Indexes of Radicle are Sensitive and Effective for Assessing Copper and Zinc Tolerance in Germinating Seeds of Suaeda salsa
1
State Key Laboratory of Desert and Oasis Ecology, Xinjiang Institute of Ecology and Geography, Chinese Academy of Sciences, Urumqi 830011, China
2
University of Chinese Academy of Sciences, Beijing 100049, China
3
Tasmanian Institute of Agriculture, University of Tasmania, Hobart 7005, Australia
*
Author to whom correspondence should be addressed.
Agriculture 2020, 10(10), 445; https://0-doi-org.brum.beds.ac.uk/10.3390/agriculture10100445
Submission received: 24 August 2020
/
Revised: 24 September 2020
/
Accepted: 28 September 2020
/
Published: 30 September 2020
(This article belongs to the Special Issue Recent Advances in Technological and Agronomic Practices for Sustainable Agriculture)
Abstract
:Euhalophytes, such as Suaeda salsa, are ideal candidates to remediate heavy metal-polluted saline soils. However, the metal tolerance ability of dimorphic seeds and subsequent seedlings is largely unknown. This study investigated the tolerance of S. salsa seeds to different concentrations of Cu2+ (0–300 mM) and Zn2+ (0–300 mM) during germination and seedling growth stages. Results showed that dimorphic seeds of S. salsa had high metal tolerance during germination, and even germinated under 300 mM Cu and Zn treatments. However, seedling growth was more sensitive to metal solutions and radicle growth was almost completely inhibited by Cu at 10 mM, and by Zn at 50 mM. Germinating seeds and seedlings of S. salsa had a higher metal toxicity threshold of Zn than that of Cu. In all indexes, indexes of radicle were the most sensitive and effective indicator of metal tolerance. Seeds of S. salsa germinated successfully and seedlings survived under high Zn and Cu stress. The results suggest that S. salsa could be sown directly in heavy metal-contaminated soils for phytoremediation.
1. Introduction
Heavy metal pollution is a great environmental threat that reduces plant productivity [1]. With the rapid development of industry and agriculture worldwide, heavy metal-contaminated soil has become a serious environmental problem [2]. Polluted soils not only lead to deleterious effects on plants, but also pose human health risks via direct ingestion, contact with polluted soil, and the food chain [3,4]. In recent years, saline soils, including those in coastal areas and arid regions, are influenced by heavy metals [5,6,7]. Developing halophyte remediation technologies may help solve this problem [8,9]. The first critical step of phytoremediation is seedling emergence in the heavy metal-contaminated soils. Halophytes generally exhibit high salt tolerance during germination and seedling establishment. However, their ability to tolerate high levels of heavy metals is still largely unknown.
Seed germination is a critical transition because dry seeds are the most tolerant of and seedlings are the most sensitive to environmental stresses [10]. During the germination stage, seed germination percentage and velocity decrease with the increase in heavy metal concentrations [11,12]. Furthermore, seedling growth parameters are even more sensitive to heavy metal stress [13,14,15]. There are few studies on the inhibition of seed germination and seedling growth thereafter on wild species caused by heavy metals [6,16]. For example, seeds of several Australian native species, namely Astrebla lappacea, Themeda australis, Austrostipa scabra and Acacia harpophylla, were placed in different concentrations of arsenic (As), copper (Cu), zinc (Zn), manganese (Mn) and lead (Pb) to test their tolerance ability during germination and seedling growth stages [14].
Cu and Zn are essential micronutrients for plants at low levels of concentration, but they are toxic and retard growth or even cause death for most plant species at higher concentrations [11,17]. When in excess, Zn limits plant growth of root and expansion of leaves. Cu toxicity is characterized by chlorosis of leaves and the inhibition of root growth [18]. Cu and Zn toxicity have been reported for many plants, including many economically important crops. It has been reported that some plants have a high tolerance to Cu and Zn, and even accumulate large amounts of them in aboveground tissues [19,20].
Euhalophyte Suaeda salsa grows in inland saline soils and intertidal regions. This plant species has a high salt tolerance during its whole life cycle, from the germination phase to the fruiting phase [21]. In intertidal regions, S. salsa even can form a monospecific community. It can also absorb and accumulate different heavy metals, such as As, Pb, chromium (Cr) and Cu [7,17]. NaCl improved translocation and accumulation of Pb in S. salsa under Pb stress, thus enhancing the phytoextraction of Pb [22]. This species produces two types of seeds that differ in seed color, seed morph, dormancy type and germination characteristics. As Cu-tolerant halophytes, S. salsa plants grown from dimorphic seeds have different salt tolerances but exhibit similar responses to Cu [23]. Dimorphic seeds of S. salsa can germinate under a high NaCl concentration, and brown seeds have a higher germination percentage and velocity under salt stress during germination [21,24]. Although several studies have tested the tolerance ability of S. salsa seeds to different heavy metals [25,26], little information is known regarding the effect of seed type on heavy metal tolerance of S. salsa.
To evaluate the heavy metal tolerance of germinating seeds correctly, it is necessary to select an effective index. Though germination percentage and germination velocity are common indicators, several research studies suggest that indexes related to young seedlings are more suitable for metal tolerance analyses [6,14]. Thus, in this study, we selected two indexes for germinating seeds and four indexes for seedling establishment. The goal of this study was to determine the effect of Cu and Zn stress on the halophyte S. salsa at the germination and early seedling growth stages. Specifically, we asked the following questions: (1) Do dimorphic seeds of S. salsa have the same metal tolerance during germination? (2) Which index is more suitable for the proper analysis of heavy metal tolerance? (3) Does Cu exhibit stronger toxicity than Zn at the same concentrations?
2. Materials and Methods
2.1. Plant Materials
Mature fruits of S. salsa were collected from at least 50 plants growing in a salt desert in Karamay (North Xinjiang, China) in November 2019. Vegetation consists of plant species such as Suaeda aralocaspica, Salsola subcrassa and Phragmites australis. This site belongs to a temperate continental desert arid climate. The annual average temperature is 8.1 °C. The mean annual precipitation is 105 mm and mean annual potential evaporation is 3545 mm.
The fruits were allowed to dry naturally for 2 weeks in laboratory room. Seeds were separated from the dried plant material and sorted into brown seeds and black seeds. Each type of seed was pooled and stored at room temperature until used in experiments.
2.2. Chemicals
Water-soluble metal compounds were used throughout. CuSO4·5H2O and ZnSO4·7H2O were purchased from Fuchen Chemical Reagent Co., Ltd. (Tianjin, China).
2.3. Germination Experiment
Effects of different concentrations of Cu and Zn on the germination of dimorphic seeds of S. salsa were evaluated using single metal solutions prepared in deionized water. For each treatment, four replicates of 25 seeds were incubated in 50 mm diameter Petri dishes on two layers of No. 1 filter paper moistened with 2.5 mL of distilled water or with different concentrations (0.01, 0.05, 0.1, 0.5, 1, 5, 10, 50, 100, 150, 200, 250 and 300 mM) of Cu and Zn. To avoid evaporation, after being covered with lids, the edges of the Petri dishes were sealed with Parafilm. Then, the Petri dishes were transferred to light incubator chamber (GXZ-380, Jiangnan Instrument Factory, Zhejiang, China) and incubated at daily (12/12-h) temperature regimes of 10: 25 °C under a 12 h daylight photoperiod for 20 days. The dishes were opened daily to count the number of germinated seedlings. Because black seeds are smaller and the seed coat of black seeds is more rigid than that of brown seeds, the germination test standards for them are different. For black seeds, the radicle was ≥1mm. For brown seeds, the radicle was ≥2 mm. Germination percentage (%) = (the number of seeds germinated in different metal solutions/total number of seeds tested) × 100. The velocity of germination was estimated using a modified Timson’s index of germination velocity [27].
2.4. Seedling Incubation
For the first week of the germination experiment, at each counting, germinated seeds were transferred into new Petri dishes (90 mm diameter) with the same solutions under the same temperature and light conditions. Incubation of the seedlings was terminated at the end of the germination experiment. Radicle length and shoot length were measured for 20 randomly selected seedlings under a microscope with Olympus CellSens software. Radicle tolerance index (%) = (mean length of the radicle in metal treatment/mean length of the radicle in distilled water control) × 100. Shoot tolerance index (%) = (mean length of the shoot in metal treatment/mean length of the shoot in distilled water control) × 100.
2.5. Data Analysis
Data for germination percentage, germination index, shoot and radicle tolerance index were analyzed by linear regression using the enter linear regression method (all independent variables were entered into the equation in a single step). The multiple linear regression model included seed type (brown and black seeds), heavy metal type (Cu and Zn) and metal concentration (0, 0.01, 0.05, 0.1, 0.5, 1, 5, 10, 50, 100, 150, 200, 250 and 300 mM). All statistical analyses were conducted using SPSS 16.0 (SPSS, Inc., Chicago, IL, USA). All data were expressed as means ± SE. One-way ANOVA and Turkey’s test were used to determine significant differences among different concentrations of Cu or Zn treatments for different indexes of each seed type of S. salsa. Independent samples T-Test was used to determine whether there was a difference between dimorphic seeds for different indexes of at the same Cu or Zn concentrations.
3. Results
3.1. Germination
Germination percentage and germination index were significantly affected by seed type (p < 0.001), metal type (p < 0.001) and metal concentration (p < 0.001) (Table 1).
Germination percentages of brown seeds in all Cu treatments ranged from 38% to 100%, whereas those of black seeds were 51–83% (Table 2). In other words, germination percentages of brown seeds were higher than that of black seeds at a low Cu concentration, similar to that of black seeds at a medium concentration, and lower at a high concentration. Germination percentages of dimorphic seeds in Zn solutions showed a similar trend. Germination indexes of brown seeds in all Cu treatments were 36.2–98.2%, whereas those of black seeds were 30.9–61.1% (Table 3). Germination indexes of brown seeds in all Zn treatments were 52.1–98%, whereas those of black seeds were 50.5–61%. At the same Cu or Zn concentration, the germination index of brown seeds was significantly higher than that of black seeds (Table 3).
For each seed type, at the same concentration, seeds generally had a higher germination percentage and index in Zn solution than in Cu solution. For example, germination of brown seeds was 99% at 5 mM Zn solution, whereas only 81% germination was reached at 5 mM Cu solution (Table 2). Germination index of black seeds reached 53.9% at the highest level of Zn toxicity (300 mM), but the germination index of black seeds was only 30.9% at the same level of Cu toxicity (Table 3).
As Cu concentration increased from 0 to 300 mM, germination percentage and germination index of dimorphic seeds decreased (Table 2 and Table 3). For brown seeds, germination percentage decreased from 100% at control to 38% at 300 mM. There was a different trend for the germination responses of dimorphic seeds in Zn solutions. The germination percentage and germination index of brown seeds also showed a decline trend as in Cu solutions. However, for black seeds, germination percentages and germination indexes did not show a significant difference among different Zn concentrations (Table 2 and Table 3).
3.2. Seedling Growth
Radicle and shoot lengths were significantly affected by seed type (p < 0.001), heavy metal type (p < 0.001) and metal concentration (p < 0.001) (Table 1).
Brown seeds generally had higher shoot lengths than black seeds in the same Cu or Zn solutions (Figure 1 and Figure 2). Radicle lengths of brown seeds in all Cu treatments were 2.2–14.3 mm, whereas those of black seeds were 1.2–8.3 mm (Figure 1). Radicle length of brown seeds was higher than that of black seeds at the same Cu concentrations. Similarly, the radicle of brown seeds had higher length growth than that of black seeds in the same Zn solutions (Figure 2).
For each seed type, at the same concentration, seeds generally had higher lengths and better growth of radicles and shoots in Zn solution than that in Cu solution. For example, the radicle length of brown seeds was 10.0 mm at 0.1 mM Zn solution, whereas it was only 4.4 mm at the same concentration of Cu. Radicle growth was almost completely inhibited by Cu at 10 mM, and by Zn at 50 mM (Figure 3 and Figure 4).
The radicle and shoot length of seedlings grown from dimorphic seeds decreased with the increase of metal concentrations. Radicle length from brown seeds was significantly reduced compared to the control at Cu concentrations of 0.05 mM and higher. Shoot length from brown seeds was not affected by Cu up to 0.1 mM but it was significantly reduced at 0.5 mM and progressively reduced further at higher concentrations compared to control (Figure 1 and Figure 3). The decreasing trend of radicle and shoot lengths in Zn solutions was similarly observed in Cu solutions, but was less severe (Figure 2).
The radicle tolerance index and the shoot tolerance index showed similar changes in radicle and shoot lengths (Table 4 and Table 5). Both indexes were usually higher in Zn solutions. The radicle tolerance index was more sensitive to metal toxicity than the shoot tolerance index. The radicle tolerance index reached limitation values in relatively lower metal concentrations. For example, the limitation value for the radicle tolerance index of seedlings from brown seeds is 10 mM Cu concentration. However, for shoot tolerance index, it was 150 mM Cu concentration (Table 4).
4. Discussion
Although dormancy and germination of dimorphic seeds of S. salsa and eco-physiological responses of plants grown from dimorphic seeds to different environmental factors have been studied extensively [5,21,23,24], our study is the first to analyze germination of dimorphic seeds and seedling growth thereafter in different heavy metal solutions. In addition, our data indicate that both types of seeds of S. salsa have high Cu and Zn tolerance during the germination stage, and young seedling growth is a critical stage for metal tolerance. Cu is more toxic than Zn to germinating seeds, especially for radicle growth. The results suggest that seeds and seedlings of S. salsa are not only tolerant to high salinity but also to high levels of heavy metals, such as Cu and Zn.
Dimorphic seeds of S. salsa displayed differential germination responses to Cu and Zn toxicity. The germination percentage of brown seeds reached 38% and 54% at 300 mM Cu and Zn, respectively. However, germination of black seeds was 54% and 78%. The germination difference of dimorphic seeds in metal solutions might be related to their differential salt tolerances. Brown seeds of S. salsa are more salt tolerant than black seeds [21]. The contrasting abiotic tolerances of dimorphic seeds are also found in other plant species, such as Bidens pilosa [28], as well as Arthrocnemum macrostachyum [29] and Torilis arvensis [30]. This might be due to the difference in antioxidant ability between dimorphic seeds [29]. Furthermore, the tolerance difference of dimorphic seeds to abiotic stresses even has a carry-over effect. For example, the differential salinity tolerance of dimorphic seeds of Suaeda splendens carried over from seeds to seedlings [31]. Radicle and shoot lengths of brown seeds are generally longer than those of black seeds of S. salsa under the same metal treatment, however, this might be caused by the size difference between dimorphic seeds and the delayed germination of black seeds. Besides, the radicle and shoot tolerance indexes did not show a clear difference in pattern for dimorphic seeds. Moreover, adult plants grown from dimorphic seeds of S. salsa exhibited similar eco-physiological responses to Cu. Thus, heavy metal tolerance of seedlings between dimorphic seeds needs more indexes to evaluate.
Cu had more inhibitory effects on seed germination and, thereafter, seedlings of S. salsa compared to Zn. Cu and Zn are essential micronutrients and are required for different physiological processes. However, at high concentrations, both metals stimulate the production of ROS (Reactive oxygen species) and adversely affect plant growth and metabolism. Cu at a high concentration has higher toxicity than Zn [12]. This can also be reflected by the definition of Cu and Zn hyperaccumulator plants. Hyperaccumulation of Cu was defined as >300 ppm foliar Cu [32]. Zn hyperaccumulator can accumulate >10,000 ppm in aerial parts [20]. The germination index of brown and black seeds reached 81.2 and 47.5, respectively, at 10 mM Cu, but the germination index of brown and black seeds was 94.9 and 61, respectively, at the same concentration of Zn. Furthermore, at the seedling growth stage, the radicle tolerance indexes of brown and black seeds were 30.65 and 45.7, respectively, at 0.1 mM Cu, but that were 68.61 and 70.81 at 0.1 mM Zn. S. salsa seeds had high Cu and Zn tolerance during germination. Even at 100 mmol L−1 Cu and Zn, the germination percentages of both types of seeds were higher than 65%. Germination percentages of most plant species significantly decline under 0.5 mM Cu and Zn [14,33]. However, germination of S. salsa seeds did not show a significant difference until under 5 mM Cu and Zn. Seedlings of S. salsa did not show obvious toxic symptoms under 0.1 mM Cu and 1 mM Zn (Figure 3). Thus, S. salsa was tolerant to high concentrations of Cu and Zn at the germination and seedling stages.
Among all the indexes, radicle length and radicle tolerance index are more sensitive to Cu and Zn. Germination percentage and germination index are insensitive to metal stress, especially under Zn treatments. For black seeds, germination percentages and indexes did not significantly change under 0 to 300 mM Zn. Compared with the indexes of germinated seeds, the indexes of seedlings were more sensitive to metal stresses. With the increase in metal concentration, indexes of seedlings decrease gradually. For example, the radicle tolerance index of black seeds decreased from 100 to 48 when the Zn concentration changed from control to 0.5 mM Zn. It was also found that the indexes of radicle were more sensitive to metal stresses than those of shoot. For example, the radicle tolerance index of brown seeds was 24 under 1 mM Cu and the shoot tolerance index of brown seeds was 58 under the same Cu concentration. This high sensitivity of radicles can be explained by the fact that the radicle is the first part of a seedling to suffer from metal toxicity. Thus, when selecting high metal-tolerant halophytes, we should test not only the tolerance indexes of seeds and adult plants but also the indexes of seedlings.
5. Conclusions
In summary, this study shows that indexes of radicle are the most sensitive and effective indicator of metal tolerance for germinating seeds of S. salsa. These indexes may also serve as a useful index for future research on the tolerance of different metals for plants during germination and seedling growth stages. The present study demonstrates that dimorphic seeds of S. salsa are able to germinate under high Zn and Cu concentrations. However, seedling growth, especially the radicle growth, is more sensitive to the same level of metal stress. Overall, successful germination and survival of seedlings of S. salsa under medium Zn and Cu metal stress has been proved. Thus, this plant species might provide an important contribution to phytoremediation by sowing seeds directly into heavy metal contaminated soils.
Author Contributions
Conceptualization, L.W. and L.J.; investigation, H.Z. and L.J.; writing—original draft preparation, H.Z., L.J and L.W.; writing—review and editing, M.T., J.M., Z.Z. and L.W.; visualization, H.Z. and L.W.; project administration, L.W.; funding acquisition, Z.Z. All authors have read and agreed to the published version of the manuscript.
Funding
This research was funded by the National Key Research and Development Program of China (grant number 2018YFE0207200) and the Strategic Priority Research Program of the Chinese Academy of Sciences (grant number XDA2003010302).
Conflicts of Interest
The authors declare no conflict of interest.
References
- Hussain, S.; Khaliq, A.; Noor, M.A.; Tanveer, M.; Husssin, H.A.; Hussain, S.; Shah, T.; Mehmood, T. Metal toxicity and nitrogen metabolism in plants: An overview. In Carbon and Nitrogen Cycling in Soil; Datta, R., Meena, R.S., Pathan, S.I., Ceccherini, M.T., Eds.; Springer: Singapore, 2020; pp. 221–248. [Google Scholar]
- Muthusaravanan, S.; Sivarajasekar, N.; Vivek, J.S.; Paramasivan, T.; Naushad, M.; Prakashmaran, J.; Gayathri, V.; AI-Duaij, O.K. Phytoremediation of heavy metals: Mechanisms, methods and enhancements. Environ. Chem. Lett. 2018, 16, 1339–1359. [Google Scholar] [CrossRef]
- Ali, H.; Khan, E.; Sajad, M.A. Phytoremediation of heavy metals-Concepts and applications. Chemosphere 2013, 91, 869–881. [Google Scholar] [CrossRef]
- Ghori, N.H.; Ghori, T.; Hayat, M.Q.; Imadi, S.R.; Gul, A.; Altay, V.; Ozturk, M. Heavy metal stress and responses in plants. Int. J. Environ. Sci. Technol. 2019, 16, 1807–1828. [Google Scholar] [CrossRef]
- He, J.; Ji, Z.X.; Wang, Q.Z.; Liu, C.F.; Zhou, Y.B. Effect of Cu and Pb pollution on the growth and antioxidant enzyme activity of Suaeda heteroptera. Ecol. Eng. 2016, 87, 102–109. [Google Scholar] [CrossRef]
- Nedjimi, B. Germination characteristics of Peganum harmala L. (Nitrariaceae) subjected to heavy metals: Implications for the use in polluted dryland restoration. Int. J. Environ. Sci. Technol. 2020, 17, 2113–2122. [Google Scholar] [CrossRef]
- Shang, C.L.; Wang, L.; Tian, C.Y.; Song, J. Heavy metal tolerance and potential for remediation of heavy metal-contaminated saline soils for the euhalophyte Suaeda salsa. Plant Signal. Behav. 2020. [Google Scholar] [CrossRef]
- Wang, H.L.; Tian, C.Y.; Jiang, L.; Wang, L. Remediation of heavy metals contaminated saline soils: A halophyte choice? Environ. Sci. Technol. 2014, 48, 21–22. [Google Scholar] [CrossRef]
- Van Oosten, M.J.; Maggio, A. Functional biology of halophytes in the phytoremediation of heavy metal contaminated soils. Environ. Exp. Bot. 2015, 111, 135–146. [Google Scholar] [CrossRef]
- Gutterman, Y. Survival Strategies of Annual Desert Plants; Springer: Berlin, Germany, 2002. [Google Scholar]
- Ye, N.; Li, H.; Zhu, G.; Liu, R.; Xu, W.; Jing, Y.; Peng, X.; Zhang, J. Copper suppresses abscisic acid catabolism and catalase activity, and inhibits seed germination of rice. Plant Cell Physiol. 2014, 55, 2008–2016. [Google Scholar] [CrossRef] [Green Version]
- Pokorska-Niewiada, K.; Rajkowska-Myśliwiec, M.; Protasowicki, M. Acute lethal toxicity of heavy metals to the seeds of plants of high importance to humans. Bull. Environ. Contam. Toxicol. 2018, 101, 222–228. [Google Scholar] [CrossRef] [Green Version]
- Li, W.; Khan, M.A.; Yamaguchi, S.; Kamiya, Y. Effects of heavy metals on seed germination and early seedling growth of Arabidopsis thaliana. Plant Growth Regul. 2005, 46, 45–50. [Google Scholar] [CrossRef]
- Guterres, J.; Rossato, L.; Doley, D.; Pudmenzky, A.; Bee, C.; Cobena, V. Assessing germination characteristics of Australian native plant species in metal/metalloid solution. J. Hazard. Mater. 2019, 364, 173–181. [Google Scholar] [CrossRef]
- Yáñez-Espinosa, L.; Briones-Gallardo, R.; Flores, J.; Álvarez del Castillo, E. Effect of heavy metals on seed germination and seedling development of Nama aff. stenophylla collected on the slope of a mine tailing dump. Int. J. Phytoremediation 2020. [Google Scholar] [CrossRef]
- Nanda, R.; Agrawal, V. Elucidation of zinc and copper induced oxidative stress, DNA damage and activation of defence system during seed germination in Cassia angustifolia Vahl. Environ. Exp. Bot. 2016, 125, 31–41. [Google Scholar] [CrossRef]
- Liu, X.; Shen, X.; Lai, Y.; Ji, K.; Sun, H.; Wang, Y.; Hou, C.; Zou, N.; Wan, J.; Yu, J. Toxicological proteomic responses of halophyte Suaeda salsa to lead and zinc. Ecotoxicol. Environ. Saf. 2016, 134, 163–171. [Google Scholar] [CrossRef] [PubMed]
- Marschner, P. Marschner’s Mineral Nutrition of High Plants, 3rd ed.; Science Press: Beijing, China, 2013. [Google Scholar]
- Lange, B.; van der Ent, A.; Baker, A.J.M.; Echevarria, G.; Mahy, G.; Malaisse, F.; Meerts, P.; Pourret, O.; Verbruggen, N.; Faucon, M.P. Copper and cobalt accumulation in plants: A critical assessment of the current state of knowledge. New Phytol. 2016, 213, 537–551. [Google Scholar] [CrossRef] [PubMed]
- Balafrej, H.; Bogusz, D.; Triqui, Z.-E.A.; Guedira, A.; Bendaou, N.; Smouni, A.; Fahr, M. Zinc hyperaccumulation in plants: A review. Plants 2020, 9, 562. [Google Scholar] [CrossRef] [PubMed]
- Song, J.; Wang, B. Using euhalophytes to understand salt tolerance and to develop saline agriculture: Suaeda salsa as a promising model. Ann. Bot. 2015, 115, 541–553. [Google Scholar] [CrossRef] [Green Version]
- Wang, F.L.; Song, N.N. Salinity-induced alterations in plant growth, antioxidant enzyme activities, and lead transportation and accumulation in Suaeda salsa: Implications for phytoremediation. Ecotoxicology 2019, 28, 520–527. [Google Scholar] [CrossRef]
- Jiang, L.; Wang, L.; Zhang, K.; Tian, C.Y. Copper-induced similar changes in growth and physiological responses of plants grown from dimorphic seeds of Suaeda salsa. Pak. J. Bot. 2018, 50, 871–877. [Google Scholar]
- Song, J.; Fan, H.; Zhao, Y.; Jia, Y.; Du, X.; Wang, B. Effect of salinity on germination, seedling emergence, seedling growth and ion accumulation of a euhalophyte Suaeda salsa in an interidal zone and on saline inland. Aquat. Bot. 2008, 88, 331–337. [Google Scholar] [CrossRef]
- Liu, S.; Yang, C.; Xie, W.; Xia, C.; Fan, P. The effects of cadmium on germination and seedling growth of Suaeda salsa. Procedia Environ. Sci. 2012, 16, 293–298. [Google Scholar] [CrossRef] [Green Version]
- Wan, Z.; Gao, T.; Zhou, Y.; Wang, Y.; Chang, G.; Ju, T.; Yang, Y.; Zhang, Q. Seed germination, bud growth and heavy-metal accumulation of Suaeda salsa. Chin. J. Biotechnol. 2020, 36, 493–507, (In Chinese with English Abstract). [Google Scholar] [CrossRef]
- Ajmal, K.M.; Gul, B.; Weber, D.J. Germination of dimorphic seeds of Suaeda moquinii under high salinity stress. Aust. J. Bot. 2001, 49, 185–192. [Google Scholar]
- Zhang, K.; Yao, L.; Zhang, Y.; Tao, J. Achene heteromorphism in Bidens pilosa (Asteraceae): Differences in germination and possible adaptive significance. AoB Plants 2019, 11, plz026. [Google Scholar] [CrossRef] [Green Version]
- Nisar, F.; Gul, B.; Khan, M.A.; Hameed, A. Heteromorphic seeds of coastal halophytes Arthrocnemum macrostachyum and A. indicum display differential patterns of hydrogen peroxide accumulation, lipid peroxidation and antioxidant activities under increasing salinity. Plant Physiol. Biochem. 2019, 144, 58–63. [Google Scholar] [CrossRef]
- Payamani, R.; Nosratti, I.; Amerian, M. Variations in the germination characteristics in response to environmental factors between the hairy and spiny seeds of hedge parsley (Torilis arvensis Huds.). Weed Biol. Manag. 2018, 18, 176–183. [Google Scholar] [CrossRef]
- Redondo-Gómez, S.; Mateos-Naranjo, E.; Cambrollé, J.; Luque, T.; Figueroa, M.E.; Davy, A.J. Carry-over of differential salt tolerance in plants grown from dimorphic seeds of Suaeda splendens. Ann. Bot. 2008, 102, 103–112. [Google Scholar] [CrossRef]
- van der Ent, A.; Baker, A.J.M.; Reeves, R.D.; Pollard, A.J.; Schat, H. Hyperaccumulators of metal and metalloid trace elements: Facts and fiction. Plant Soil 2013, 362, 319–334. [Google Scholar] [CrossRef]
- Boi, M.E.; Porceddu, M.; Cappai, G.; De Giudici, G.; Bacchetta, G. Effects of zinc and lead on seed germination of Helichrysum microphyllum subsp. tyrrhenicum, a metal-tolerant plant. Int. J. Environ. Sci. Technol. 2020, 17, 1917–1928. [Google Scholar] [CrossRef]
Figure 1.
Effect of Cu on (a) shoot and (b) radicle length of seedlings grown from dimorphic seeds of S. salsa.
Figure 1.
Effect of Cu on (a) shoot and (b) radicle length of seedlings grown from dimorphic seeds of S. salsa.
Figure 2.
Effect of Zn on (a) shoot and (b) radicle length of seedlings grown from dimorphic seeds of S. salsa.
Figure 2.
Effect of Zn on (a) shoot and (b) radicle length of seedlings grown from dimorphic seeds of S. salsa.
Figure 3.
Radicle elongation of seedlings grown from dimorphic seeds of S. salsa after 20 days in various concentrations of Cu solutions.
Figure 3.
Radicle elongation of seedlings grown from dimorphic seeds of S. salsa after 20 days in various concentrations of Cu solutions.
Figure 4.
Radicle elongation of seedlings grown from dimorphic seeds of S. salsa after 20 days in various concentrations of Zn solutions.
Figure 4.
Radicle elongation of seedlings grown from dimorphic seeds of S. salsa after 20 days in various concentrations of Zn solutions.
Table 1.
Multivariate analysis of correlates associated with germination percentage and index of dimorphic seeds of Suaeda salsa, radicle and shoot length of seedlings grown from both types of seeds.
Table 1.
Multivariate analysis of correlates associated with germination percentage and index of dimorphic seeds of Suaeda salsa, radicle and shoot length of seedlings grown from both types of seeds.
| Index | Factor | B (SE) | β | p-Value |
|---|---|---|---|---|
| Germination percentage | Metal type | 8.607 (1.561) | 0.259 | <0.001 |
| Seed type | −10.036 (1.561) | −0.302 | <0.001 | |
| Solution concentration | −0.097 (0.008) | −0.598 | <0.001 | |
| Germination index | Metal type | 8.471 (1.41) | 0.199 | <0.001 |
| Seed type | −29.421 (1.41) | −0.692 | <0.001 | |
| Solution concentration | −0.102 (0.007) | −0.489 | <0.001 | |
| Radicle length | Metal type | 1.137 (0.209) | 0.143 | <0.001 |
| Seed type | −1.651 (0.209) | −0.208 | <0.001 | |
| Solution concentration | −0.016 (0.001) | −0.404 | <0.001 | |
| Shoot length | Metal type | 1.102 (0.14) | 0.158 | <0.001 |
| Seed type | −1.394 (0.14) | −0.201 | <0.001 | |
| Solution concentration | −0.024 (0.001) | −0.695 | <0.001 |
Table 2.
Effect of CuSO4 and ZnSO4 on germination percentage of dimorphic seeds of S. salsa.
| Concentration (mM) | CuSO4 | ZnSO4 | ||
|---|---|---|---|---|
| Brown Seed | Black Seed | Brown Seed | Black Seed | |
| 0 | 100.0 ± 0.0 Aa | 74.0 ± 2.6 Bab | 100.0 ± 0.0 Aa | 82.0 ± 2.6 Ba |
| 0.01 | 100.0 ± 0.0 Aa | 71.0 ± 1.9B Abc | 99.0 ± 1.0 Aa | 72.0 ± 5.4 Ba |
| 0.05 | 96.0 ± 1.6 Aab | 77.0 ± 4.4 Bab | 100.0 ± 0.0 Aa | 68.0 ± 2.3 Ba |
| 0.1 | 99.0 ± 1.0 Aab | 73.0 ± 3.4 Bab | 98.0 ± 1.2 Aa | 69.0 ± 5.7 Ba |
| 0.5 | 100.0 ± 0.0 Aa | 83.0 ± 2.5 Ba | 99.0 ± 1.0 Aa | 81.0 ± 1.9 Ba |
| 1 | 98.0 ± 1.2 Aab | 73.0 ± 6.6 Bab | 99.0 ± 1.0 Aa | 80.0 ± 5.2 Ba |
| 5 | 81.0 ± 5.7 Ac | 70.0 ± 4.8 Aabc | 99.0 ± 1.0 Aa | 76.0 ± 0.0 Ba |
| 10 | 85.0 ± 3.8 Abc | 71.0 ± 4.1 Babc | 98.0 ± 1.2 Aa | 81.0 ± 5.5 Aa |
| 50 | 73.0 ± 4.4 Acd | 66.0 ± 5.3 Aabc | 78.0 ± 2.0 Ab | 77.0 ± 3.0 Aa |
| 100 | 61.0 ± 1.0 Ade | 57.0 ± 5.7 Abc | 70.0 ± 3.8 Abc | 82.0 ± 5.0 Aa |
| 150 | 55.0 ± 1.0 Be | 63.0 ± 1.0 Aabc | 77.0 ± 4.7 Ab | 82.0 ± 2.6 Aa |
| 200 | 55.0 ± 2.5 Ae | 51.0 ± 3.4 Ac | 69.0 ± 3.4 Abc | 79.0 ± 5.3 Aa |
| 250 | 63.0 ± 3.0 Ade | 64.0 ± 3.7 Aabc | 66.0 ± 4.2 Abc | 77.0 ± 1.9 Aa |
| 300 | 38.0 ± 4.8 Bf | 52.0 ± 2.3 Ac | 54.0 ± 10.5 Ac | 78.0 ± 4.8 Aa |
The standard error annotated by different lower-case letters among different concentration for the same seed type and metal type indicate significant differences at p < 0.05, Tukey’s post hoc test. The standard errors annotated by different higher-case letters between dimorphic seeds at the same concentration of Cu or Zn indicate significant differences at p < 0.05, Tukey’s post hoc test.
Table 3.
Effect of CuSO4 and ZnSO4 on germination index of dimorphic seeds of S. salsa.
| Concentration(mM) | CuSO4 | ZnSO4 | ||
|---|---|---|---|---|
| Brown Seed | Black Seed | Brown Seed | Black Seed | |
| 0 | 97.6 ± 0.4 Aa | 49.0 ± 2.4B Abcd | 97.4 ± 0.2 Aa | 60.9 ± 2.2 Ba |
| 0.01 | 97.8 ± 0.1 Aa | 51.0 ± 1.0B Abc | 96.5 ± 1.1 Aa | 52.6 ± 4.3 Ba |
| 0.05 | 93.5 ± 1.2 A Ab | 56.2 ± 2.8 Bab | 98.0 ± 0.4 Aa | 50.5 ± 2.4 Ba |
| 0.1 | 96.0 ± 0.7 Aa | 50.3 ± 2.3 Babc | 95.8 ± 1.0 Aa | 51.1 ± 4.1 Ba |
| 0.5 | 98.2 ± 0.1 Aa | 61.1 ± 2.5 Ba | 96.0 ± 1.1 Aa | 58.7 ± 1.6 Ba |
| 1 | 96.5 ± 1.1 Aa | 51.9 ± 5.2B Ab | 96.9 ± 1.0 Aa | 58.2 ± 4.8 Ba |
| 5 | 78.1 ± 5.2 Ac | 49.8 ± 4.6B Abc | 97.2 ± 1.1 Aa | 56.9 ± 0.9 Ba |
| 10 | 81.2 ± 3.9 Abc | 47.5 ± 3.9B Abcd | 94.9 ± 1.5 Aa | 61.0 ± 3.9 Ba |
| 50 | 70.5 ± 4.1 Acd | 44.2 ± 3.7 Bbcde | 76.4 ± 2.2 Ab | 53.0 ± 3.0 Ba |
| 100 | 56.7 ± 1 Ae | 35.4 ± 5.5 Bbcde | 68.2 ± 3.9 Abc | 57.2 ± 3.9 Aa |
| 150 | 52.0 ± 0.7 Ae | 41.3 ± 0.5 Bde | 74.5 ± 4.1 Ab | 57.5 ± 2.0 Ba |
| 200 | 52.6 ± 2.3 Ae | 33.1 ± 1.8 Bde | 66.9 ± 3.5 Abc | 50.5 ± 2.9 Ba |
| 250 | 59.0 ± 2.7 Ade | 42.6 ± 2.2 Bbcde | 63.9 ± 3.9 Abc | 50.7 ± 1.3 Ba |
| 300 | 36.2 ± 4.3 Af | 30.9 ± 1.2 Ae | 52.1 ± 10.0 Ac | 53.9 ± 2.6 Aa |
The standard errors annotated by different lower-case letters among different concentrations for the same seed type and metal type indicate significant differences at p < 0.05, Tukey’s post hoc test. The standard errors annotated by different higher-case letters between dimorphic seeds at the same concentration of Cu or Zn indicate significant differences at p < 0.05, Tukey’s post hoc test.
Table 4.
Effect of CuSO4 and ZnSO4 on the radicle tolerance index of S. salsa seedlings grown from brown and black seeds.
Table 4.
Effect of CuSO4 and ZnSO4 on the radicle tolerance index of S. salsa seedlings grown from brown and black seeds.
| Concentration (mM) | CuSO4 | ZnSO4 | ||
|---|---|---|---|---|
| Brown Seed | Black Seed | Brown Seed | Black Seed | |
| 0 | 100.00 | 100.00 | 100.00 | 100.00 |
| 0.01 | 80.33 | 81.08 | 73.40 | 97.68 |
| 0.05 | 40.53 | 63.80 | 66.88 | 83.18 |
| 0.1 | 30.65 | 45.70 | 68.61 | 70.8 |
| 0.5 | 30.66 | 34.71 | 43.82 | 48.47 |
| 1 | 24.40 | 32.26 | 35.95 | 34.83 |
| 5 | 23.77 | 29.59 | 29.53 | 30.62 |
| 10 | 15.35 | 27.62 | 26.05 | 30.73 |
| 50 | 19.25 | 18.93 | 19.68 | 27.82 |
| 100 | 18.73 | 18.79 | 17.79 | 26.07 |
| 150 | 19.52 | 16.23 | 20.62 | 26.60 |
| 200 | 18.56 | 14.04 | 18.79 | 26.06 |
| 250 | 17.91 | 14.95 | 18.91 | 23.94 |
| 300 | 19.21 | 16.32 | 20.76 | 23.03 |
Table 5.
Effect of CuSO4 and ZnSO4 on shoot tolerance index of S. salsa seedlings grown from brown and black seeds.
Table 5.
Effect of CuSO4 and ZnSO4 on shoot tolerance index of S. salsa seedlings grown from brown and black seeds.
| Concentration (mM) | CuSO4 | ZnSO4 | ||
|---|---|---|---|---|
| Brown Seed | Black Seed | Brown Seed | Black Seed | |
| 0 | 100.00 | 100.00 | 100.00 | 100.00 |
| 0.01 | 110.38 | 96.15 | 86.03 | 95.08 |
| 0.05 | 95.48 | 91.51 | 88.74 | 99.15 |
| 0.1 | 93.58 | 102.76 | 92.82 | 100.06 |
| 0.5 | 72.58 | 87.00 | 71.07 | 102.76 |
| 1 | 58.40 | 81.77 | 65.50 | 90.03 |
| 5 | 37.51 | 33.47 | 54.97 | 76.59 |
| 10 | 33.28 | 7.61 | 69.47 | 53.57 |
| 50 | 21.58 | 0.00 | 45.73 | 19.57 |
| 100 | 15.96 | 0.00 | 40.69 | 8.16 |
| 150 | 0.00 | 0.00 | 47.44 | 7.73 |
| 200 | 0.00 | 0.00 | 28.13 | 7.55 |
| 250 | 0.00 | 0.00 | 23.56 | 7.42 |
| 300 | 0.00 | 0.00 | 17.39 | 0.00 |
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MDPI and ACS Style
Zhang, H.; Jiang, L.; Tanveer, M.; Ma, J.; Zhao, Z.; Wang, L. Indexes of Radicle are Sensitive and Effective for Assessing Copper and Zinc Tolerance in Germinating Seeds of Suaeda salsa. Agriculture 2020, 10, 445. https://0-doi-org.brum.beds.ac.uk/10.3390/agriculture10100445
AMA Style
Zhang H, Jiang L, Tanveer M, Ma J, Zhao Z, Wang L. Indexes of Radicle are Sensitive and Effective for Assessing Copper and Zinc Tolerance in Germinating Seeds of Suaeda salsa. Agriculture. 2020; 10(10):445. https://0-doi-org.brum.beds.ac.uk/10.3390/agriculture10100445
Chicago/Turabian StyleZhang, Hao, Li Jiang, Mohsin Tanveer, Jinbiao Ma, Zhenyong Zhao, and Lei Wang. 2020. "Indexes of Radicle are Sensitive and Effective for Assessing Copper and Zinc Tolerance in Germinating Seeds of Suaeda salsa" Agriculture 10, no. 10: 445. https://0-doi-org.brum.beds.ac.uk/10.3390/agriculture10100445
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