stimulate from top the to growthbottom), of especiallyB. papyrifera at 11.49seedlings. mg/kg Afterand 14.71 20 d, mg/kg the leaf Cd phenotypeconcentrations. of B. papyrifera There wereseedlings folds on changed the surface (Figure of S1:the Theleaves.
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